Diverse excitatory and inhibitory synaptic plasticity outcomes in complex horizontal circuits near a functional border of adult neocortex

Abstract

The primary somatosensory cortex (SI) is topographically organized into a map of the body. This organization is dynamic, undergoing experience-dependent modifications throughout life. It has been hypothesized that excitatory and inhibitory synaptic plasticity of horizontal intracortical connections contributes to functional reorganization. However, very little is known about synaptic plasticity of these connections; particularly the characteristics of inhibitory synaptic plasticity, its relationship to excitatory synaptic plasticity, and their relationship to the functional organization of the cortex. To investigate this, we located the border between the forepaw and lower jaw representation of SI in vivo, and used whole cell-patch electrophysiology to record post-synaptic excitatory and inhibitory currents in complex horizontal connections in vitro. Connections that remained within the representation (continuous) and those that crossed from one representation to another (discontinuous) were stimulated differentially, allowing us to examine differences associated with the border. To induce synaptic plasticity, tetanic stimulation was applied to either continuous or discontinuous pathways. Tetanic stimulation induced diverse forms of excitatory and inhibitory synaptic plasticity, with LTP dominating for excitation and LTD dominating for inhibition. The border did not restrict plasticity in either case. In contrast, tetanization elicited LTP of monosynaptic inhibitory responses in continuous, but not discontinuous connections. These results demonstrate that continuous and discontinuous pathways are capable of diverse synaptic plasticity responses that are differentially inducible. Furthermore, continuous connections can undergo monosynaptic inhibitory LTP, independent of excitatory drive onto interneurons. Thus, coordinated excitatory and inhibitory synaptic plasticity of horizontal connections are capable of contributing to functional reorganization.