Neural mechanism underlying behavioral choice in Pleurobranchaea

Abstract

Feeding behavior normally takes precedence over withdrawal from tactile stimulation in P. californica behavioral hierarchy, an adaptation that presumably prevents withdrawal from food. The neuronal interactions between the feeding and withdrawal motor systems were analyzed to determine the neural mechanisms by which this instance of behavioral choice is mediated. The withdrawal motor system is organized as a simple reflex in which primary sensory inputs activate a withdrawal-command interneuron, which in turn excites a population of withdrawal motoneurons. Sensory inputs also may directly activate the withdrawal motoneurons. A neuronal correlate of the withdrawal response can be evoked by electrical stimulation of the large oral veil nerve and recorded as a characteristic extracellular discharge from the small oral veil nerve. Electrical activation of the feeding system by stomatogastric nerve stimulation suppresses the electrically evoked withdrawal response in semi-intact preparations and in isolated nervous systems. The suppression occurs independently of sensory feedback and is mediated by central neurons. A microelectrode survey of neurons in the feeding motor system revealed a reidentifiable pair of corollary discharge (CD) neurons in the buccal ganglion that is capable of suppressing the withdrawal response. Intracellular analysis of these neurons showed that they are coactive with feeding and capable of fully suppressing withdrawal at physiological discharge frequencies. Silencing both CD neurons by hyperpolarization abolishes most of the suppression of withdrawal output during feeding output. This pair of identified neurons is both necessary and sufficient to account for most of the suppression of withdrawal during feeding. Intracellular recording from putative withdrawal motoneurons while activating the withdrawal motor system revealed a train of large, unitary EPSP [excitatory postsynaptic potential] from a presynaptic neuron, the withdrawal-command neuron. These EPSP occur with the same time course as the withdrawal response, which they presumably underlie. EPSP from this command neuron are abolished by activation of the feeding system or by intracellular stimulation of the aforementioned CD neurons. Feeding probably takes precedence over withdrawal in Pleurobranchaea''s behavioral hierarchy because the identified pair of CD neurons that is part of the feeding network inhibits the withdrawal-command neuron. Behavioral choice is probably mediated by inhibitory interactions between competing motor systems.