Imunocytochemical localization and direct assays of serotonin-containing neurons in Aplysia

Ono, Joyce K.; McCaman, Richard E.

doi:10.1016/0306-4522(84)90044-7

Cited by 109 publications

(66 citation statements)

References 31 publications

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“…These results are consistent with those of Ono and McCaman (1984), who found differences in the serotonin concentration of antiserotonin immunoreactive neurons from the same individual. In immunoreactive cell clusters, nonreacting cells were present, and intracellularly, differences in immunoreactivity were found in the nucleus and the perikaryon.…”

Section: Discussionsupporting

confidence: 94%

“…Immunoreactive cells also appear to be present in this area in juvenile Aplysia (Goldstein et , 1984). In the buccal and pleural ganglia of Aplysia californica, we do not find serotonin-like immunoreactive somata, which is in agreement with results of both Ono and McCaman (1984) and Goldstein et al (1984). Serotonin has been proposed as the transmitter in a left pleural ganglion interneuron which produces heterosynaptic facilitation (Shimahara and Tauc, 1978), but the negative finding for antiserotonin immunoreactive somata in the pleural ganglia suggests that this neuron does not use serotonin as its natural transmitter.…”

Section: Discussionsupporting

confidence: 92%

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Serotonin immunoreactivity of neurons in the gastropod Aplysia californica

Longley¹,

Longley²

1986

J. Neurobiol.

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Serotonergic neurons and axons were mapped in the central ganglia of Aplysia californica using antiserotonin antibody on intact ganglia and on serial sections. Immunoreactive axons and processes were present in all ganglia and nerves, and distinct somata were detected in all ganglia except the buccal and pleural ganglia. The cells stained included known serotonergic neurons: the giant cerebral neurons and the RB cells of the abdominal ganglion. The area of the abdominal ganglion where interneurons are located which produce facilitation during the gill withdrawal reflex was carefully examined for antiserotonin immunoreactive neurons. None were found, but two bilaterally symmetric pairs of immunoreactive axons were identified which descend from the contralateral cerebral or pedal ganglion to abdominal ganglion. Because of the continuous proximity of this pair of axons, they could be recognized and traced into the abdominal ganglion neuropil in each preparation. If serotonin is a facilitating transmitter in the abdominal ganglion, these and other antiserotonin immunoreactive axons in the pleuroabdominal connectives may be implicated in this facilitation.

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Section: Discussionsupporting

confidence: 94%

Section: Discussionsupporting

confidence: 92%

Serotonin immunoreactivity of neurons in the gastropod Aplysia californica

Longley¹,

Longley²

1986

J. Neurobiol.

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“…The neuropil of the pedal ganglion contains a large number of serotonin-immunoreactive neurites ( Fig. 4A; Tritt et al 1983;Ono and McCaman 1984;Nolen and Carew 1994;Wright et al 1995;Marinesco and Carew 2002). As before, only sections with both sensory and motor neuron processes were examined.…”

Section: Proximity Of Serotonergic Input To Sensorimotor Contactsmentioning

confidence: 99%

Quantitation of Contacts Among Sensory, Motor, and Serotonergic Neurons in the Pedal Ganglion of Aplysia

Zhang¹,

Wainwright²,

Byrne³

et al. 2003

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Present models of long-term sensitization in Aplysia californica indicate that the enhanced behavioral response is due, at least in part, to outgrowth of sensory neurons mediating defensive withdrawal reflexes. Presumably, this outgrowth strengthens pre-existing connections by formation of new synapses with follower neurons. However, the relationship between the number of sensorimotor contacts and the physiological strength of the connection has never been examined in intact ganglia. As a first step in addressing this issue, we used confocal microscopy to examine sites of contact between sensory and motor neurons in naive animals. Our results revealed relatively few contacts between physiologically connected cells. In addition, the number of contact sites was proportional to the amplitude of the EPSP elicited in the follower motor neuron by direct stimulation of the sensory neuron. This is the first time such a correlation has been observed in the central nervous system. Serotonin is the neurotransmitter most closely examined for its role in modulating synaptic strength at the sensorimotor synapse. However, the structural relationship of serotonergic processes and sensorimotor synapses has never been examined. Surprisingly, serotonergic processes usually made contact with sensory and motor neurons at sites located relatively distant from the sensorimotor synapse. This result implies that heterosynaptic regulation is due to nondirected release of serotonin into the neuropil.

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“…A more complete understanding of the roles of the SCPs and serotonin in behavioral plasticity of the defensive withdrawal reflex must await the identification and characterization of those peptidergic and serotonergic neurons whose processes project to the siphon sensory neurons. Only two group of facilitator neurons have so far been identified, the L28 and L29 cells (14), and neither of these contains immunoreactive SCPB (33) or serotonin (12,13). Rather the L29 cells appear to contain yet a fourth facilitatory transmitter (27).…”

Section: Scp Fpscilitates Synaptic Transmission From Siphon Sensorymentioning

confidence: 99%

Two endogenous neuropeptides modulate the gill and siphon withdrawal reflex in Aplysia by presynaptic facilitation involving cAMP-dependent closure of a serotonin-sensitive potassium channel.

Abrams¹,

Castellucci²,

Camardo³

et al. 1984

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

225

159

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We have found that two endogenous neuropeptides in Aplysia, the small cardioactive peptides SCPA and SCPB, facilitate synaptic transmission from siphon mechanosensory neurons and enhance the defensive withdrawal reflex that these sensory neurons mediate. Single-channel recording revealed that these peptides close a specific K+ channel, the S channel, which is sensitive to cAMP. Moreover, the peptides increase cAMP levels in these sensory neurons. This reduction in K+ current slows the repolarization of the action potential in these cells, which increases transmitter release. In these actions, the SCPs resemble both noxious sensitizing stimuli, which enhance the reflex, and serotonin. Bioassay of HPLC fractions of abdominal ganglion extracts and immunocytochemistry indicate that both the SCPs and serotonin are present in the ganglion and are found in processes close to the siphon sensory neurons, suggesting that these transmitters may be involved in behavioral sensitization. Recent evidence suggests that one group of identified facilitatory interneurons, the L29 cells, does not appear to contain either the SCPs or serotonin but may use yet another facilitatory transmitter.Thus, it appears that several transmitters can converge to produce presynaptic facilitation in the sensory neurons of the defensive withdrawal reflex. AU of the transmitters studied here, the SCPs and serotonin, act via an identical molecular cascade: cAMP-dependent closure of the S-K' channel, broadening of the presynaptic action potential, and facilitation of transmitter release.Peptide transmitters have been a focus of interest in neurobiology because they often have modulatory effects on behavior (1). However, it has only rarely been possible to relate the behavioral action of a neuropeptide to its cellular action on specific nerve cells (2-4, 38). We here report that two molluscan neuropeptides increase the gain of the gill and siphon withdrawal reflex of Aplysia by presynaptically facilitating transmission from the sensory neurons of the reflex pathway. By combining single-channel and biochemical analyses, we have found that this facilitation involves the cAMP-mediated closure of a specific K+ channel, the recently described S channel (5).This defensive withdrawal reflex in Aplysia is enhanced during two simple forms of learning: sensitization and classical conditioning (6,7). In each case, a noxious stimulus produces presynaptic facilitation of synaptic transmission from the afferent neurons in the reflex, the mechanosensory neurons in the abdominal ganglion that innervate the siphon, to interneurons and motoneurons (8, 9). Although application of serotonin to the abdominal ganglion stimulates the facilitatory actions of noxious stimuli (10,11), there is now evidence from the immunocytochemical studies of Ono and McCaman (12) and Kistler et al. (13) that at least one set of facilitatory interneurons, the L29 cells (14), is not serotonergic. Thus transmitters other than serotonin are involved in sensitization. We were therefore ...

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Imunocytochemical localization and direct assays of serotonin-containing neurons in Aplysia

Cited by 109 publications

References 31 publications

Serotonin immunoreactivity of neurons in the gastropod Aplysia californica

Serotonin immunoreactivity of neurons in the gastropod Aplysia californica

Quantitation of Contacts Among Sensory, Motor, and Serotonergic Neurons in the Pedal Ganglion of Aplysia

Two endogenous neuropeptides modulate the gill and siphon withdrawal reflex in Aplysia by presynaptic facilitation involving cAMP-dependent closure of a serotonin-sensitive potassium channel.

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