Serotonin immunoreactivity of neurons in the gastropod <i>Aplysia californica</i>

Longley, Roger D.; Longley, Alison J.

doi:10.1002/neu.480170408

Cited by 95 publications

(79 citation statements)

References 40 publications

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“…These same synaptic, paracrine and endocrine mechanisms of serotonin release occur in Aplysia [Schwartz and Shkolnik, 1981;Kistler, Jr. et al, 1985;Longley and Longley, 1986]. Although serotonin has unitary, concentration-dependent effects in many systems, its facilitatory effect on central synapses in Aplysia has recently been shown to depend on the temporal pattern of exposure [Mauelshagen et al, 1998].…”

Section: Metamodulation: Dependence On Exposurementioning

confidence: 99%

Metamodulation of the Crayfish Escape Circuit

et al. 2002

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Neuromodulation provides a means of changing the excitability of neurons or the effect of synapses, and so extends the performance range of neural circuits. Metamodulation occurs when the neuromodulatory effect is itself modulated, often in response to a change in the behavioral state of the animal. The well-studied neural circuit that mediates escape in the crayfish is modulated by serotonin, and this modulation is subject to two forms of metamodulation. First, the serotonergic modulation of the Lateral Giant (LG) command neuron for escape depends on the pattern of exposure of the cell to serotonin. High and low concentrations, and rapid and slow exposures each produce opposite modulatory effects on sensory-evoked EPSPs in LG. In addition, brief exposures produce transient modulatory effects, whereas longer exposures produce long-term facilitation. These different patterns of exposure may result from serotonin neurotransmission, paracrine transmission, and hormonal release, all of which occur in the vicinity of LG. The second form of metamodulation enables serotonergic modulation to track slow changes in the social status of the crayfish. Slowly applied serotonin facilitates LG’s response in socially isolated crayfish and in new dominant and subordinate animals. Facilitation is retained in the dominant animal during two weeks of continuous pairing of the animals, but facilitation gradually changes to inhibition in the subordinate crayfish. These and related changes in serotonin modulation appear to result from changes in the population of serotonin receptors that mediate the modulatory effects in LG. Whereas the exposure-dependent metamodulation enables rapid changes in serotonergic modulation of LG to occur, the status-dependent metamodulation enables serotonergic modulation of LG to track the slow maturation of social relationships.

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Section: Metamodulation: Dependence On Exposurementioning

confidence: 99%

Metamodulation of the Crayfish Escape Circuit

et al. 2002

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“…The immunocytochemical procedure was slightly modified from the whole-mount technique of Longley and Longley (27). Rabbit anti-Phe-Met-Arg-Phe-NH2 antisera was obtained from Immuno Nuclear (Stillwater, MN) and rhodamine-labeled goat anti-rabbit antiserum was obtained from Cappel Laboratories (Cochranville, PA).…”

Section: Methodsmentioning

confidence: 99%

Tail shock produces inhibition as well as sensitization of the siphon-withdrawal reflex of Aplysia: possible behavioral role for presynaptic inhibition mediated by the peptide Phe-Met-Arg-Phe-NH2.

Mackey

Glanzman

Small

et al. 1987

Proc. Natl. Acad. Sci. U.S.A.

128

141

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Recent studies have shown that, in addition to being modulated by presynaptic facilitation, the sensory neurons of the gill-and siphon-withdrawal reflex ofAplysia are also capable of being modulated by transient presynaptic inhibition produced by the peptide Phe-Met-Arg-Phe-NH2. These two modulatory effects involve different second-messenger systems: the facilitation is mediated through cAMP-dependent protein phosphorylation, and the inhibition is mediated through the lipoxygenase pathway of arachidonic acid. To explore the behavioral function of this inhibition, we have carried out a parametric analysis of the effect of tail shock on the siphon-withdrawal reflex. In addition to producing sensitization of the withdrawal reflex, tail shock also transiently inhibits the reflex. The inhibition is produced by relatively weak shock, whereas sensitization is more prominent and may mask the inhibition with stronger shock. Furthermore, inhibition is not observed after habituation training. Cellular studies suggest that the behavioral inhibition is mediated, at least in part, by presynaptic inhibition of transmitter release from the siphon sensory neurons. Moreover, we have identified an interneuron within the left pleural ganglion (LPL16) that shows Phe-Met-Arg-Phe-NH2 immunoreactivity, is activated by tail shock, and simulates the presynaptic inhibitory actions produced by tail shock. Therefore, our results suggest that presynaptic inhibition mediated by Phe-Met-Arg-Phe-NH2 and its lipoxygenase second messenger contributes to behavioral inhibition of the siphon-withdrawal reflex.Modern studies of the properties of stimuli that serve as reinforcers for sensitization and classical conditioning in vertebrate learning reveal that these stimuli usually have two components, a prominent facilitatory component and a lessobvious inhibitory component. The facilitatory component is important for sensitization and conventional classical conditioning, whereas the inhibitory component is important for conditioned inhibition (1, 2). These dual properties of unconditioned stimuli have also been studied recently in invertebrates (6,14,(20)(21)(22)(23)(24)(25)(26)35). We describe here the existence of an inhibitory component of the unconditioned stimulus for learning in Aplysia and show that this component appears to use Phe-Met-Arg-Phe-NH2 as one of its transmitters.

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“…In Asperspina, 5-HT-LIR perikarya are generally restricted to the major ganglia of the CNS, where cell bodies form clusters in specific regions of each ganglion, similar to the distribution of serotonergic perikarya in the ganglia of other larger opisthobranchs (Langley and Langley, 1986;Moroz et al, 1997;Sudlow et al, 1998). For example, in the notaspid Pleurobranchaea californica MacFarland, 1966, and the nudibranch Tritonia diomedea Bergh, 1894, serotonergic cells cluster in the dorsal region of the cerebropleural ganglia (Sudlow et al, 1998).…”

Section: Discussionmentioning

confidence: 99%

“…Based on analyses of P. californica, at least one subgroup of these serotonergic neurons contributes to a pattern generator pathway involved in the swimming escape response (Jing and Gillette, 1999). Interestingly, no serotonergic perikarya occupy the pleural region of the cerebro-pleural ganglia in P. californica or T. diomedea; similarly, no serotonergic perikarya are present in the pleural ganglia of the anaspid Aplysia californica Cooper, 1863 (Langley and Langley, 1986), and none were detected in the right pleural ganglion of Asperspina (see Fig. 5).…”

Section: Discussionmentioning

confidence: 99%

Serotonin-like Immunoreactivity in the Central and Peripheral Nervous Systems of the Interstitial AcochlideanAsperspinasp. (Opisthobranchia)

Hochberg

2007

The Biological Bulletin

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Abstract. Species of Acochlidea are common members of the marine interstitial environment and defined in part by their minuscule size and highly divergent morphology relative to other benthic opisthobranchs. Despite these differences, acochlideans such as species of Asperspina display many plesiomorphic characteristics, including an unfused condition of their neural ganglia. To gain insight into the distribution of specific neural subsets within acochlidean ganglia, a species of Asperspina was studied by using antiserotonin immunohistochemistry and epifluorescence and confocal laser scanning microscopy. Results reveal similarities between Asperspina and larger opisthobranchs in the general distribution of serotonergic perikarya in the central nervous system. Specifically, the arrangement of perikarya into regional clusters within the cerebral and pedal ganglia and the absence of immunoreactive perikarya in the pleural ganglia are similar to the model species of Aplysia californica, Pleurobranchaea californica, and Tritonia diomedea. Moreover, serotonergic innervation of the rhinophores in all opisthobranchs, including Asperspina sp., originates from the cerebral ganglion instead of directly from the rhinophoral ganglion. Serotonergic innervation of the body wall, including the epithelium, muscles, and pedal sole, appears to arise exclusively from pedal and accessory ganglia. These observations indicate a general conservation of serotoninlike immunoreactivity in the central and peripheral nervous systems of acochlidean and other benthic opisthobranchs.

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Serotonin immunoreactivity of neurons in the gastropod Aplysia californica

Cited by 95 publications

References 40 publications

Metamodulation of the Crayfish Escape Circuit

Metamodulation of the Crayfish Escape Circuit

Tail shock produces inhibition as well as sensitization of the siphon-withdrawal reflex of Aplysia: possible behavioral role for presynaptic inhibition mediated by the peptide Phe-Met-Arg-Phe-NH2.

Serotonin-like Immunoreactivity in the Central and Peripheral Nervous Systems of the Interstitial AcochlideanAsperspinasp. (Opisthobranchia)

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