Lamprey Serotonin

Cross references:     Lamprey Neurotransmitters
Serotonin Gate (5-HT3R)    Serotonin Metabotropic Receptor

    "lamprey serotonin"
        PubMed = 128     http://www.ncbi.nlm.nih.gov/pubmed/?term=lamprey+serotonin
        Google = 958,000 https://www.google.com/search?q=lamprey+serotonin&ie=utf-8&oe=utf-8&aq=t&rls=org.mozilla:en-US:official&client=firefox-a&channel=np&source=hp

1985
Distribution of serotonergic neurons and processes in the lamprey spinal cord.
http://www.ncbi.nlm.nih.gov/pubmed/3889703
    "The distribution of serotonin in the spinal cord in two species of lamprey, Ichthyomyzon unicuspis and Petromyzon marinus, was studied by indirect immunofluorescence techniques. Multipolar cell bodies containing serotonin-like immunoreactivity were found along the length of the spinal cord, along the midline and slightly ventral to the central canal. These cell bodies send a diffuse projection of processes throughout the spinal cord, including: (1) a dense projection to the ventral surface; (2) a strong projection to the ventromedial longitudinal fiber tracts; (3) a less intense projection to the dorsal longitudinal fiber tracts; and (4) a weak projection to the lateral fiber tracts. Lesion experiments showed that processes descending from the brain or rostral spinal cord provide a major projection to the lateral fiber tracts and smaller contributions to the dorsal and ventromedial fiber tracts. Fluorescent processes were also observed in the dorsal roots and serotonergic peripheral cell bodies were seen adjacent to the dorsal roots. Our results suggest that the serotonergic innervation of the lamprey spinal cord arises from three sources: spinal interneurons, descending tracts and peripheral (possibly sensory) input. This provides an anatomical substrate for our recent finding that serotonin modulates the central pattern generator for locomotion in the lamprey spinal cord."

1985
    Serotonin modulates the central pattern generator for locomotion in the isolated lamprey spinal cord.
http://www.ncbi.nlm.nih.gov/pubmed/4056654
    "The central pattern generator for locomotion in the spinal cord of the lamprey can be activated in vitro by the addition of D-glutamate to the bathing saline. Serotonin has no effects when bath-applied alone, but it modulates the D-glutamate-activated swimming pattern. Three major effects are observed: a dose-dependent reduction in the frequency of rhythmic ventral root burst discharge; enhancement of the intensity of burst discharge, due in part to the recruitment of previously inactive motoneurones; prolongation of the intersegmental phase lag. Motoneurone activation appears to result from enhanced synaptic drive from the central pattern generator; no direct effects of serotonin on the motoneurones themselves (resting potential, input resistance or threshold for action potential generation) were observed. Theoretical and experimental studies suggest that the prolongation of the intersegmental phase lag results at least in part from differential effects of serotonin on segmental oscillators in different parts of the spinal cord. Isolated caudal pieces of the cord were more strongly affected by serotonin than isolated rostral pieces. We propose that serotonin may be an endogenous modulator of the central pattern generator for locomotion in the lamprey. It may have a role in the generation of a family of related undulatory movements (swimming, crawling, burrowing) by a single central pattern generator".    - Free full text -

1986
    A spinal projection of 5-hydroxytryptamine neurons in the lamprey brainstem; evidence from combined retrograde tracing and immunohistochemistry.
http://www.ncbi.nlm.nih.gov/pubmed/3725200
    "To investigate whether there is a descending contribution to the spinal 5-hydroxytryptamine (5-HT) innervation in the lamprey, a primitive vertebrate, a study using retrograde transport of the fluorescent tracer Fast blue combined with 5-HT immunohistochemistry was conducted. Two to 4 weeks after an injection of Fast blue into the rostral spinal cord, retrogradely labelled cells were seen throughout the brainstem. Two groups of these cells, one within the posterior reticular nucleus of the rhombencephalon and another rostral to the trigeminal motor nucleus, were labelled after incubation with 5-HT antiserum. These findings suggest that in addition to the well-described local intraspinal 5-HT system, there is also, as in higher vertebrates, a descending 5-HT projection from the brainstem which extends at least 20 segments into the spinal cord."

1991

5-Hydroxytryptamine depresses reticulospinal excitatory postsynaptic potentials in motoneurons of the lamprey.
http://www.ncbi.nlm.nih.gov/pubmed/1676146
    "Application of 5-hydroxytryptamine (5-HT) to the lamprey spinal cord in vitro reversibly depressed the chemical component of excitatory post-synaptic potentials recorded intracellularly in motoneurons and evoked by stimulation of single reticulospinal Müller cells. The depression could be produced either by local application of small volumes of 10 mM 5-HT to the surface of the spinal cord or by bath-application of 1 or 10 microM 5-HT. No effect on the input resistance of the postsynaptic cells or their sensitivity to glutamate, the suspected transmitter at this synapse, could be detected, suggesting the possibility of a presynaptic action of 5-HT at this synapse in the lamprey."
    117 Related citations:
http://www.ncbi.nlm.nih.gov/pubmed?linkname=pubmed_pubmed&from_uid=1676146
    10 Cited by's:
http://www.ncbi.nlm.nih.gov/pubmed?linkname=pubmed_pubmed_citedin&from_uid=1676146

1992
The serotoninergic system of the brain of the lamprey
http://www.ncbi.nlm.nih.gov/pubmed/1418750
Only abstract available online. Article not obtainable through library.
"The distribution of serotonin(5HT)-immunoreactive cell bodies, nerve fibers and terminals was investigated by light microscopy in the lamprey Lampetra fluviatilis. Twenty-three distinct groups of 5HT neuronal somata were identified from diencephalic to rhombencephalic levels in the brain. The diencephalon contained a subependymal population of immunoreactive cells in contact with the cerebrospinal fluid (CSF), which could be subdivided into five separate groups situated in the hypothalamus and ventral thalamus; five additional groups of immunoreactive diencephalic neurons, situated in the dorsal thalamus and thalamo-pretectum, which were not in contact with the CSF, were also identified. In the midbrain, in addition to a few labelled neurons in the optic tectum, two structures containing immunoreactive cells were identified in the tegmentum mesencephali. None of these 5HT cells corresponded to the retinopetal neurons which are situated in the same region. A very large number of 5HT neurons were observed in the hindbrain which could be divided into seven groups in the isthmus rhombencephali and a further three in the rhombencephalon proper. Immunoreactive fibers and terminals were widely distributed throughout the neuraxis. In the telencephalon two 5HT fibers assemblies, lateral and medial, could be identified which terminated in both pallial and subpallial structures. The richest serotoninergic innervation in the telencephalon was found in the lateral portion of the primordium hippocampi and the medial part of the corpus striatum. In the diencephalon, the distribution of immunoreactive fibers and terminals was heterogeneous, being most pronounced in the lateral hypothalamic area and in the infundibulum. The densest arborization of fibers in the mesencephalon was found in the stratum fibrosum et cellulare externum of the optic tectum, a major site of retinal projection, and in the nucleus interpeduncularis mesencephali as well as in the oculomotor nuclei. The rhombencephalon is richly endowed with serotoninergic fibers and terminals, many labelled arborizations being found in the nuclei isthmi rhombencephali and around the nucleus motorius nervi trigemini. Comparative analysis of the serotoninergic systems of petromyzontiforms and gnathostomes indicates that the evolution of this system involves a progressive elimination of the rostral immunoreactive cells and an increasing complexity of the caudal population of serotoninergic neurons."

166 Related citations:
http://www.ncbi.nlm.nih.gov/pubmed?linkname=pubmed_pubmed&from_uid=1418750

My comment:
     Note how wide spread serotonin already is: 23 distinct groups!

1994
    5-HT innervation of reticulospinal neurons and other brainstem structures in lamprey.
http://www.ncbi.nlm.nih.gov/pubmed/7515906
    "In order to determine if reticulospinal neurons involved in the control of locomotion and responsive to exogenously applied 5-hydroxytryptamine (5-HT) are innervated by fibers that contain serotonin, the serotoninergic innervation of reticulospinal neurons, identified by retrograde labeling with fluorescein-conjugated dextran-amine (FDA), was investigated by immunohistochemistry in the lamprey brainstem. A widespread distribution of 5-HT immunoreactive (5-HT-ir) fibers was seen within the basal plate of the brainstem, an area containing reticulospinal somata and dendritic aborizations. Numerous 5-HT varicose fibers were found in close relation to large reticulospinal cell bodies, particularly in the middle and anterior rhombencephalic reticular nuclei (MRRN and ARRN). Some of these reticulospinal somata were surrounded by a very dense pericellular 5-HT innervation. 5-HT-ir fibers were also seen in other brain structures that are known to influence reticulospinal neurons such as the rhombencephalic alar plate containing sensory relay interneurons, cranial nerves (III-X), cerebellum, and tectum. These findings suggest that, as in the spinal cord, motor behavior controlled by reticulospinal neurons may be subject to a serotoninergic modulation."
   "In the present study, we report that there is a widespread 5-HT fiber distribution in the brainstem basal plate, a region largely occupied by dendrites of reticulospinal neurons. Furthermore, there is a very dense 5-HT innervation surrounding reticulospinal cell bodies of the middle and anterior rhombencephalic reticular nuclei.
    "It seems likely that these cells will be subjected to a strong 5-HT influence, although the receptor distribution on their cell body and dendrites has yet to be determined. Electron microscopy is necessary to determine whether these terminals form conventional synaptic contacts with the reticulospinal cell bodies or if they largely lack synaptic specializations, as described in the spinal cord.
    "However, as for spinal neurons, 5-HT reduces the late afterhyperpolarization in reticulospinal cells, an effect that results from the reduction of currents mediated by Ca2+-activated K+ channels. Moreover, 5-HT may also modify the resting membrane potential of reticulospinal neurons)."
    "In summary, 5-HT systems in the brainstem are most likely to play a key role in modulating reticulospinal output from the brainstem as well as the output of other neurons in the alar plate, the cerebellum, and the tectum."

1996
    Rostrocaudal distribution of 5-HT innervation in the lamprey spinal cord and differential effects of 5-HT on fictive locomotion.
http://www.ncbi.nlm.nih.gov/pubmed/8906499
    " Intraspinal 5-HT cells form a very dense ventromedial plexus in which the dendrites of neurons forming the locomotor network are distributed. The number of 5-HT cells and varicosities in this plexus decreases in the fin area (segments 70-90), and then increases somewhat in the most caudal segments. The descending 5-HT fibers from the rhombencephalon are located in the lateral and ventral columns, and their numbers gradually decrease to around 50% in the tail part of the spinal cord. In contrast, the number of 5-HT-ir axons in the dorsal column remains the same along the spinal cord."

2007
Development of the serotonergic system in the central nervous system of the sea lamprey.
http://www.ncbi.nlm.nih.gov/pubmed/17485194
     Only abstract available online. I got the PDF from the library.
from the Abstract:
    "Here, the development of the serotonergic system in the central nervous system of the sea lamprey, Petromyzon marinus, was investigated by immunohistochemical analysis of specimens ranging from embryos to adults. The different serotonin-immunoreactive (5-HT-ir) neuronal populations that are found in adults were observed between the embryonic and metamorphic stages.
    The earliest serotonergic neurons were observed in the basal plate of the isthmus region of late embryos. In prolarvae, progressive appearance of new serotonergic cell groups was observed: firstly in the spinal cord, then in the pineal organ, tuberal region, zona limitans intrathalamica, rostral isthmus, and the caudal part of the rhombencephalon.
    In early larvae a new group of serotonergic cells was observed in the mammillary region, whereas in the pretectal region and the parapineal organ the first serotonergic cells were seen in the middle and late larval stages, respectively.
    The first serotonergic fibres appeared in early prolarvae, with fibres that ascend and descend from the isthmic cell group, and the number of immunoreactive fibres increased progressively until the adult stage.
    The results reveal strong resemblances between lampreys and other vertebrates in the spatio-temporal pattern of development of brainstem populations. This study also reveals a shared pattern of early ascending and descending serotonergic pathways in lampreys and jawed vertebrates."
from the PDF:
    4.7. Development of serotonergic projections
     "The adult lamprey brain is richly and widely innervated by serotonergic fibres.
    The first serotonergic fibres appear in the primordial marginal zone adjacent to the first isthmic serotonergic neurons in late embryos/early prolarvae, and soon after ascending and descending serotonergic fibres are observed growing in the primordial marginal area .
    In the present study, serotonergic axons from the isthmic group also coursed dorsally to the optic tectum and dorsocaudally to the octavolateral area in early stages. In developing mammals,
serotonin is released by growing axons before conventional synapses become established, and modulate events such as cell division, neuronal migration and cell differentiation. The first lamprey serotonergic fibres may accomplish similar functions during development.
    The main longitudinal ascending and descending serotonergic pathways are formed early in lamprey development, and some axons or axon collaterals then leave the main pathways to reach different targets and branch, as reported in rat embryos.
    The main serotonergic ascending pathway of prolarvae arises from the isthmic group. When
diencephalic groups appear, axons from these groups intermingle with those from the isthmic group, making it impossible to distinguish between axons of hypothalamic or isthmic origin. The mixture of axons originating from the rhombencephalon and diencephalon in ascending serotonergic pathways has also been reported in teleosts.
    Serotonergic fibres reach the prolarval telencephalon at the beginning of the pigmentation stage, when the telencephalon is still very poorly differentiated. Early serotonergic innervation of the telencephalon also occurs in mammalian embryos.
    The arrival of first serotonergic fibres to the striatum (burrowing stage) coincides with the appearance of the striatal GABAergic population, and precedes that of incoming
dopaminergic fibres. The early arrival of serotonergic fibres to the lamprey striatum, just before dopaminergic fibres, is compatible with regulation by serotonin of the ingrowth and terminal development of these fibres, as suggested in the rat cortex.
    From middle-sized larvae, when most telencephalic regions are easily recognizable, serotonergic fibres are especially abundant in the pallial marginal region. A notable exception is the medial pallium, which in adults is very richly innervated by 5-HT-ir fibres, but lacks serotonergic innervation until late larval stages. Proliferation studies in sea lamprey indicate that this is a late developing pallial region), which may explain the late maturation of its serotonergic innervation.
     In mammals, serotonin appears to be involved in regulation of the development of the cortex, but possible developmental roles for serotonin in the larval lamprey are speculative.
     The serotonergic isthmic group of lampreys projects to the spinal cord, as seen in early developmental stages. Spinal projections from this 5-HT-ir group have also been observed by
Hay-Schmidt in early river lamprey larvae, and characterized experimentally by Brodin et al. in adult river lampreys. Similar projections occur in zebrafish.
    The caudal rhombencephalic group also projects to the spinal cord in adults.
     Although in the adult rat the superior raphe nuclei project rostrally and the posterior raphe nuclei project caudally, most of the first serotonergic cells appear to be monopolar and initially
the same cells show both descending and ascending processes.
These data suggest that the presence of ascending and descending projections from the
isthmic group (superior raphe) represents a primitive condition of vertebrates. As in the rat, rhombencephalic serotonergic nuclei of lamprey also send contralateral processes across the midline beneath the floor plate. In the developing rat, growth of the contralateral 5-HT-ir
processes precedes migration movements, which leads to fusion of 5-HT-ir cell groups in the midline; this does not occur in lamprey."
    "The results reveal strong resemblances between lampreys and other vertebrates in the spatio-temporal pattern of development of brainstem populations. This study also reveals a shared pattern of early ascending and descending serotonergic pathways in lampreys and jawed vertebrates."
    "Development of serotonergic system in sea lamprey begins at about the same time as development of the GABAergic system, but both systems precede the dopaminergic system. ... Some serotonergic and GABAergic neurons appear to be among the first differentiated neurons of the brain."

2008
    Development and organization of the descending serotonergic brainstem-spinal projections in the sea lamprey.
http://www.ncbi.nlm.nih.gov/pubmed/18602462
    "The organization and development of the descending spinal projections from serotonergic rhombencephalic neurons in the larval sea lamprey were investigated by double labeling, tract-tracing methods and immunocytochemistry against serotonin. The results showed that two serotonergic populations of the isthmic and vagal reticular regions present reticulospinal neurons from the beginning of the larval period. Of the three serotonergic subpopulations recognized in the isthmic reticular group, only two - the medial and ventral subpopulations - project to the spinal cord, with most of the projecting cells in the caudal part of the medial isthmic subpopulation. Occasional cells projecting to the spinal cord were observed in the ventral subpopulation. The vagal reticular serotonergic nucleus situated in the caudal rhombencephalon also presents cells with descending projections. The early development of the brainstem serotonergic projections to the spinal cord appears to be a conserved trait in all vertebrates studied. Although a serotonergic hindbrain-spinal projection system appears to have been present before the divergence of agnathans and gnathostomes, no serotonergic cells were observed in the raphe region in lamprey. Moreover, proportionally more rostral hindbrain serotonergic cells contribute to the spinal serotonergic projections in the sea lamprey than in jawed vertebrates."

2009
    Extensive presence of serotonergic cells and fibers in the peripheral nervous system of lampreys.
http://www.ncbi.nlm.nih.gov/pubmed/19025991
    "Lampreys are suitable animal models for studying the evolution of the vertebrate nervous system because they belong to the earliest group of extant vertebrates, the agnathans. The general organization of the serotonergic central nervous system is well known in lampreys, but information about its peripheral organization is lacking. In the present study, high-performance liquid chromatography and immunohistochemistry with an antibody against serotonin were used to study the presence and peripheral distribution of serotonergic elements in the head of larval sea lampreys. Adult lampreys were also analyzed in order to compare the organization of the system in larval and postmetamorphic stages. Serotonergic cells were observed in the cranial nerve ganglia, the musculature, the taste buds, and in the gills. Serotonergic fibers were extensive in all tissues except the epidermis. Possible roles were proposed for the different cell types observed in relation to their location, structure, and innervation patterns. The serotonergic cells appear to be involved in the oxygen and taste chemoreception processes, the modulation of musculature contraction, and in the regulation of cilia beat frequency and mucus secretion in lampreys. The extensive presence of serotonergic elements in the peripheral nervous system of lampreys suggests a close relationship with the organization of this system in invertebrate groups."

2009
Serotonin and GABA are colocalized in restricted groups of neurons in the larval sea lamprey brain: insights into the early evolution of neurotransmitter colocalization in vertebrates (Goog)
http://onlinelibrary.wiley.com/doi/10.1111/j.1469-7580.2009.01119.x/full
Only abstract available online. I got the PDF from the library.
    "The colocalization of 5-HT and GABA in neurons of the sea lamprey brain was studied using antibodies directed against 5-HT and GABA and confocal microscopy. Colocalization of the neurotransmitters was observed in the diencephalon and the isthmus. ... Of the three serotonergic isthmic subgroups already recognized in the sea lamprey isthmus (dorsal, medial and ventral), such double-labelled cells were only observed in the ventral subgroup ... An equivalence between these lamprey isthmic cells and the serotonergic/GABAergic raphe cells of mammals is suggested."
    "Double immunofluorescence experiments in tissue fixed in a paraformaldehyde/glutaraldehyde mixture revealed the presence of GABA-ir neurons in addition to 5-HT-ir neurons in most regions of the sea lamprey brain containing serotonergic cells. However, colocalization of GABA and 5-HT immunoreactivities in cells was only observed in a few
serotonergic groups"
    "The GABA-ir population of the rostral part of the thalamus was far more abundant than that of 5-HT-ir cells, so that the GABA-ir cells outside the zona limitans were 5-HT negative." "... the larger 5-HT-ir cells of the medial isthmic subgroup were not GABA-ir, although numerous GABA-ir cells were intermingled with these serotonergic cells" "In the caudal rhombencephalon, the 5-HT-ir cells of the vagal nucleus were intermingled with GABA-ir cells but no double-labelled cells were observed"

CotA Lamprey Serotonin
140729 - 1503 modified

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