Directional avoidance turns encoded by single interneurons and sustained by multifunctional serotonergic cells

Jian Jing, Rhanor Gillette

Research output: Contribution to journalArticle

Abstract

Avoidance turns in the sea slug Pleurobranchaea are responses to noxious stimuli and replace orienting turns to food stimuli after avoidance conditioning or satiation. Avoidance turns proved to be centrally patterned behaviors, the fictive expression of which could be elicited in reduced preparations and the isolated CNS. Activity in one of a bilateral interneuron pair, the A4 cells, was necessary and sufficient to drive the avoidance turn toward the contralateral side. Single A4 cells appeared to encode both turn direction and angle, in contrast to directional behaviors of other animals in which displacement angle is usually encoded by multiple units. The As1-4 cells, bilateral serotonergic cell clusters, excited the prolonged A4 burst during the turn through electrical and chemical coupling. However, during the escape swim, As1-4 became integral elements of the swim motor network, and A4 activity was entrained to the swim rhythm by alternating excitatory-inhibitory inputs, with only weak spiking. This provides a likely mechanism for the previously observed suppression of the avoidance turn by escape swimming. These observations add significant new aspects to the multiplying known functions of As1-4 and their homologs in other molluscs and point to a pivotal role of these neurons in the organization of gastropod behavior. Simple functional models predict (1) the essential actions of inhibitor neurons in the directionality of the turning network motor output and (2) an integrating role for As1-4 in the behavioral switch between turning avoidance and swimming escape, on the basis of their response to increasing stimulus intensity.

Original languageEnglish (US)
Pages (from-to)3039-3051
Number of pages13
JournalJournal of Neuroscience
Volume23
Issue number7
StatePublished - Apr 1 2003

Fingerprint

Interneurons
Gastropoda
Pleurobranchaea
Satiation
Neurons
Animal Behavior
Mollusca
Oceans and Seas
Food

Keywords

  • Avoidance behavior
  • Behavioral decision
  • Central pattern generator
  • Directional behavior
  • Escape swimming
  • Mollusc
  • Orienting and avoidance turns
  • Pleurobranchaea
  • Population coding
  • Premotor neurons

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Directional avoidance turns encoded by single interneurons and sustained by multifunctional serotonergic cells. / Jing, Jian; Gillette, Rhanor.

In: Journal of Neuroscience, Vol. 23, No. 7, 01.04.2003, p. 3039-3051.

Research output: Contribution to journalArticle

@article{1e6b53c442c94358963086c13ba0e746,
title = "Directional avoidance turns encoded by single interneurons and sustained by multifunctional serotonergic cells",
abstract = "Avoidance turns in the sea slug Pleurobranchaea are responses to noxious stimuli and replace orienting turns to food stimuli after avoidance conditioning or satiation. Avoidance turns proved to be centrally patterned behaviors, the fictive expression of which could be elicited in reduced preparations and the isolated CNS. Activity in one of a bilateral interneuron pair, the A4 cells, was necessary and sufficient to drive the avoidance turn toward the contralateral side. Single A4 cells appeared to encode both turn direction and angle, in contrast to directional behaviors of other animals in which displacement angle is usually encoded by multiple units. The As1-4 cells, bilateral serotonergic cell clusters, excited the prolonged A4 burst during the turn through electrical and chemical coupling. However, during the escape swim, As1-4 became integral elements of the swim motor network, and A4 activity was entrained to the swim rhythm by alternating excitatory-inhibitory inputs, with only weak spiking. This provides a likely mechanism for the previously observed suppression of the avoidance turn by escape swimming. These observations add significant new aspects to the multiplying known functions of As1-4 and their homologs in other molluscs and point to a pivotal role of these neurons in the organization of gastropod behavior. Simple functional models predict (1) the essential actions of inhibitor neurons in the directionality of the turning network motor output and (2) an integrating role for As1-4 in the behavioral switch between turning avoidance and swimming escape, on the basis of their response to increasing stimulus intensity.",
keywords = "Avoidance behavior, Behavioral decision, Central pattern generator, Directional behavior, Escape swimming, Mollusc, Orienting and avoidance turns, Pleurobranchaea, Population coding, Premotor neurons",
author = "Jian Jing and Rhanor Gillette",
year = "2003",
month = "4",
day = "1",
language = "English (US)",
volume = "23",
pages = "3039--3051",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "7",

}

TY - JOUR

T1 - Directional avoidance turns encoded by single interneurons and sustained by multifunctional serotonergic cells

AU - Jing, Jian

AU - Gillette, Rhanor

PY - 2003/4/1

Y1 - 2003/4/1

N2 - Avoidance turns in the sea slug Pleurobranchaea are responses to noxious stimuli and replace orienting turns to food stimuli after avoidance conditioning or satiation. Avoidance turns proved to be centrally patterned behaviors, the fictive expression of which could be elicited in reduced preparations and the isolated CNS. Activity in one of a bilateral interneuron pair, the A4 cells, was necessary and sufficient to drive the avoidance turn toward the contralateral side. Single A4 cells appeared to encode both turn direction and angle, in contrast to directional behaviors of other animals in which displacement angle is usually encoded by multiple units. The As1-4 cells, bilateral serotonergic cell clusters, excited the prolonged A4 burst during the turn through electrical and chemical coupling. However, during the escape swim, As1-4 became integral elements of the swim motor network, and A4 activity was entrained to the swim rhythm by alternating excitatory-inhibitory inputs, with only weak spiking. This provides a likely mechanism for the previously observed suppression of the avoidance turn by escape swimming. These observations add significant new aspects to the multiplying known functions of As1-4 and their homologs in other molluscs and point to a pivotal role of these neurons in the organization of gastropod behavior. Simple functional models predict (1) the essential actions of inhibitor neurons in the directionality of the turning network motor output and (2) an integrating role for As1-4 in the behavioral switch between turning avoidance and swimming escape, on the basis of their response to increasing stimulus intensity.

AB - Avoidance turns in the sea slug Pleurobranchaea are responses to noxious stimuli and replace orienting turns to food stimuli after avoidance conditioning or satiation. Avoidance turns proved to be centrally patterned behaviors, the fictive expression of which could be elicited in reduced preparations and the isolated CNS. Activity in one of a bilateral interneuron pair, the A4 cells, was necessary and sufficient to drive the avoidance turn toward the contralateral side. Single A4 cells appeared to encode both turn direction and angle, in contrast to directional behaviors of other animals in which displacement angle is usually encoded by multiple units. The As1-4 cells, bilateral serotonergic cell clusters, excited the prolonged A4 burst during the turn through electrical and chemical coupling. However, during the escape swim, As1-4 became integral elements of the swim motor network, and A4 activity was entrained to the swim rhythm by alternating excitatory-inhibitory inputs, with only weak spiking. This provides a likely mechanism for the previously observed suppression of the avoidance turn by escape swimming. These observations add significant new aspects to the multiplying known functions of As1-4 and their homologs in other molluscs and point to a pivotal role of these neurons in the organization of gastropod behavior. Simple functional models predict (1) the essential actions of inhibitor neurons in the directionality of the turning network motor output and (2) an integrating role for As1-4 in the behavioral switch between turning avoidance and swimming escape, on the basis of their response to increasing stimulus intensity.

KW - Avoidance behavior

KW - Behavioral decision

KW - Central pattern generator

KW - Directional behavior

KW - Escape swimming

KW - Mollusc

KW - Orienting and avoidance turns

KW - Pleurobranchaea

KW - Population coding

KW - Premotor neurons

UR - http://www.scopus.com/inward/record.url?scp=0037388707&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0037388707&partnerID=8YFLogxK

M3 - Article

C2 - 12684491

AN - SCOPUS:0037388707

VL - 23

SP - 3039

EP - 3051

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 7

ER -