Interneuronal mechanism for Tinbergen's hierarchical model of behavioral choice.
Interneuronal mechanism for Tinbergen's hierarchical model of behavioral choice.
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DOI:
10.1016/j.cub.2014.07.044
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发表时间:
2014-09-08
期刊:
影响因子:
9.2
通讯作者:
Kemenes, Ildiko
中科院分区:
文献类型:
--
作者:
Pirger, Zsolt;Crossley, Michael;Laszlo, Zita;Naskar, Souvik;Kemenes, Gyoergy;O'Shea, Michael;Benjamin, Paul R.;Kemenes, Ildiko
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. Behavioral choice between mutually exclusive behaviors is hierarchically organized Touch-induced whole-body withdrawal inhibits sucrose-driven feeding rhythms Two interneurons with asymmetrical connectivity allow withdrawal to override feeding Suppression of feeding is due to the enhancement of tonic inhibition A current model of behavioral choice depends on the reconfiguration of shared interneuronal networks. Pirger et al. provide evidence for the alternative Tinbergen model, which depends on a hierarchically based competition between autonomous networks. An asymmetrical inhibitory interneuronal pathway allows one behavior to dominate the other.
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