HETEROSYNAPTIC FACILITATION OF TAIL SENSORY NEURON SYNAPTIC TRANSMISSION DURING HABITUATION IN TAIL-INDUCED TAIL AND SIPHON WITHDRAWAL REFLEXES OF APLYSIA

In cellular studies of habituation, such as in the gill and siphon wit hdrawal reflex to tactile stimulation of the siphon of Aplysia, a mech anism that has emerged as an explanation for response decrement during habituation is homosynaptic depression at sensory neurons mediating t he behavioral response. We have examined the contribution of homosynap tic depression to habituation in sensory neurons that contribute to tw o reflex behaviors in Aplysia, tail withdrawal and siphon withdrawal, both elicited by threshold-level tail stimulation. In a companion pape r (this issue), we reported that repeated tail stimulation, identical to that producing habituation in siphon withdrawal in freely moving an imals, also produces habituation in reduced preparations. In this pape r, we extend these behavioral findings by showing that in reduced prep arations, identical tail stimulation also produces habituation of the tail withdrawal reflex. In addition, our cellular experiments show tha t (1) identified sensory and motor neurons in both reflex systems resp ond to identical repeated tail stimulation; in sensory neurons it prod uces a progressive decrease in spike number and increase in spike late ncy, and in motor neurons it produces progressive decrement in complex EPSPs and spike output. (2) Homosynaptic depression of the tail senso ry neuron to tail motor neuron synapse does occur when the sensory neu rons are activated repetitively by intracellular current. (3) Homosyna ptic depression at this synapse does not occur when the sensory neuron s are activated repetitively by threshold-level tail stimuli that elic it the behavioral reflex and cause habituation; rather, the sensory ne urons exhibit significant heterosynaptic facilitation. Thus, in these reflexes, habituation is not accompanied by homosynaptic depression at the sensory neurons, suggesting that the plasticity underlying habitu ation occurs primarily at interneuronal sites.