Interneuronal mechanism for Tinbergen's hierarchical model of behavioral choice

Pirger, Zsolt, Crossley, Michael, Naskar, Souvik, Kemenes, György, O'Shea, Michael, Benjamin, Paul R and Kemenes, Ildikó (2014) Interneuronal mechanism for Tinbergen's hierarchical model of behavioral choice. Current Biology, 24 (17). pp. 2018-2024. ISSN 0960-9822

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Abstract

Recent studies of behavioral choice support the notion that the decision to carry out one behavior rather than another depends on the reconfiguration of shared interneuronal networks. We investigated another decision-making strategy, derived from the classical ethological literature, which proposes that behavioral choice depends on competition between autonomous networks. According to this model, behavioral choice depends on inhibitory interactions between incompatible hierarchically organized behaviors. We provide evidence for this by investigating the interneuronal mechanisms mediating behavioral choice between two autonomous circuits that underlie whole-body withdrawal and feeding in the pond snail Lymnaea. Whole-body withdrawal is a defensive reflex that is initiated by tactile contact with predators. As predicted by the hierarchical model, tactile stimuli that evoke whole-body withdrawal
responses also inhibit ongoing feeding in the presence
of feeding stimuli. By recording neurons from the
feeding and withdrawal networks, we found no direct synaptic connections between the interneuronal and motoneuronal elements that generate the two behaviors. Instead, we discovered that behavioral choice depends on the interaction between two unique types of interneurons with asymmetrical synaptic connectivity that allows withdrawal to override feeding. One type of interneuron, the Pleuro-Buccal (PlB), is an extrinsic modulatory neuron of the feeding network that completely inhibits feeding when excited by touch-induced monosynaptic input from the second type of interneuron, Pedal-Dorsal12 (PeD12). PeD12 plays a critical role in behavioral choice by providing a synaptic pathway joining the two behavioral networks that underlies the competitive dominance of whole-body withdrawal over
feeding.

Item Type: Article
Schools and Departments: School of Life Sciences > Neuroscience
Subjects: Q Science
Q Science > Q Science (General)
R Medicine > RC Internal medicine > RC0321 Neurosciences. Biological psychiatry. Neuropsychiatry
Depositing User: Paul Benjamin
Date Deposited: 09 Sep 2014 12:21
Last Modified: 07 Mar 2017 10:57
URI: http://sro.sussex.ac.uk/id/eprint/49872

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Project NameSussex Project NumberFunderFunder Ref
Lapses in memory: opportunities for adaptive behaviourG1199BBSRC-BIOTECHNOLOGY & BIOLOGICAL SCIENCES RESEARCH COUNCILBB/K018515/1