Journal of Integrative Neuroscience, 2018, 17(2): 177-184 DOI: 10.31083/JIN-170048

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The gastrointestinal-brain axis in humans as an evolutionary advance of the root-leaf axis in plants: A hypothesis linking quantum effects of light to serotonin and auxin

Tonello Lucio,1,*, Gashi Bekim2, Scuotto Alessandro1, Cappello Glenda1, Cocchi Massimo1, Gabrielli Fabio1, A. Tuszynski Jack3

LUDES Foundation, Smart City, Kalkara, 1001, Malta

Department of Biology, University of Prishtina "Hasan Prishtina", Prishtina, 10000, Kosovo

Department of Physics, University of Alberta, Edmonton, Alberta, T6G 2J1, Canada

*Corresponding Author(s): luciotonello@gmail.com (Lucio Tonello)

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Copyright:  ©2018 The authors. Published by IMR press.

Abstract

Living organisms tend to find viable strategies under ambient conditions that optimize their search for, and utilization of, life-sustaining resources. For plants, a leading role in this process is performed by auxin, a plant hormone that drives morphological development, dynamics, and movement to optimize the absorption of light (through branches and leaves) and chemical "food" (through roots). Similarly to auxin in plants, serotonin seems to play an important role in higher animals, especially humans. Here, it is proposed that morphological and functional similarities between (i) plant leaves and the animal/human brain and (ii) plant roots and the animal/human gastro-intestinal tract have general features in common. Plants interact with light and use it for biological energy, whereas, neurons in the central nervous system seem to interact with biophotons and use them for proper brain function. Further, as auxin drives the "arborescence" of roots within the soil, similarly serotonin seems to facilitate enteric nervous system connectivity within the human gastrointestinal tract. This auxin/serotonin parallel suggests the root- branch axis in plants may be an evolutionary precursor to the gastrointestinal-brain axis in humans. Finally, it is hypothesized that light might be an important factor, both in gastrointestinal dynamics and brain function. Such a comparison may indicate a key role for the interaction of light and serotonin in neuronal physiology (possibly in both the central nervous system and the enteric nervous system), and according to recent work, mind and consciousness.

Keywords: Gastrointestinal-brain axis; tryptophan; serotonin; auxin; light; quantum brain model; biophotons; plants

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Tonello Lucio, Gashi Bekim, Scuotto Alessandro, Cappello Glenda, Cocchi Massimo, Gabrielli Fabio, A. Tuszynski Jack. The gastrointestinal-brain axis in humans as an evolutionary advance of the root-leaf axis in plants: A hypothesis linking quantum effects of light to serotonin and auxin. Journal of Integrative Neuroscience, 2018, 17(2): 177-184 doi:10.31083/JIN-170048

1. Introduction

According to Darwin's theory of evolution by natural selection, all organisms exhibit a tendency under ambient conditions to optimize their means of access to, and utilization of, life-sustaining resources. Considerable empirical evidence reveals that this strategy involves nutrients and other energy-giving resources (water, light, heat, shelter) as metabolism is a necessary pre-condition for life, but requires various energy-rich inputs and components for enzymatic reactions to enable such efficient utilization. As demonstrated in plants, an important leading role in pursuing such aims is played by auxin, which is a hormone produced in the stem tip that promotes cell elongation. Auxin moves to the darker side of the plant, causing the cells there to grow larger than the corresponding cells on the lighter side. It acts to drive plant growth, development of morphology, dynamics, and even their movement in order to optimize the absorption of an essential vital element: light (through branches and leaves), and "food" in the form of proper chemical substances (absorbed through roots). Comparable features and behaviors can be identified to provide parallels between plants and humans that suggest evolutionary advance inherited from ancient ancestors, retained and adapted for the needs of the human body. In particular, as does auxin in plants, serotonin seems to play a similar role in higher animals, especially humans [1,2]. Serotonin is a monoamine neurotransmitter bio-chemically derived from tryptopan, which is predominantly found in the central nervous system (CNS), the gastrointestinal (GI) tract and the blood platelets of animals, including humans. Recent findings from different lines of research newly suggest the possibility of common strategies developed by both plants and humans that may be understood through their shared remote ancestry. In particular, morphological and functional similarities between plant leaves and animal/human brain, as well as plant roots and animal/human GI can be outlined in terms of general morphological and functional features.

Pertinent to this connection, the following questions are proposed: given a parallel between serotonin in animals and auxin in plants, could light and food be factors playing similar roles in plants and humans, respectively? Is it plausible that the root-leaf axis is the evolutionary ancestor of the GI-brain axis? The latter has been the subject of keen research interest in recent years. However, to the best of the authors knowledge, virtually no attention has been given to a possible root-leaf axis in plants. In a recent paper, Mender [3] drew attention to the parallel between quantum phenomena involved in plant and algae photosynthetic processes on the one hand and consciousness in the human brain on the other hand. He noted that energy harvesting by photosynthesis in plants could be viewed as a precursor to complex quantum process powering neural correlates of human consciousness. In the present paper a direct parallel between the specific mechanisms involving the root-leaf axis in plants and the GI-brain axis in humans is elaborated. With such a parallel, the reader's attention is drawn to this idea which here is elaborated as a hypothesis that possibly concerns such a relatable array of conjectures.

2. A plant-human comparison

One of the fundamental aspects of plant survival is its light absorption capability, since light is a primary source of living energy on our planet driving the photosynthesis that propels plant growth. Plants then become sources of food for higher organisms in a food chain that eventually terminates with the human consumption of both plants and animals for survival. Light has another fundamental role in the Plant Kingdom: it not only provides energy for photosynthesis but also transmits reliable information, mainly regarding local environmental conditions. Light intensity, and the direction it comes from, informs a plant that absorbs it about its immediate environment. Light may blocked or its intensity reduced depending upon the distribution and density of organic and inorganic materials surrounding a given plant. Recently, it has been convincingly and realistically hypothesized that plants could have developed a form of primitive vision ability allowing them to receive and process large amounts of information provided by light [4, 5]. Furthermore, light interaction with auxin, elicits local responses as well as long-distance signalling. Light coordinates growth between the shoot and the root and affects plants from roots to leaves by modulating their growth and development [6,7]. To expand on this Halliday et al. [7]is quoted: "Light imposes a strong influence on multiple facets of the auxin system, controlling auxin levels, transport, and responsiveness}". In particular, "light triggers auxin synthesis in developing young leaves… whereas auxin transported to the root is required for lateral root emergence and primary root elongation". Supplementary to the above references, there is strong light-auxin interaction in terms of light intensity affecting auxin levels, which is turn coordinates development between the shoot and the roots, manipulating plant growth in order to tune and adapt a plant to its light environment. Such interactions appear to be the basis of plant plasticity [8].

It is apparent that the dynamics generated by light-auxin interactions seems to involve phytochrome. For example, in Arabidopsis, the mechanism may be linked to phytochrome A and B. These enzymes can impose a strong influence on auxin levels in plants, by acting through tryptophan metabolism enzymes (SUR2 and TAA1) and, as a feedback mechanism working on available auxin, transcriptionally regulating several enzymes encoding genes (GH3 family) as reported by Franklin and Whitelam [9] and Halliday et al. [7]. Further, the role of light is involved with both the distribution of auxin from shoot to root and its flux. Light pathways may modify auxin distribution by controlling the abundance of auxin efflux carriers such as PIN-FORMED proteins and p-glycoproteins of the ATP-binding cassette family B (ABCB) transporter molecules, through phytochromes and, probably also, cryptochromes.

Furthermore, light moderates sensitivity to auxin within the cell by imposing control on the nuclear auxin response pathway. It can dampen or amplify the response to auxin and thus regulate signal transduction such that light can target responses at specific locations in the plant.

Interestingly, light and auxin seem to have common gene targets. In fact, at the molecular level, auxin activates the transcription of three gene families: Aux/IAA, SAUR, and GH3. Several studies [7,9,10,11,12,13,14] suggest that light (through phytochrome) seems to be involved in regulating the expression of several of the same genes belonging to the gene families: Aux/IAA, SAUR, and GH3. There are a number of transcription factor convergence points that enable the coordinated regulation of genes by light and auxin.

3. Branches, leaves and brain neurons

Auxin is the main factor involved in the optimization of light capture by leaves [6,7], thus it can play out different strategies such as directly driving plant growth, its morphology, and dynamics, from shape, via branch structure and arborescence, to the arrangement of leaves, and even their "movement". For instance, the turning of the leaf toward the direction of light, its source of energy, depends upon the rearrangement of the cytoskeleton inside the cells of leaves through a mechanism directly involving auxin [1,6,7].The actions of auxin in plants strongly resembles the well-known actions of serotonin in neuronal development and adult neuroplasticity in mammals [15,16]. Strong evidence indicates that serotonin performs a major driving role in neuronal morphology and dynamics [17,18,19].

Accordingly, comparable to the way in which auxin strongly affects the structure of branches and leaves (to optimize photosynthesis oriented light absorption) so in animals/humans, serotonin strongly influences the morphology of neurons involved in CNS neuronal networking. Moreover, auxin and serotonin have biochemical structural properties in common and hence exhibit some analogous biological functions. Biochemically, they are both tryptophan metabolites, they have a very similar molecular structure and hence similar chemical and physical properties as argued above and in the references cited there. Unsurprisingly, this strongly suggests that auxins perform similar functions in plants and animals. Therefore, the following questions arise: In analogy to auxin in plants, is it possible that there is a type of “light interaction” in the CNS, involving serotonin and neuronal development and morphology? Is there a neuronal equivalent to arborescence, in analogy to that exhibited by the branches and leaves of plants? Would this mechanism involve neurons interacting with light or even actively searching for light or doing something similar? Are there any other possible similarities and what might their roles be?

A growing body of evidence supports the idea of the involvement of biophotons within the inner workings of the human brain. Several possible ways of interaction with neurons have been suggested and they indicate that photons may play a key role in neural information processing, electromagnetic signalling, and may be involved in quantum mechanical brain mechanisms, as elaborated on in several recent reports [20,21,22,23]. In particular, mitochondria and microtubules in neurons as well as myelinated axons have been hypothesized to serve as photonic waveguides [24,25,26,27]. Also, it has been shown that glutamate (which is by far the most abundant neurotransmitter molecule in the nervous systems of vertebrates—on the basis of its involvement in over 90% of synaptic connections in the human brain) could induce biophotonic activities and transmission in neural circuits [28].

Hence, in human brain, neurons seem to interact with biophotons, which are light quanta spanning the near-UV to near-IR frequency range. In an analogous manner to plants, which interact with light and use it for biological energy, it is feasible that neurons are able to interact with photons as explained in detail by Kumar et al. [24]. While as of yet there are no experimentally documented specific functions of biophotons in the brain, the speed and precise nature of photon-receptor interactions offer an attractive mechanism that evolutionary exploration could have found of use for in optimizing brain function, for example, in the coordination and synchronization of cognitive functions. Future studies should be directed toward addressing specific roles for biophotons in the brain. It is reasonable to expect that a biological organ such as the brain, which operates at great efficiency using electrical signals involving action potentials, also uses electromagnetic signals that could provide an independent channel of communication [29]. A double comparison between plant leaves and animal neurons can be summed up as follows: they both use auxin/serotonin, they both interact with light. Is this an accidental coincidence or is this correlation significant from an evolutionary perspective?

It has even been suggested that interactions of neurons with biophotons could be a fundamental element involved in the emergence of cognitive abilities or even the basis for consciousness [2,30]. Therefore, since the auxin interaction with light is a driving force in plants providing a mechanism for the optimization of biological energy absorption and utilization, serotonin and biophotons could drive neurons in order to organize an active "mind" or be a spark that ignites "consciousness". This is, of course, a bold and unproven hypothesis with a somewhat provocative intent, which we hope will generate a robust debate in the research community.

4. Roots and the gastrointestinal tract

The fundamental element for plant survival is their "food" intake, represented by water, nitrogen and important minerals and micronutrient compounds searched for and captured by roots. Plants can send their roots deep into the soil to capture what is needed and, as in the case of leaves, above ground to search for optimal light exposure. Movement performed underground by roots depends upon auxin [31]. Thus, auxin controls and steers root growth, plasticity, and movement so as to optimize "food" search and absorption.

Is there a similar behavior applicable to animal/human physiology, possibly driven once again by serotonin? What about the GI? Serotonin's role in the GI has been very well studied. Among several suggested aims and functions involving it, a most interesting one is linked to the Enteric Nervous System (ENS), a neural network located in the GI. In fact, serotonin has been observed to stimulate stem cells to divide and give rise to new neurons of the ENS even in adult animals [32]. Its ability appears to be essential for post-natal and adult health. Enteric neuronal serotonin affects growth/maintenance of the ENS in terms of neurogenesis (as well as intestinal mucosa) [33,34]. Moreover, the ability of serotoninergic neurons to sculpt the ENS potentially enables environmental stimuli that alter the activity of serotoninergic neurons to produce long-lasting changes in the structure and function of the ENS [35]. Hence, as auxin drives "arborescence" of the roots for plants inside the soil, so too does serotonin appear to lead the wiring of ENS neurons in the human GI?

It is well known that the action of auxin on plant roots is clearly oriented toward the search for and intake of food. These processes include information transmission regarding environmental conditions and this process is hypothesized to involve feedback loops for back-and-forth information transmission. What is known about ENS function with analogous properties to those of the auxin-root system? The ENS is exposed to, and interacts with, the outer (microbiota, metabolites, and nutrients) and inner (immune cells and stromal cells) microenvironment of the GI. Moreover, two types of enteric neuron send signals: Some of which densely innervate intestinal villi and detect food, while others target stomach and intestinal muscle and sense stretch [36,37].

A clear comparison between plant roots and the animal (human in particular) GI (ENS) seems to involve the following properties. They both use auxin/serotonin for their organization and functionality as well as for information transmission. Also, they both work in order to optimize food intake and absorption interacting with substance of the outside world in a similar way. Moreover, they both need the presence of symbiotic bacteria for their performance: these bacteria belong, above all, to philum Firmicutes, particularly to the class Clostridida [38,39]. Then again from the morphological point of view, the spatial geometry of roots and the GI seems to be similar. In particular, it is easy to recognize fractal structures in the roots of plants [40] as well as in the animal/human GI, the ENS in particular [41]. From this perspective, at least for some elements, the ENS clearly mimics and directly resembles the role, function, and dynamics of the corresponding properties of plant roots.

5. An evolutionary aspect

Interestingly, auxin is linked to leaves and roots in plants just as, in humans; serotonin is linked with the brain neurons in the CNS and with the GI neurons in the ENS, respectively. Given this connection the peculiar role of the neuron as a serotonin-coupled cell should be stressed in the plant-human comparison. Notably, the morphology of roots resemble GI morphology, from the fractal perspective, ENS neurons in particular. Interestingly, also leaves, branches, and canopies follow fractal geometry development [42] as well as brain neuron arborescence [43]. It is well known that such a geometry is widespread in nature to have maximize capillary penetration, provide wide diffusion, and optimize exchange surfaces (e.g. think of the structure of the lung) [41,44,45].

Azmitia [1] claims that one of the serotonin (and similar compounds') roles in plants and humans seems to be driving cells "in order to tract the source of relevant stimuli". As mentioned above, the role of auxin in plants is its interaction with light in the case of leaves and the search for food in the case of roots. In the same way, the role of serotonin in the human body could be hypothesized to interact with light (in the form of internally generated biophotons) in the brain and to search for food in the GI. Consequently, the auxin/serotonin parallel suggests a comparison between what could be somehow called the root-branches axis in plants as the ancient precursors of the GI-brain axis (GBA) in humans (see Fig.1).

Fig. 1.

Fig. 1.   An illustration of the roles of auxin in plants and serotonin in humans. Auxin is linked to leaves and roots in plants just as serotonin in humans is linked to brain neurons (CNS) and with GI neurons (ENS), respectively. Both auxin and serotonin interact with light, the former through branches and leaves, the latter through the CNS. On the other hand, auxin and serotonin interact with food, the former through roots, the latter through the ENS.


It should be noted that in humans, serotonin synthesis from tryptophan uses TPH (tryptophan hydroxylase) enzymes and two separate types of TPH are known: TPH1 and TPH2. The first is located in non-brain tissue and it is responsible for producing most of the serotonin found in the body, including the blood [46]. Alternatively, TPH2 is entirely restricted to neurons of the raphe nuclei and the ENS and is the enzyme responsible for producing all of the serotonin in the brain and in the ENS [47]. So, interestingly, the serotonin of the brain and of the ENS are both synthesized through a common enzyme, TPH2 (different from the serotonin available in the rest of the body available through the TPH1 synthesis), thus suggesting, once again, a possible common root. In other words, the GBA could be seen as an evolution of the dynamics of branches (leaves) and roots because of the similar aim and function of the common family of compounds, the tryptophan metabolites, i.e. serotonin and auxin.

Hence, in terms of the retention and refinement of evolutionary advances, the hypothesis is based on the lines of reasoning presented above, suggesting that the human GI could be seen as playing an analogous role to that of the root of a plant. The evolutionary step that comprised the acquisition of great movement ability (e.g. crawling, walking, and running) gained by animals in general and humans in particular, also necessitated a means for making access to their food sources "portable". Animals had somehow to take with them a "piece" of the earth in order to find vital nutrition elements "on the go." Therefore, evolution may have led to the generation of a food container (the gastro-intestinal tract) that can be carried along with the now mobile living systems (animals).

From this perspective, what could be the evolutionary meaning of brain neurons in humans? They have been compared to plant leaves but branches and leaves are in the open air, neurons are not. In humans, such "open air" has been enclosed in the skull. Therefore, the head of an animal can be viewed within the same evolutionary point of view as a parallel to the open environment of a plant. However, the skull confines and isolates the animal's brain and prevents most of the externally generated photons from reaching the brain's neurons. Nonetheless, the parallel between neurons and leaves is not entirely lost due to the fact that the skull encloses the brain. While the source of light for a plant is the sun, the source of biophotons is not external, but produced within brain cells as a byproduct of metabolism. In fact, possible sources of biophotons have been identified as the result of mitochondrial respiration [48, 49] or lipid oxidation [50,51]. Nevertheless, miniature photon-producing version of the sun may be present within us. In this sense, our head may be interpreted as a luminous environment, made "portable", and evolved to become self-illuminated.

6. Discussion

The proposed scenario reported here suggests light as the main factor affecting the function of leaves in plants in terms of capturing sunlight and storing its energy, and equally an important factor for human neurons in terms of biophotons and their utilization in cognitive processes and possibly playing a crucial role in consciousness.

At the same time, it has been well known for decades that light influences the growth and development of roots [52,53,54]. In a recent paper, Lee et al. [55] show that in plants, Arabidopsis thaliana in particular, "light also influences root growth and development". Specifically, they demonstrated that "light was efficiently conducted through the stems to the roots", and that "underground roots directly sense stem-piped light to monitor the aboveground light environment".

In view of the above arguments, if the human CNS is similar to plant leaves in terms of light behavior, and if neurons of the CNS and neurons of the ENS are similar with the ENS being similar to plants root, then it seems reasonable that the ENS should be involved in light-oriented dynamics. Strictly speaking, this hypothesis suggests that light could be an important factor in the brain and in GI dynamics, whose interactions may play a role similar to that played by the root-leaf axis in plants, i.e. as a messenger of the "environmental light" condition. Thus, according to what is proposed above, in humans the "environmental light" is represented by brain biophotons so, a possible hypothesis is that "human light" could be a messenger within the GI-brain axis. It is our contention that at the very least biophoton involvement in the ENS should be seriously considered.

It has been described that auxin plays a fundamental role in plants, from roots to leaves. At the same time, it has been shown that a parallel role seems to be played by serotonin in humans, from the GI to brain. In order to perform its tasks, auxin interacts with light. On the other hand, in humans, serotonin seems to be involved in neuron dynamics, development and behavior but it still remains unknown as to what its possible interaction with light mat be (beyond its known involvement in the activation of enzymatic conversion of 5-hydroxytryptophan to serotonin [56] and in other physiological processes [57]). In other words, we have argued that in humans serotonin and light are involved in similar cellular processes, which could be used for the same purposes and could be playing similar roles. However, in the absence of the crucial experimental demonstration of biophoton generation and utilization in the brain, what specific mechanisms are involved in these interactions still remains to be determined.

In an earlier article it was proposed a possible quantum interaction may be based on the presence of an indole ring within the serotonin molecule Tonello et al. [2] but the suggested mechanism, while feasible, remains no more than conjecture. Nonetheless, the plant/human comparison seems to strongly suggest the key role of the interaction between light and serotonin as a fundamental element for insight into neuron physiology (maybe both in the CNS and ENS). Such an understanding may lead to the unlocking of the mysteries of the mind and consciousness. It is worth noting that "Fluorescent and absorbing substances should interfere with such a biophoton communication system. Of all natural amino acids, nature has chosen the aromatic ones with the strongest fluorescence, tryptophan, phenylalanine and tyrosine as precursors for the neurotransmitters involved in mood reactions: serotonin, dopamine and norepinephrine" [23].

Unfortunately, in plants, things are not as clear. Halliday et al. [7] claim that "Although researchers have uncovered many examples of light and auxin signal integration, the future challenge is now to generate a model of the light-auxin network, with spatial and temporal resolution, that can predict plant behavior in response to environmental light stimuli". It appears as a final conjecture that a better understanding of the auxin-light interaction could also lead to a better understanding of the cognitive mechanisms taking place in the brain by opening a new line of investigations focused on the electromagnetic interactions involving biomolecules such as auxin, in addition to the well-studied electric signalling via action potentials and chemical signalling via neurotransmitters. The subtleness of electromagnetic interactions and their precise coupling to molecular absorption due to resonance effects offer numerous advantages and could explain a number of enigmatic features of the human mind [58].

Acknowledgments

LT thanks Prof. Claudio Morellato for his lifelong priceless teachings. JAT thanks NSERC (Canada) for funding his research.

Conflict of Interest

All authors declare no conflicts of interest.

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Tepperman JM, Zhu T, Chang H-S, Wang X, Quail PH ( 2001)

Multiple transcription-factor genes are early targets of phytochrome A signaling

Proceedings of the National Academy of Sciences 98(16), 9437-9442.

DOI:10.1073/pnas.161300998      URL     [Cited within: 1]

Devlin PF, Yanovsky MJ, Kay SA ( 2003)

A genomic analysis of the shade avoidance response in Arabidopsis

Plant Physiology 133(4), 1617-1629.

DOI:10.1104/pp.103.034397      URL     PMID:14645734      [Cited within: 1]

Plants respond to the proximity of neighboring vegetation by elongating to prevent shading. Red-depleted light reflected from neighboring vegetation triggers a shade avoidance response leading to a dramatic change in plant architecture. These changes in light quality are detected by the phytochrome family of photoreceptors. We analyzed global changes in gene expression over time in wild-type, phyB mutant, and phyA phyB double mutant seedlings of Arabidopsis in response to simulated shade. Using pattern fitting software, we identified 301 genes as shade responsive with patterns of expression corresponding to one of various physiological response modes. A requirement for a consistent pattern of expression across 12 chips in this way allowed more subtle changes in gene expression to be considered meaningful. A number of previously characterized genes involved in light and hormone signaling were identified as shade responsive, as well as several putative, novel shade-specific signal transduction factors. In addition, changes in expression of genes in a range of pathways associated with elongation growth and stress responses were observed. The majority of shade-responsive genes demonstrated antagonistic regulation by phyA and phyB in response to shade following the pattern of many physiological responses. An analysis of promoter elements of genes regulated in this way identified conserved promoter motifs potentially important in shade regulation.

Carabelli M, Possenti M, Sessa G, Ciolfi A, Sassi M, Morelli G, Ruberti I ( 2007)

Canopy shade causes a rapid and transient arrest in leaf development through auxin-induced cytokinin oxidase activity

Genes & Development 21(15), 1863-1868.

DOI:10.1101/gad.432607      URL     PMID:17671088      [Cited within: 1]

Abstract A plant grown under canopies perceives the reduction in the ratio of red (R) to far-red (FR) light as a warning of competition, and enhances elongation growth in an attempt to overgrow its neighbors. Here, we report that the same low R/FR signal that induces hypocotyl elongation also triggers a rapid arrest of leaf primordium growth, ensuring that plant resources are redirected into extension growth. The growth arrest induced by low R/FR depends on auxin-induced cytokinin breakdown in incipient vein cells of developing primordia, thus demonstrating the existence of a previously unrecognized regulatory circuit underlying plant response to canopy shade.

Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ ( 2008)

Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants

Cell 133(1), 164-176.

DOI:10.1016/j.cell.2008.01.049      URL     PMID:18394996      [Cited within: 1]

Plants grown at high densities perceive a decrease in the red to far-red (R:FR) ratio of incoming light, resulting from absorption of red light by canopy leaves and reflection of far-red light from neighboring plants. These changes in light quality trigger a series of responses known collectively as the shade avoidance syndrome. During shade avoidance, stems elongate at the expense of leaf and storage organ expansion, branching is inhibited, and flowering is accelerated. We identified several loci in Arabidopsis, mutations in which lead to plants defective in multiple shade avoidance responses. Here we describe TAA1, an aminotransferase, and show that TAA1 catalyzes the formation of indole-3-pyruvic acid (IPA) from L-tryptophan (L-Trp), the first step in a previously proposed, but uncharacterized, auxin biosynthetic pathway. This pathway is rapidly deployed to synthesize auxin at the high levels required to initiate the multiple changes in body plan associated with shade avoidance.

Turlejski K ( 1996)

Evolutionary ancient roles of serotonin: long-lasting regulation of activity and development

Acta Neurobiologiae Experimentalis 56, 619-636.

URL     PMID:8768313      [Cited within: 1]

Biogenic monoamines (catecholamines, indoleamines and histamine) are evolutionary old and important modulators of long-lasting changes in the functional state of cells. They are found in many protozoans and in almost all metazoans. Monoamines preserve their evolutionary old functions (first of all being intracellular signals and later hormones and growth factors) even in those animals in which they acquired the function of neurotransmitter. The older functions of serotonin, an important member of the family of indoleamines, are reviewed here. Described are: presence of serotonin in organisms at various phylogenetic levels; its role in embryonal, foetal and postnatal development, especially in the development of the central nervous system. It is concluded that in none of these functions serotonin is the only factor, but it is an ubiquitous and important modulator of a vast array of processes and functions taking part in development and plasticity.

Azmitia EC ( 1999)

Serotonin neurons, neuroplasticity, and homeostasis of neural tissue

Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 21(1), 33S-45S.

DOI:10.1016/S0893-133X(99)00022-6      URL     PMID:10432487      [Cited within: 1]

Homeostasis is the process by which the internal milieu of the body is able to maintain equilibrium in the face of constant insults from the external world. Endocrine, immune, and vascular systems play pivotal roles in adjusting internal biochemical reactions to counteract assaults from the outside. Despite the vast accumulation of data over the last 50 years, a role for serotonin in brain homeostasis has not been proposed. In this chapter I will review the plasticity and anatomy of serotonergic neurons in integrating external sensory and motor systems as well as internal endocrine, glial and vascular signals with the various cellular elements comprising neural tissue. Steroids and neuropeptides have both been shown to alter the morphology of serotonergic neurons. In turn, alterations in serotonin levels in the adult brain can change the morphology of its target cells. A pivotal role for serotonin in the homeostasis of neural tissue is consistent with the function of serotonin throughout evolution and explains the large number of biological systems, behavioral activities, and clinical diseases associated with serotonergic neurons.

Wirth A, Holst K, Ponimaskin E ( 2017)

How serotonin receptors regulate morphogenic signalling in neurons

Progress in Neurobiology 151, 35-56.

DOI:10.1016/j.pneurobio.2016.03.007      URL     PMID:27013076      [Cited within: 1]

Serotonin (5-hydroxytrympamine or 5-HT) is one of the phylogenetically oldest neurotransmitters, and the serotonergic system is among the earliest developed neuronal systems. Serotonin is critically involved in regulating multiple physiological functions, acting via a heterogenic receptor family that includes G protein-coupled receptors and ligand-gated ion channels. Although serotonergic neurons comprise a widely distributed and complex network that targets nearly every brain structure, serotonin-mediated signalling is under strict temporal and spatial control. Imbalance in serotonergic signalling is implicated in many pathophysiological conditions, including schizophrenia, Alzheimer's disease, depression, and anxiety. In addition to its well-established role as a neurotransmitter, serotonin is involved in many aspects of neural development, including neurite outgrowth, somatic morphology regulation, growth cone motility, synaptogenesis, and control of dendritic spine shape and density. The morphogenic effects of serotonin are developmentally regulated, and serotonin availability during sensitive developmental stages can modulate the formation and functions of behaviourally relevant neuronal networks in adulthood. Here we provide an overview of the molecular mechanisms responsible for the morphogenic effects of serotonin elicited by its different receptors in neurons. We also discuss the role of serotonin receptor-mediated morphogenic signalling in the development and maintenance of pathophysiological conditions.

Speranza L, Labus J, Volpicelli F, Guseva D, Lacivita E, Leopoldo M, Bellenchi GC, di Porzio U, Bijata M, Perrone-Capano C ( 2017)

Serotonin 5-HT 7 receptor increases the density of dendritic spines and facilitates synaptogenesis in forebrain neurons

Journal of Neurochemistry 141(5), 647-661.

DOI:10.1111/jnc.13962      URL     PMID:28122114      [Cited within: 1]

Abstract Precise control of dendritic spine density and synapse formation is critical for normal and pathological brain functions. Therefore, signaling pathways influencing dendrite outgrowth and remodeling remain a subject of extensive investigations. Here we report that prolonged activation of the serotonin 5-HT7 receptor (5-HT7R) with selective agonist LP-211 promotes formation of dendritic spines and facilitates synaptogenesis in postnatal cortical and striatal neurons. Critical role of 5-HT7R in neuronal morphogenesis was confirmed by analysis of neurons isolated from 5-HT7R-deficient mice and by pharmacological inactivation of the receptor. Acute activation of 5-HT7R results in pronounced neurite elongation in postnatal striatal and cortical neurons, thus extending previous data on the morphogenic role of 5-HT7R in embryonic and hippocampal neurons. We also observed decreased number of spines in neurons with either genetically (i.e. 5-HT7R-KO) or pharmacologically (i.e. antagonist treatment) blocked 5-HT7R, suggesting that constitutive 5-HT7R activity is critically involved in the spinogenesis. Moreover, cyclin-dependent kinase 5 (Cdk5) and small GTPase Cdc42 were identified as important downstream effectors mediating morphogenic effects of 5-HT7R in neurons. Altogether, our data suggest that the 5-HT7R-mediated structural reorganization during the postnatal development might have a crucial role for the development and plasticity of forebrain areas such as cortex and striatum, and thereby can be implicated in regulation of the higher cognitive functions. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.

Fernandez SP, Muzerelle A, Scotto-Lomassese S, Barik J, Gruart A, Delgado-García JM, Gaspar P ( 2017)

Constitutive and acquired serotonin deficiency alters memory and hippocampal synaptic plasticity

Neuropsychopharmacology 42(2), 512.

DOI:10.1038/npp.2016.134      URL     PMID:27461084      [Cited within: 1]

Abstract Serotonin (5-HT) deficiency occurs in a number of brain disorders that affect cognitive function. However, a direct causal relationship between 5-HT hypo-transmission and memory and underlying mechanisms has not been established. We used mice with a constitutive depletion of 5-HT brain levels (Pet1KO mice) to analyze the contribution of 5-HT to different forms of learning and memory. Pet1KO mice exhibited a striking deficit in novel object recognition memory, a hippocampal-dependent task. No alterations were found in tasks for social recognition, procedural learning, or fear memory. Viral delivery of designer receptors exclusively activated by designer drugs was used to selectively silence the activity of 5-HT neurons in the raphe. Inhibition of 5-HT neurons in the median raphe, but not the dorsal raphe, was sufficient to impair object recognition in adult mice. In vivo electrophysiology in behaving mice showed that long-term potentiation in the hippocampus of 5-HT-deficient mice was altered, and administration of the 5-HT1A agonist 8-OHDPAT rescued the memory deficits. Our data suggest that hyposerotonergia selectively affects declarative hippocampal-dependent memory. Serotonergic projections from the median raphe are necessary to regulate object memory and hippocampal synaptic plasticity processes, through an inhibitory control mediated by 5-HT1A receptors.

Costa J, Dotta B, Persinger M ( 2016)

Lagged coherence of photon emissions and spectral power densities between the cerebral hemispheres of human subjects during rest conditions: Phase shift and quantum possibilities

World Journal of Neuroscience 6(2), 119.

DOI:10.4236/wjns.2016.62015      URL     [Cited within: 1]

Tang R, Dai J ( 2014)

Biophoton signal transmission and processing in the brain

Journal of Photochemistry and Photobiology B: Biology 139, 71-75.

DOI:10.1016/j.jphotobiol.2013.12.008      URL     PMID:24461927      [Cited within: 1]

The transmission and processing of neural information in the nervous system plays a key role in neural functions. It is well accepted that neural communication is mediated by bioelectricity and chemical molecules via the processes called bioelectrical and chemical transmission, respectively. Indeed, the traditional theories seem to give valuable explanations for the basic functions of the nervous system, but difficult to construct general accepted concepts or principles to provide reasonable explanations of higher brain functions and mental activities, such as perception, learning and memory, emotion and consciousness. Therefore, many unanswered questions and debates over the neural encoding and mechanisms of neuronal networks remain. Cell to cell communication by biophotons, also called ultra-weak photon emissions, has been demonstrated in several plants, bacteria and certain animal cells. Recently, both experimental evidence and theoretical speculation have suggested that biophotons may play a potential role in neural signal transmission and processing, contributing to the understanding of the high functions of nervous system. In this paper, we review the relevant experimental findings and discuss the possible underlying mechanisms of biophoton signal transmission and processing in the nervous system.

Schwartz JM, Stapp HP, Beauregard M ( 2005)

Quantum physics in neuroscience and psychology: a neurophysical model of mind-brain interaction

Philosophical Transactions of the Royal Society of London B: Biological Sciences 360(1458), 1309-1327.

DOI:10.1098/rstb.2004.1598      URL     PMID:16147524      [Cited within: 1]

Neuropsychological research on the neural basis of behaviour generally posits that brain mechanisms will ultimately suffice to explain all psychologically described phenomena. This assumption stems from the idea that the brain is made up entirely of material particles and fields, and that all causal mechanisms relevant to neuroscience can therefore be formulated solely in terms of properties of these elements. Thus, terms having intrinsic mentalistic and/or experiential content (e.g. 'feeling', 'knowing' and 'effort') are not included as primary causal factors. This theoretical restriction is motivated primarily by ideas about the natural world that have been known to be fundamentally incorrect for more than three-quarters of a century. Contemporary basic physical theory differs profoundly from classic physics on the important matter of how the consciousness of human agents enters into the structure of empirical phenomena. The new principles contradict the older idea that local mechanical processes alone can account for the structure of all observed empirical data. Contemporary physical theory brings directly and irreducibly into the overall causal structure certain psychologically described choices made by human agents about how they will act. This key development in basic physical theory is applicable to neuroscience, and it provides neuroscientists and psychologists with an alternative conceptual framework for describing neural processes. Indeed, owing to certain structural features of ion channels critical to synaptic function, contemporary physical theory must in principle be used when analysing human brain dynamics. The new framework, unlike its classic-physics-based predecessor, is erected directly upon, and is compatible with, the prevailing principles of physics. It is able to represent more adequately than classic concepts the neuroplastic mechanisms relevant to the growing number of empirical studies of the capacity of directed attention and mental effort to systematically alter brain function.

Grass F, Klima H, Kasper S ( 2004)

Biophotons, microtubules and CNS, is our brain a “Holographic computer”?

Medical Hypotheses 62(2), 169-172.

DOI:10.1016/S0306-9877(03)00308-6      URL     PMID:14962620      [Cited within: 2]

Several experiments show that there is a cell to cell communication by light in different cell types. This article describes theoretical mechanisms and subcellular structures that could be involved in this phenomenon. Special consideration is given to the nervous system, since it would have excellent conditions for such mechanisms. Neurons are large colourless cells with wide arborisations, have an active metabolism generating photons, contain little pigment, and have a prominent cytoskeleton consisting of hollow microtubules. As brain and spinal cord are protected from environmental light by bone and connective tissue, the signal to noise ratio should be high for photons as signal. Fluorescent and absorbing substances should interfere with such a communication system. Of all biogenic amines nature has chosen the ones with the strongest fluorescence as neurotransmitters for mood reactions: serotonin, dopamine and norepinephrine. If these mechanisms are of relevance our brain would have to be looked upon as a “holographic computer”.

Scholkmann F ( 2016)

Long range physical cell-to-cell signalling via mitochondria inside membrane nanotubes: a hypothesis

Theoretical Biology and Medical Modelling 13(1), 16.

DOI:10.1186/s12976-016-0042-5      URL     PMID:4896004      [Cited within: 2]

Coordinated interaction of single cells by cell-to-cell communication (signalling) enables complex behaviour necessary for the functioning of multicellular organisms. A quite newly discovered cell-to-cell signalling mechanism relies on nanotubular cell-co-cell connections, termed “membrane nanotubes” (MNTs). The present paper presents the hypothesis that mitochondria inside MNTs can form a connected structure (mitochondrial network) which enables the exchange of energy and signals between cells. It is proposed that two modes of energy and signal transmission may occur: electrical/electrochemical and electromagnetic (optical). Experimental work supporting the hypothesis is reviewed, and suggestions for future research regarding the discussed topic are given.

Kumar S, Boone K, Tuszynski J, Barclay P, Simon C ( 2016)

Possible existence of optical communication channels in the brain

Scientific Reports 6, 36508.

DOI:10.1038/srep36508      URL     PMID:5098150      [Cited within: 1]

Abstract Given that many fundamental questions in neuroscience are still open, it seems pertinent to explore whether the brain might use other physical modalities than the ones that have been discovered so far. In particular it is well established that neurons can emit photons, which prompts the question whether these biophotons could serve as signals between neurons, in addition to the well-known electro-chemical signals. For such communication to be targeted, the photons would need to travel in waveguides. Here we show, based on detailed theoretical modeling, that myelinated axons could serve as photonic waveguides, taking into account realistic optical imperfections. We propose experiments, both in vivo and in vitro, to test our hypothesis. We discuss the implications of our results, including the question whether photons could mediate long-range quantum entanglement in the brain.

Rahnama M, Tuszynski JA, Bokkon I, Cifra M, Sardar P, Salari V ( 2011)

Emission of mitochondrial biophotons and their effect on electrical activity of membrane via microtubules

Journal of Integrative Neuroscience 10(1), 65-88.

DOI:10.1142/S0219635211002622      URL     PMID:21425483      [Cited within: 1]

In this paper we argue that, in addition to electrical and chemical signals propagating in the neurons of the brain, signal propagation takes place in the form of biophoton production. This statement is supported by recent experimental confirmation of photon guiding properties of a single neuron. We have investigated the interaction of mitochondrial biophotons with microtubules from a quantum mechanical point of view. Our theoretical analysis indicates that the interaction of biophotons and microtubules causes transitions/fluctuations of microtubules between coherent and incoherent states. A significant relationship between the fluctuation function of microtubules and alpha-EEG diagrams is elaborated on in this paper. We argue that the role of biophotons in the brain merits special attention.

Jibu M, Hagan S, Hameroff SR, Pribram KH, Yasue K ( 1994)

Quantum optical coherence in cytoskeletal microtubules: implications for brain function

Biosystems 32(3), 195-209.

DOI:10.1016/0303-2647(94)90043-4      URL     PMID:7919117      [Cited within: 1]

‘Laser-like,' long-range coherent quantum phenomena may occur biologically within cytoskeletal microtubules. This paper presents a theoretical prediction of the occurrence in biological media of the phenomena which we term ‘superradiance' and ‘self-induced transparency'. Interactions between the electric dipole field of water molecules confined within the hollow core of microtubules and the quantized electromagnetic radiation field are considered, and microtubules are theorized to play the roles of non-linear coherent optical devices. Superradiance is a specific quantum mechanical ordering phenomenon with characteristic times much shorter than those of thermal interaction. Consequently, optical signalling (and computation) in microtubules would be free from both thermal noise and loss. Superradiant optical computing in networks of microtubules and other cytoskeletal structures may provide a basis for biomolecular cognition and a substrate for consciousness.

Tang R, Dai J ( 2014)

Spatiotemporal imaging of glutamate-induced biophotonic activities and transmission in neural circuits

PloS one 9(1), e85643.

DOI:10.1371/journal.pone.0085643      URL     PMID:24454909      [Cited within: 1]

The processing of neural information in neural circuits plays key roles in neural functions. Biophotons, also called ultra-weak photon emissions (UPE), may play potential roles in neural signal transmission, contributing to the understanding of the high functions of nervous system such as vision, learning and memory, cognition and consciousness. However, the experimental analysis of biophotonic activities (emissions) in neural circuits has been hampered due to technical limitations. Here by developing and optimizing an in vitro biophoton imaging method, we characterize the spatiotemporal biophotonic activities and transmission in mouse brain slices. We show that the long-lasting application of glutamate to coronal brain slices produces a gradual and significant increase of biophotonic activities and achieves the maximal effect within approximately 90 min, which then lasts for a relatively long time (>200 min). The initiation and/or maintenance of biophotonic activities by glutamate can be significantly blocked by oxygen and glucose deprivation, together with the application of a cytochrome c oxidase inhibitor (sodium azide), but only partly by an action potential inhibitor (TTX), an anesthetic (procaine), or the removal of intracellular and extracellular Ca2+. We also show that the detected biophotonic activities in the corpus callosum and thalamus in sagittal brain slices mostly originate from axons or axonal terminals of cortical projection neurons, and that the hyperphosphorylation of microtubule-associated protein tau leads to a significant decrease of biophotonic activities in these two areas. Furthermore, the application of glutamate in the hippocampal dentate gyrus results in increased biophotonic activities in its intrahippocampal projection areas. These results suggest that the glutamate-induced biophotonic activities reflect biophotonic transmission along the axons and in neural circuits, which may be a new mechanism for the processing of neural information.

Goodman G, Poznanski R, Cacha L, Bercovich D ( 2015)

The Two-Brains Hypothesis: Towards a guide for brain-brain and brain-machine interfaces

Journal of Integrative Neuroscience 14(3), 281-293.

DOI:10.1142/S0219635215500235      URL     PMID:26477360      [Cited within: 1]

Great advances have been made in signaling information on brain activity in individuals, or passing between an individual and a computer or robot. These include recording of natural activity using implants under the scalp or by external means or the reverse feeding of such data into the brain. In one recent example, noninvasive transcranial magnetic stimulation (TMS) allowed feeding of digitalized information into the central nervous system (CNS). Thus, noninvasive electroencephalography (EEG) recordings of motor signals at the scalp, representing specific motor intention of hand moving in individual humans, were fed as repetitive transcranial magnetic stimulation (rTMS) at a maximum intensity of 2.0T through a circular magnetic coil placed flush on each of the heads of subjects present at a different location. The TMS was said to induce an electric current influencing axons of the motor cortex causing the intended hand movement: the first example of the transfer of motor intention and its expression, between the brains of two remote humans. However, to date the mechanisms involved, not least that relating to the participation of magnetic induction, remain unclear. In general, in animal biology, magnetic fields are usually the poor relation of neuronal current: generally “unseen” and if apparent, disregarded or just given a nod. Niels Bohr searched for a biological parallel to complementary phenomena of physics. Pertinently, the two-brains hypothesis (TBH) proposed recently that advanced animals, especially man, have two brains i.e., the animal CNS evolved as two fundamentally different though interdependent, complementary organs: one electro-ionic (tangible, known and accessible), and the other, electromagnetic (intangible and difficult to access)02— a stable, structured and functional 3D compendium of variously induced interacting electro-magnetic (EM) fields. Research on the CNS in health and disease progresses including that on brain–brain, brain–computer and brain–robot engineering. As they grow even closer, these disciplines involve their own unique complexities, including direction by the laws of inductive physics. So the novel TBH hypothesis has wide fundamental implications, including those related to TMS. These require rethinking and renewed research engaging the fully complementary equivalence of mutual magnetic and electric field induction in the CNS and, within this context, a new mathematics of the brain to decipher higher cognitive operations not possible with current brain–brain and brain–machine interfaces. Bohr may now rest.

Craddock TJ, Priel A, Tuszynski JA ( 2014)

Keeping time: Could quantum beating in microtubules be the basis for the neural synchrony related to consciousness?

Journal of Integrative Neuroscience 13(2), 293-311.

DOI:10.1142/S0219635214400019      URL     PMID:25012713      [Cited within: 1]

This paper discusses the possibility of quantum coherent oscillations playing a role in neuronal signaling. Consciousness correlates strongly with coherent neural oscillations, however the mechanisms by which neurons synchronize are not fully elucidated. Recent experimental evidence of quantum beats in light-harvesting complexes of plants (LHCII) and bacteria provided a stimulus for seeking similar effects in important structures found in animal cells, especially in neurons. We argue that microtubules (MTs), which play critical roles in all eukaryotic cells, possess structural and functional characteristics that are consistent with quantum coherent excitations in the aromatic groups of their tryptophan residues. Furthermore we outline the consequences of these findings on neuronal processes including the emergence of consciousness.

Ivanchenko MG, Coffeen WC, Lomax TL, Dubrovsky JG ( 2006)

Mutations in the Diageotropica (Dgt) gene uncouple patterned cell division during lateral root initiation from proliferative cell division in the pericycle

The Plant Journal 46(3), 436-447.

DOI:10.1111/tpj.2006.46.issue-3      URL     [Cited within: 1]

Liu MT, Kuan YH, Wang J, Hen R, Gershon MD ( 2009)

5-HT4 receptormediated neuroprotection and neurogenesis in the enteric nervous system of adult mice

Journal of Neuroscience 29(31), 9683-9699.

DOI:10.1523/JNEUROSCI.1145-09.2009      URL     PMID:2749879      [Cited within: 1]

Although the mature enteric nervous system (ENS) has been shown to retain stem cells, enteric neurogenesis has not previously been demonstrated in adults. The relative number of enteric neurons in wild-type (WT) mice and those lacking 5-HT(4) receptors [knock-out (KO)] was found to be similar at birth; however, the abundance of ENS neurons increased during the first 4 months after birth in WT but not KO littermates. Enteric neurons subsequently decreased in both WT and KO but at 12 months were significantly more numerous in WT. We tested the hypothesis that stimulation of the 5-HT(4) receptor promotes enteric neuron survival and/or neurogenesis. In vitro, 5-HT(4) agonists increased enteric neuronal development/survival, decreased apoptosis, and activated CREB (cAMP response element-binding protein). In vivo, in WT but not KO mice, 5-HT(4) agonists induced bromodeoxyuridine incorporation into cells that expressed markers of neurons (HuC/D, doublecortin), neural precursors (Sox10, nestin, Phox2b), or stem cells (Musashi-1). This is the first demonstration of adult enteric neurogenesis; our results suggest that 5-HT(4) receptors are required postnatally for ENS growth and maintenance.

Gross ER, Gershon MD, Margolis KG, Gertsberg ZV, Cowles RA ( 2012)

Neuronal serotonin regulates growth of the intestinal mucosa in mice

Gastroenterology 143(2), 408-417.

DOI:10.1053/j.gastro.2012.05.007      URL     PMID:22609381      [Cited within: 1]

The enteric abundance of serotonin (5-HT), its ability to promote proliferation of neural precursors, and reports that 5-HT antagonists affect crypt epithelial proliferation led us to investigate whether 5-HT affects growth and maintenance of the intestinal mucosa in mice. cMice that lack the serotonin re-uptake transporter (SERTKO mice) and wild-type mice were given injections of selective serotonin re-uptake inhibitors (gain-of-function models). We also analyzed mice that lack tryptophan hydroxylase-1 (TPH1KO mice, which lack mucosal but not neuronal 5-HT) and mice deficient in tryptophan hydroxylase-2 (TPH2KO mice, which lack neuronal but not mucosal 5-HT) (loss-of-function models). Wild-type and SERTKO mice were given ketanserin (an antagonist of the 5-HT receptor, 5-HT2A) or scopolamine (an antagonist of the muscarinic receptor). 5-HT2A receptors and choline acetyltransferase were localized by immunocytochemical analysis. Growth of the mucosa and proliferation of mucosal cells were significantly greater in SERTKO mice and in mice given selective serotonin re-uptake inhibitors than in wild-type mice, but were diminished in TPH2KO (but not in TPH1KO) mice. Ketanserin and scopolamine each prevented the ability of SERT knockout or inhibition to increase mucosal growth and proliferation. Cholinergic submucosal neurons reacted with antibodies against 5-HT2A. 5-HT promotes growth and turnover of the intestinal mucosal epithelium. Surprisingly, these processes appear to be mediated by neuronal, rather than mucosal, 5-HT. The 5-HT2A receptor activates cholinergic neurons, which provide a muscarinic innervation to epithelial effectors.

Greig CJ, Gandotra N, Tackett JJ, Bamdad MC, Cowles RA ( 2016)

Enhanced serotonin signaling increases intestinal neuroplasticity

Journal of Surgical Research 206(1), 151-158.

DOI:10.1016/j.jss.2016.07.021      URL     PMID:27916355      [Cited within: 1]

The intestinal mucosa recovers from injury by accelerating enterocyte proliferation resulting in villus growth. A similar phenomenon is seen after massive bowel resection. Serotonin (5-HT) has been implicated as an important regulator of mucosal homeostasis by promoting growth in the epithelium. The impact of 5-HT on other components of growing villi is not known. We hypothesized that 5-HT timulated growth in the intestinal epithelium would be associated with growth in other components of the villus such as enteric neural axonal processes. Enteric serotonergic signaling is inactivated by the serotonin reuptake transporter, or SERT, molecule. Enhanced serotonin signaling was achieved via SERT knockout (SERTKO) and administration of selective serotonin reuptake inhibitors (SSRI) to wild-type mice (WT-SSRI). 5-HT synthesis inhibition was achieved with administration of 4-chloro-L-phenylalanine (PCPA). Intestinal segments from age-matched WT, SERTKO, WT-SSRI, and corresponding PCPA-treated animals were assessed via villus height, crypt depth, and crypt proliferation. Gap 43, a marker of neuroplasticity, was assessed via immunofluorescence and Western blot. SERTKO and WT-SSRI mice had taller villi, deeper crypts, and increased enterocyte proliferation compared with WT mice. Gap 43 expression via immunofluorescence was significantly increased in SERTKO and WT-SSRI samples, as well as in Western blot analysis. PCPA-treated SERTKO and WT-SSRI animals demonstrated reversal of 5-HT nduced growth and Gap 43 expression. Enhanced 5-HT signaling results in intestinal mucosal growth in both the epithelial cell compartment and the enteric nervous system. Furthermore, 5-HT synthesis inhibition resulted in reversal of effects, suggesting that 5-HT is a critically important regulator of intestinal mucosal growth and neuronal plasticity.

Gershon MD ( 2013)

5-Hydroxytryptamine (serotonin) in the gastrointestinal tract

Current Opinion in Endocrinology, Diabetes, and Obesity 20(1), 14.

DOI:10.1097/MED.0b013e32835bc703      URL     PMID:23222853      [Cited within: 1]

Purpose of review;Although the gut contains most of the body's 5-hydroxytryptamine (5-HT), many of its most important functions have recently been discovered. This review summarizes and directs attention to this new burst of knowledge.Recent findings;Enteroendocrine cells have classically been regarded as pressure sensors, which secrete 5-HT to initiate peristaltic reflexes; nevertheless, recent data obtained from studies of mice that selectively lack 5-HT either in enterochromaffin cells (deletion of tryptophan hydroxylase 1 knockout; TPH1KO) or neurons (TPH2KO) imply that neuronal 5-HT is more important for constitutive gastrointestinal transit than that of enteroendocrine cells. The enteric nervous system of TPH2KO mice, however, also lacks a full complement of neurons; therefore, it is not clear whether slow transit in TPH2KO animals is due to their neuronal deficiency or absence of serotonergic neurotransmission. Neuronal 5-HT promotes the growth/maintenance of the mucosa as well as neurogenesis. Enteroendocrine cell derived 5-HT is an essential component of the gastrointestinal inflammatory response; thus, deletion of the serotonin transporter increases, whereas TPH1KO decreases the severity of intestinal inflammation. Enteroendocrine cell derived 5-HT, moreover, is also a hormone, which inhibits osteoblast proliferation and promotes hepatic regeneration.Summary;New studies show that enteric 5-HT is a polyfunctional signalling molecule, acting both in developing and mature animals as a neurotransmitter paracrine factor, endocrine hormone and growth factor.

Obata Y, Pachnis V ( 2016)

The effect of microbiota and the immune system on the development and organization of the enteric nervous system

Gastroenterology 151(5), 836-844.

DOI:10.1053/j.gastro.2016.07.044      URL     PMID:5102499      [Cited within: 1]

The gastrointestinal (GI) tract is essential for the absorption of nutrients, induction of mucosal and systemic immune responses and maintenance of a healthy gut microbiota. Key aspects of gastrointestinal physiology are controlled by the enteric nervous system (ENS), which is composed of enteric neurons and glial cells. The ENS is exposed to and interacts with the ‘outer' (microbiota, metabolites and nutrients) and ‘inner' (immune cells and stromal cells) microenvironment of the gut. Although the cellular blueprint of the ENS is mostly in place by birth, the functional maturation of intestinal neural networks is completed within the microenvironment of the postnatal gut, under the influence of gut microbiota and the mucosal immune system. Recent studies have demonstrated the importance of molecular interactions among microbiota, enteric neurons and immune cells for GI homeostasis. In addition to its role in GI physiology, the ENS has been associated with the pathogenesis of neurodegenerative disorders, such as Parkinson's disease (PD), raising the possibility that microbiota-ENS interactions could offer a viable strategy for influencing the course of brain diseases. Here, we discuss recent advances on the role of microbiota and the immune system on the development and homeostasis of the ENS, a key relay station along the gut-brain axis.

Williams EK, Chang RB, Strochlic DE, Umans BD, Lowell BB, Liberles SD ( 2016)

Sensory neurons that detect stretch and nutrients in the digestive system

Cell 166(1), 209-221.

DOI:10.1016/j.cell.2016.05.011      URL     PMID:27238020      [Cited within: 1]

Two types of neurons sending signals from the gut to the brain control digestion. One densely innervates intestinal villi and detects food, while another targets stomach and intestinal muscle and senses stretch.

Küsel K, Karnholz A, Trinkwalter T, Devereux R, Acker G, Drake HL ( 2001)

Physiological ecology of Clostridium glycolicum RD-1, an aerotolerant acetogen isolated from sea grass roots

Applied and Environmental Microbiology 67(10), 4734-4741.

DOI:10.1128/AEM.67.10.4734-4741.2001      URL     [Cited within: 1]

Mariat D, Firmesse O, Levenez F, Guimaraes V, Sokol H, DorÉ J, Corthier G, Furet J ( 2009)

The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age

BMC Microbiology 9(1), 123.

DOI:10.1186/1471-2180-9-123      URL     PMID:2702274      [Cited within: 1]

pAbstract/p pBackground/p pIn humans, the intestinal microbiota plays an important role in the maintenance of host health by providing energy, nutrients, and immunological protection. Applying current molecular methods is necessary to surmount the limitations of classical culturing techniques in order to obtain an accurate description of the microbiota composition./p pResults/p pHere we report on the comparative assessment of human fecal microbiota from three age-groups: infants, adults and the elderly. We demonstrate that the human intestinal microbiota undergoes maturation from birth to adulthood and is further altered with ageing. The counts of major bacterial groups itClostridium leptum, Clostridium coccoides/it, itBacteroidetes, Bifidobacterium, Lactobacillus /itand itEscherichia coli /itwere assessed by quantitative PCR (qPCR). By comparing species diversity profiles, we observed age-related changes in the human fecal microbiota. The microbiota of infants was generally characterized by low levels of total bacteria. itC. leptum /itand itC. coccoides /itspecies were highly represented in the microbiota of infants, while elderly subjects exhibited high levels of itE. coli /itand itBacteroidetes/it. We observed that the ratio of itFirmicutes /itto itBacteroidetes /itevolves during different life stages. For infants, adults and elderly individuals we measured ratios of 0.4, 10.9 and 0.6, respectively./p pConclusion/p pIn this work we have confirmed that qPCR is a powerful technique in studying the diverse and complex fecal microbiota. Our work demonstrates that the fecal microbiota composition evolves throughout life, from early childhood to old age./p

Eshel A ( 1998)

On the fractal dimensions of a root system. Plant,

Cell & Environment 21(2), 247-251.

DOI:10.1046/j.1365-3040.1998.00252.x      URL     [Cited within: 1]

Several attempts have been made to apply the principles of fractal geometry to the description of root systems. However, fractal analysis of a real plant root system that maintains its original three-dimensional structure has not been performed to date. An intact root system of a dwarf tomato plant was embedded in gelatin and cut into 3 mm slices. Image analysis was used to collect the data required for determination of three-dimensional and planar fractal dimensions. It was found that the root system has characteristics of a fractal object. The variation of the planar fractal dimension of horizontal and vertical planes intersecting the root system was shown, and their maxima were found to correspond with maximal root proliferation. These results open the way for further application of fractal analysis in root research.

Goldberger AL, Rigney DR, West BJ ( 1990)

Chaos and fractals in human physiology

Scientific American 262(2), 42-49.

DOI:10.1002/cta.4490180303      URL     PMID:2296715      [Cited within: 2]

ABSTRACT The healthy heart beats to a rhythm that is ever-changing - but that can become more periodic at the onset of disease. Chaotic dynamics may underlie the formation of many fractallike structures in the body.

Prusinkiewicz P, Lindenmayer A ( 2004)

The Algorithmic Beauty of Plants

Springer Verlag, Berlin.

DOI:10.1007/978-1-4613-8476-2      URL     [Cited within: 1]

ABSTRACT See the review of the 1996 edition in Zbl 0859.92003.

PuŠkaŠ N, Zaletel I, Stefanović BD, Ristanović D ( 2015)

Fractal dimension of apical dendritic arborization differs in the superficial and the deep pyramidal neurons of the rat cerebral neocortex

Neuroscience Letters 589, 88-91.

DOI:10.1016/j.neulet.2015.01.044      URL     PMID:25603473      [Cited within: 1]

Pyramidal neurons of the mammalian cerebral cortex have specific structure and pattern of organization that involves the presence of apical dendrite. Morphology of the apical dendrite is well-known, but quantification of its complexity still remains open. Fractal analysis has proved to be a valuable method for analyzing the complexity of dendrite morphology. The aim of this study was to establish the fractal dimension of apical dendrite arborization of pyramidal neurons in distinct neocortical laminae by using the modified box-counting method. A total of thirty, Golgi impregnated neurons from the rat brain were analyzed: 15 superficial (cell bodies located within lamina II–III), and 15 deep pyramidal neurons (cell bodies situated within lamina V–VI). Analysis of topological parameters of apical dendrite arborization showed no statistical differences except in total dendritic length (p=0.02), indicating considerable homogeneity between the two groups of neurons. On the other hand, average fractal dimension of apical dendrite was 1.33±0.06 for the superficial and 1.24±0.04 for the deep cortical neurons, showing statistically significant difference between these two groups (p<0.001). In conclusion, according to the fractal dimension values, apical dendrites of the superficial pyramidal neurons tend to show higher structural complexity compared to the deep ones.

Helmberger M, Pienn M, Urschler M, Kullnig P, Stollberger R, Kovacs G, Olschewski A, Olschewski H, Bálint Z ( 2014)

Quantification of tortuosity and fractal dimension of the lung vessels in pulmonary hypertension patients

PloS one 9(1), e87515.

DOI:10.1371/journal.pone.0087515      URL     PMID:3909124      [Cited within: 1]

: Pulmonary hypertension (PH) can result in vascular pruning and increased tortuosity of the blood vessels. In this study we examined whether automatic extraction of lung vessels from contrast-enhanced thoracic computed tomography (CT) scans and calculation of tortuosity as well as 3D fractal dimension of the segmented lung vessels results in measures associated with PH. In this pilot study, 24 patients (18 with and 6 without PH) were examined with thorax CT following their diagnostic or follow-up right-sided heart catheterisation (RHC). Images of the whole thorax were acquired with a 128-slice dual-energy CT scanner. After lung identification, a vessel enhancement filter was used to estimate the lung vessel centerlines. From these, the vascular trees were generated. For each vessel segment the tortuosity was calculated using distance metric. Fractal dimension was computed using 3D box counting. Hemodynamic data from RHC was used for correlation analysis. Distance metric, the readout of vessel tortuosity, correlated with mean pulmonary arterial pressure (Spearman correlation coefficient: 03010907=09070.60) and other relevant parameters, like pulmonary vascular resistance (03010907=09070.59), arterio-venous difference in oxygen (03010907=09070.54), arterial (03010907=09070903'0.54) and venous oxygen saturation (03010907=09070903'0.68). Moreover, distance metric increased with increase of WHO functional class. In contrast, 3D fractal dimension was only significantly correlated with arterial oxygen saturation (03010907=09070.47). Automatic detection of the lung vascular tree can provide clinically relevant measures of blood vessel morphology. Non-invasive quantification of pulmonary vessel tortuosity may provide a tool to evaluate the severity of pulmonary hypertension. Trial Registration: ClinicalTrials.gov NCT01607489

Losa GA, Merlini D, Nonnenmacher TF, Weibel ER ( 2005)

Fractals in Biology and Medicine

Springer Science & Business, Berlin.

[Cited within: 1]

Patrick RP, Ames BN ( 2014)

Vitamin D hormone regulates serotonin synthesis. Part 1: relevance for autism

The FASEB Journal 28(6), 2398-2413.

DOI:10.1096/fj.13-246546      URL     [Cited within: 1]

Gutknecht L, Kriegebaum C, Waider J, Schmitt A, Lesch KP ( 2009)

Spatio-temporal expression of tryptophan hydroxylase isoforms in murine and human brain: convergent data from Tph2 knockout mice

European Neuropsychopharmacology 19(4), 266-282.

DOI:10.1016/j.euroneuro.2008.12.005      URL     PMID:19181488      [Cited within: 1]

Dysregulation of tryptophan hydroxylase (TPH)-dependent serotonin (5-HT) synthesis, has been implicated in various neuropsychiatric disorders, although the differential expression pattern of the two isoforms is controversial. Here, we report a comprehensive spatio-temporal isoform-specific analysis of TPH1 and TPH2 expression during pre- and postnatal development of mouse brain and in adult human brain. TPH2 expression was consistently detected in the raphe nuclei, as well as in fibers in the deep pineal gland and in small intestine. Although TPH1 expression was found in these peripheral tissues, no significant TPH1 expression was detected in the brain, neither during murine development, nor in mouse and human adult brain. In support of TPH2 specificity in brain 5-HT synthesis, raphe neurons of Tph2 knockout mice were completely devoid of 5-HT, with no compensatory activation of Tph1 expression. In conclusion, our findings indicate that brain 5-HT synthesis across the lifespan is exclusively maintained by TPH2.

Zhuravlev A, Tsvylev O, Zubkova S ( 1973)

Spontaneous endogenous ultraweak luminescence of rat liver mitochondria in conditions of normal metabolism

Biofizika 18(6), 1037-1040.

URL     PMID:4805512      [Cited within: 1]

react-text: 378 2-Phenylcarbamoylisatogen has been shown to stimulate succinate oxidation by rat liver mitochondria, but to inhibit the phosphorylation of ADP. The hydrolysis of ATP was also stimulated and an additive action with 2,4-dinitrophenol was demonstrated. The possible mechanism of the uncoupling action of 2-phenylcarbamoylisatogen is discussed. /react-text react-text: 379 /react-text

Tuszynski JA, Dixon JM ( 2001)

Quantitative analysis of the frequency spectrum of the radiation emitted by cytochrome oxidase enzymes

Physical Review. E, Statistical, Nonlinear, and Soft Matter Physics 64(5), 051915.

DOI:10.1103/PhysRevE.64.051915      URL     PMID:11735976      [Cited within: 1]

DOI:

Shcherbin D ( 1999)

Phosphorescent analysis of lipid peroxidation products in liposomes

Biofizika 44(4), 676-681.

DOI:10.1076/apab.107.3.257.4334      URL     PMID:10544819      [Cited within: 1]

It was found that peroxidation products incorporated into liposomes prepared from oxidized preparations of heart and the total fraction of erythrocyte are able to phosphoresce at room temperature was studied. The temperature dependences of kinetic and spectral parameters of phosphorescence were measured. It is shown that mechanism of phosphorescence quenching of has a dynamic nature. It is proposed to use endogenic molecules of the peroxidation products capable of phosphorescence as intrinsic phosphorescence probes for studying the slow molecular dynamics of in artificial and biological in a millisecond range.

Nakano M ( 1989)

Low-level chemiluminescence during lipid peroxidations and enzymatic reactions

Journal of Bioluminescence and Chemiluminescence 4(1), 231-240.

DOI:10.1002/bio.1170040133      URL     PMID:2801214      [Cited within: 1]

Abstract Low-level chemiluminescence during lipid peroxidation and enzymatic reaction have been analysed by a filter type spectrometer. Tyrosine and tryptophan residues in proteins were found to be emitters in the visible region during their enzymatic oxidation. The natural chemiluminescence from fertilization of sea urchin eggs was found to have originated from tyrosine--cation radical mediated reaction in ovo-peroxidase--membrane protein--H2O2 system.

Schiefelbein JW, Benfey PN ( 1991)

The development of plant roots: new approaches to underground problems

The Plant Cell 3(11), 1147.

DOI:10.1105/tpc.3.11.1147      URL     [Cited within: 1]

Buer CS, Muday GK ( 2004)

The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light

The Plant Cell 16(5), 1191-1205.

DOI:10.1105/tpc.020313      URL     [Cited within: 1]

Bukhov N, Bondar V, Drozdova I, Kara A, Kotov A, Maevskaya S, Vasil'ev A, Voevudskaya SY, Voronin PY, Mokronosov A ( 1996)

Development of storage roots in radish (Raphanus sativus) plants as affected by light quality

Journal of Plant Physiology 149(3, 4), 405-412.

DOI:10.1016/S0176-1617(96)80141-6      URL     [Cited within: 1]

The development of storage roots was studied in radish plants grown under blue or red light. Unlike blue light-grown plants, no tuber development was found in red light-grown plants. Instead of the storage root formation, a larger development of petioles was observed in red light-grown plants. Reduced leaf matter was found in red light-grown plants compared with blue light-grown ones. At the growth chamber photon flux density (170 mol m 2 s 1 ), similar rates of photosynthetic CO 2 fixation were found under red and blue light. Higher leaf starch accumulation was observed in red light-grown radish plants, whereas the level of soluble carbohydrates was lower than in blue light-grown plants. The absolute contents of several Calvin cycle metabolites were higher in blue light-grown plants, but the diurnal changes in their levels were similar in leaves of both variants examined. The portion of photosynthetically fixed carbon accumulated in roots was quantified as 0.50 and 0.31 for blue light-grown and red light-grown plants, respectively. The levels of two phytohormones, indole-3-acetate and zeatin plus zeatin riboside were found to be several-fold higher in roots of blue light-grown plants compared with red light-grown ones. Thus, the above hormones obviously create a higher sink demand from roots to leaves in blue light-grown plants, which facilitate the development of under-ground storage tissues. Petioles, not roots, were assumed to act as a main sink organ in red light-grown radish plants. A less strong sink demand probably also accounts for reduced assimilatory leaf matter in red light-grown plants.

Lee HJ, Ha JH, Kim SG, Choi HK, Kim ZH, Han YJ, Kim JI, Oh Y, Fragoso V, Shin K ( 2016)

Stem-piped light activates phytochrome B to trigger light responses in Arabidopsis thaliana roots

Science Signaling 9(452), ra106.

DOI:10.1126/scisignal.aaf6530      URL     PMID:27803284      [Cited within: 1]

Abstract The roles of photoreceptors and their associated signaling mechanisms have been extensively studied in plant photomorphogenesis with a major focus on the photoresponses of the shoot system. Accumulating evidence indicates that light also influences root growth and development through the light-induced release of signaling molecules that travel from the shoot to the root. We explored whether aboveground light directly influences the root system of Arabidopsis thaliana Light was efficiently conducted through the stems to the roots, where photoactivated phytochrome B (phyB) triggered expression of ELONGATED HYPOCOTYL 5 (HY5) and accumulation of HY5 protein, a transcription factor that promotes root growth in response to light. Stimulation of HY5 in response to illumination of only the shoot was reduced when root tissues carried a loss-of-function mutation in PHYB, and HY5 mutant roots exhibited alterations in root growth and gravitropism in response to shoot illumination. These findings demonstrate that the underground roots directly sense stem-piped light to monitor the aboveground light environment during plant environmental adaptation. Copyright 2016, American Association for the Advancement of Science.

Fraikin GY, Strakhovskaya MG, Ivanova EV, Rubin AB ( 1989)

Near-UV activation of enzymatic conversion of 5-hydroxytryptophan to serotonin

Photochemistry and Photobiology 49(4), 475-477.

DOI:10.1111/j.1751-1097.1989.tb09197.x      URL     PMID:2786220      [Cited within: 1]

Abstract— Near-UV (337 nm) photoactivation of the 5-hydroxytryptophan decarboxylation reaction producing serotonin has been observed. The photoactivation effect was investigated as a function of fluence rate and fluence, and pH. Photoactivation of decarboxylase activity was found to occur at nearly neutral pH values (low activity of the enzyme in the dark). The findings indicate that the effect of light is similar to a pH shift toward the acid region, which causes the enzyme conversion from the inactive to active form. Pyridoxal phosphate, the decarboxylase cofactor, in the form of an adduct absorbing at 330–340 nm, is suggested as a candidate for the role of the photoactive chromophore of decarboxylase.

Gostkowski ML, McDoniel JB, Wei J, Curey TE, Shear JB ( 1998)

Characterizing spectrally diverse biological chromophores using capillary electrophoresis with multiphoton-excited fluorescence

Journal of the American Chemical Society 120(1), 18-22.

DOI:10.1021/ja9727427      URL     [Cited within: 1]

Penrose R ( 1994)

Shadows of the Mind.

Oxford, United Kingdom.

[Cited within: 1]

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