Ontogeny of serotonin-immunoreactive neurons in juvenile Aplysia californica

Implications for the development of learning

Thomas G. Nolen, Thomas J. Carew

Research output: Contribution to journalArticle

Abstract

Serotonin has been implicated in both nonassociative learning (sensitization and dishabituation) as well as associative learning (classical conditioning) in Aplysia californica. Dishabituation and sensitization, and their underlying physiological analogs, emerge according to different developmental timetables-sensitization develops 4 to 6 weeks after dishabituation (Rankin & Carew, 1988; Nolen & Carew, 1988; Wright, McCance, Lu, & Carew, 1991). Since the late emergence of sensitization could result from the delayed expression of facilitatory neurotransmitters, we have examined the ontogeny of serotonin immunoreactivity in juvenile A. californica by means of indirect immunohistofluorescence. The purpose of these experiments was to describe the developmental timetable for the expression of serotonin immunoreactivity and to correlate the emergence of immunoreactive neurons with the ontogenetic expression of different forms of learning. While the addition of serotonin-immunoreactive cells tracked the growth of the central nervous system, juveniles contained a relatively higher proportion of immunoreactive cells than adults. Immunoreactive cell bodies were present in the abdominal, cerebral, and pedal ganglia as early as juvenile Stage 9, prior to the emergence of dishabituation in Stage 10. The posterior cerebral cluster (PCC) contained four pairs of immunoreactive cells by Stage 9, including the facilitator CB1, which, as shown in adults, heterosynaptically facilitates siphon sensory neurons. The PCC reached the adult complement of five pairs of cells, by Stage 10, long before the development of sensitization, but at the time corresponding to the emergence of dishabituation. These results suggest that the late emergence of sensitization is not simply a consequence of the late expression of serotonergic facilitatory interneurons.

Original languageEnglish (US)
Pages (from-to)282-295
Number of pages14
JournalBehavioral and Neural Biology
Volume61
Issue number3
DOIs
StatePublished - 1994

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Aplysia
Serotonin
Learning
Neurons
Classical Conditioning
Interneurons
Sensory Receptor Cells
Ganglia
Neurotransmitter Agents
Foot
Central Nervous System
Growth

ASJC Scopus subject areas

  • Physiology

Cite this

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title = "Ontogeny of serotonin-immunoreactive neurons in juvenile Aplysia californica: Implications for the development of learning",
abstract = "Serotonin has been implicated in both nonassociative learning (sensitization and dishabituation) as well as associative learning (classical conditioning) in Aplysia californica. Dishabituation and sensitization, and their underlying physiological analogs, emerge according to different developmental timetables-sensitization develops 4 to 6 weeks after dishabituation (Rankin & Carew, 1988; Nolen & Carew, 1988; Wright, McCance, Lu, & Carew, 1991). Since the late emergence of sensitization could result from the delayed expression of facilitatory neurotransmitters, we have examined the ontogeny of serotonin immunoreactivity in juvenile A. californica by means of indirect immunohistofluorescence. The purpose of these experiments was to describe the developmental timetable for the expression of serotonin immunoreactivity and to correlate the emergence of immunoreactive neurons with the ontogenetic expression of different forms of learning. While the addition of serotonin-immunoreactive cells tracked the growth of the central nervous system, juveniles contained a relatively higher proportion of immunoreactive cells than adults. Immunoreactive cell bodies were present in the abdominal, cerebral, and pedal ganglia as early as juvenile Stage 9, prior to the emergence of dishabituation in Stage 10. The posterior cerebral cluster (PCC) contained four pairs of immunoreactive cells by Stage 9, including the facilitator CB1, which, as shown in adults, heterosynaptically facilitates siphon sensory neurons. The PCC reached the adult complement of five pairs of cells, by Stage 10, long before the development of sensitization, but at the time corresponding to the emergence of dishabituation. These results suggest that the late emergence of sensitization is not simply a consequence of the late expression of serotonergic facilitatory interneurons.",
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T2 - Implications for the development of learning

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AU - Carew, Thomas J.

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N2 - Serotonin has been implicated in both nonassociative learning (sensitization and dishabituation) as well as associative learning (classical conditioning) in Aplysia californica. Dishabituation and sensitization, and their underlying physiological analogs, emerge according to different developmental timetables-sensitization develops 4 to 6 weeks after dishabituation (Rankin & Carew, 1988; Nolen & Carew, 1988; Wright, McCance, Lu, & Carew, 1991). Since the late emergence of sensitization could result from the delayed expression of facilitatory neurotransmitters, we have examined the ontogeny of serotonin immunoreactivity in juvenile A. californica by means of indirect immunohistofluorescence. The purpose of these experiments was to describe the developmental timetable for the expression of serotonin immunoreactivity and to correlate the emergence of immunoreactive neurons with the ontogenetic expression of different forms of learning. While the addition of serotonin-immunoreactive cells tracked the growth of the central nervous system, juveniles contained a relatively higher proportion of immunoreactive cells than adults. Immunoreactive cell bodies were present in the abdominal, cerebral, and pedal ganglia as early as juvenile Stage 9, prior to the emergence of dishabituation in Stage 10. The posterior cerebral cluster (PCC) contained four pairs of immunoreactive cells by Stage 9, including the facilitator CB1, which, as shown in adults, heterosynaptically facilitates siphon sensory neurons. The PCC reached the adult complement of five pairs of cells, by Stage 10, long before the development of sensitization, but at the time corresponding to the emergence of dishabituation. These results suggest that the late emergence of sensitization is not simply a consequence of the late expression of serotonergic facilitatory interneurons.

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