Cutaneous activation of the inhibitory L30 interneurons provides a mechanism for regulating adaptive gain control in the siphon withdrawal reflex of Aplysia

Abstract

The functional role of inhibition in the neural network underlying the siphon withdrawal response (SWR) of Aplysia was assessed by examining a recurrent circuit comprised of identified inhibitory interneurons (L30s), and excitatory interneurons (L29s). We previously showed that activity-dependent potentiation of the L30 inhibitory synapse onto L29 can regulate the net excitatory input elicited by tactile siphon stimulation onto siphon motor neurons (LFS cells) (Fischer and Carew, 1993a). To explore the functional significance of L30 potentiated inhibition, we have examined how a behaviorally relevant stimulus that activates the L30 interneurons modulates the SWR circuit. Utilizing a reduced preparation, we show that weak tactile stimulation of the tail strongly activates the L30s, and leads to significant potentiation of the L30 synapse. Next, we demonstrate that similar weak tail stimulation produces significant inhibition of siphon tap-evoked responses in both L29 interneurons and LFS motor neurons. We further show that this form of inhibition is transient, having a time course of approximately 60 sec. Finally, we directly tested the role of the L30s in mediating this form of inhibition by hyperpolarizing two (of three) L30 interneurons during tail stimulation. L30 inactivation significantly attenuated tail stimulation-induced inhibition of siphon-evoked input to both L29 interneurons and LFS motor neurons. Based on these results, we suggest that L30-potentiated inhibition may have an important adaptive role in optimizing the signal-to-noise ratio for activation of the SWR circuit by providing stabilization of SWR responsiveness under a wide range of environmental conditions.