Extensive Dual Innervation and Mutual Inhibition by Forelimb and Hindlimb Inputs to Ventroposterolateral Nucleus Projection Neurons in the Rat

Abstract

The stimulation of brachial plexus and sciatic nerve resulted in a precisely timed, synchronous volley of inputs to ventroposterolateral (VPL) neurons from either forelimb or hindlimb. Such stimulation activated sensory fibers of all modalities and was therefore modality-nonspecific. Extracellular recordings of modality-nonspecific single-unit evoked responses from VPL showed that 13% of VPL projection neurons responded to both forelimb and hindlimb inputs. We also demonstrated mutually inhibitory interactions between inputs from forelimb and hindlimb in 45% of VPL units. Unlike the somatotopic map produced by others using modality-specific inputs, the modality-nonspecific evoked response map of VPL had a broadly overlapping distribution of evoked responses. This was especially true for the more caudal aspects of VPL. When the delivery of stimuli was appropriately timed, forelimb inputs caused the inhibition of responses to forelimb stimulation; similarly, hindlimb inputs inhibited responses to forelimb stimulation. The inhibition had a variable duration that may reflect a combination of processes, including recurrent inhibitory collateral input from the thalamic reticular nucleus (TRN) or an intrinsic hyperpolarizing inhibitory afterpotential of the VPL neuron. The presence of an extensive converging input on VPL neurons and an inhibitory correlate to this overlapping of inputs may explain the shifting of VPL maps following lesions of peripheral nerve, spinal cord, or dorsal column nuclei (DCN).