Simultaneous reorganization in thalamocortical ensembles evolves over several hours after perioral capsaicin injections

Reorganization of the somatosensory system was quantified by simultaneously recording from single-unit neural ensembles in the whisker regions of the ventral posterior medial (VPM) nucleus of the thalamus and the primary soma tosensory (SI) cortex in anesthetized rats before, during, and after inject ing capsaicin under the skin of the lip. Capsaicin, a compound that excites and then inactivates a subset of peripheral C and A delta fibers, triggere d increases in spontaneous firing of thalamocortical neurons (10-15 min aft er injection), as well as rapid reorganization of the whisker representatio ns in both the VPM and SI. During the first hour after capsaicin injection, 57% of the 139 recorded neurons either gained or lost at least one whisker response in their receptive fields (RFs). Capsaicin-related changes contin ued to emerge for greater than or equal to 6 h after the injection: Fifty p ercent of the single-neuron RFs changed between 1-2 and 5-6 h after capsaic in injection. Most (79%) of these late changes represented neural responses that had remained unchanged in the first postcapsaicin mapping; just under 20% of these late changes appeared in neurons that had previously shown no plasticity of response. The majority of the changes (55% immediately after injection, 66% 6 h later) involved "unmasking" of new tactile responses. R F change rates were comparable in SI and VPM (57-49%). Population analysis indicated that the reorganization was associated with a lessening of the "s patial coupling" between cortical neurons-a significant reduction in firing covariance that could be related to distances between neurons. This genera l loss of spatial coupling, in conjunction with increases in spontaneous fi ring, may create a situation that is favorable for the induction of synapti c plasticity. Our results indicate that the selective inactivation of a per ipheral nociceptor subpopulation can induce rapid and long-evolving (greate r than or equal to 6 h) shifts in the balance of inhibition and excitation in the somatosensory system. The time course of these processes suggest tha t thalamic and cortical plasticity is not a linear reflection of spinal and brainstem changes that occur following the application of capsaicin.