Long-term expansion and sensitization of mechanosensory receptive fields in Aplysia support an activity-dependent model of whole-cell sensory plasticity

Abstract

Long-term changes in peripheral receptive field properties of mechanosensory/nociceptive neurons were investigated 1-3 weeks after noxious stimulation. Noxious stimuli consisted of a deep penetrating cut through the middle of the tail, strong electric shock applied to the tail surface, or a combination of deep and superficial tail stimulation. Action potentials evoked in the tail were monitored with intracellular electrodes in central somata of tail sensory neurons. Three long-term changes in receptive field properties were produced in the region of noxious stimulation: (1) mechanosensory thresholds decreased, (2) receptive field areas increased, and (3) the percentage of cells showing receptive field extension across the tail midline increased. Sizes and shapes of individual receptive fields did not vary during extensive testing of tails perfused with artificial seawater or during testing in cobalt solutions that block synaptic transmission. This stability of receptive field geometry, coupled with the observation that increased peripheral excitability in these cells does not increase receptive field size, suggests that long-term receptive field alterations involve growth of peripheral sensory processes. A model is proposed in which the signaling strength of the entire sensory cell increases in response to trauma of its receptive field. In this model long-term enhancement of central and peripheral sensory responsiveness is selectively triggered by activity dependent extrinsic modulation of the centrally located soma, which accelerates synthesis of growth-associated proteins used in collateral and regenerative sprouting of traumatized peripheral processes.