Abstract
SummaryRecent 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 [1]. We investigated another decision-making strategy, derived from the classical ethological literature [2, 3], 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 [4, 5] and feeding [6] 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.
Highlights
To investigate the interneuronal mechanisms underlying this behavioral choice, we developed a semi-intact preparation (Figure 2A) that allowed the application of tactile and sucrose stimuli to the lips while recording identified neurons from the feeding and withdrawal networks [7, 8]
We discovered that behavioral choice depends on the interaction between two unique types of interneurons
The second type, Pedal-Dorsal12 (PeD12), is a newly discovered interneuron (Figures 2A and S1A available online) that plays a critical role in behavioral choice by providing the synaptic pathway that underlies the competitive interaction between the otherwise autonomous feeding and withdrawal-response networks
Summary
As predicted by the Tinbergen hierarchical model of behavioral choice [2], tactile stimuli that evoke whole-body withdrawal responses in Lymnaea significantly inhibit feeding even in the presence of a strong feeding stimulus (Figure 1). To investigate the interneuronal mechanisms underlying this behavioral choice, we developed a semi-intact preparation (Figure 2A) that allowed the application of tactile and sucrose stimuli to the lips while recording identified neurons from the feeding and withdrawal networks [7, 8].
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