The Journal of Neuroscience, April 1, 2003, 23(7):3039
Directional Avoidance Turns Encoded by Single Interneurons and
Sustained by Multifunctional Serotonergic Cells
Jian
Jing and
Rhanor
Gillette
Department of Molecular and Integrative Physiology and the
Neuroscience Program, University of Illinois, Urbana, Illinois 61801
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.
Key words:
Pleurobranchaea; orienting and
avoidance turns; directional behavior; population coding; escape
swimming; central pattern generator; mollusc; premotor neurons; avoidance behavior; behavioral decision
Copyright © 2003 Society for Neuroscience 0270-6474/03/2373039-13$05.00/0
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