Local circuit properties underlying cortical reorganization.
Peripheral denervation has been shown to cause reorganization of the deafferented somatotopic region in primary somatosensory cortex (S1). However, the basic mechanisms that underlie reorganization are not well understood. In the experiments described in this paper, a novel in vivo/in vitro preparation of adult rat S1 was used to determine changes in local circuit properties associated with the denervation-induced plasticity of the cortical representation in rat S1. In the present studies, deafferentation of rat S1 was induced by cutting the radial and median nerves in the forelimb of adult rats, resulting in a rapid shift of the location of the forepaw/lower jaw border; the amount of the shift increased over the times assayed, through 28 days after denervation. The locations of both borders (i.e., original and reorganized) were marked with vital dyes, and slices from the marked region were used for whole-cell recording. Responses were evoked using electrical stimulation of supragranular S1 and recorded in supragranular neurons close to either the original or reorganized border. For each neuron, postsynaptic potentials (PSPs) were evoked by stimulation of fibers that crossed the border site (CB stim) and by equivalent stimulation that did not cross (NCB stim). Monosynaptic inhibitory postsynaptic potentials (IPSPs) were also examined after blocking excitatory transmission with 15 microM CNQX plus 100 microM DL-APV. The amplitudes of PSPs and IPSPs were compared between CB and NCB stimulation to quantify effects of the border sites on excitation and inhibition. Previous results using this preparation in the normal (i.e., without induced plasticity) rat S1 demonstrated that at a normal border both PSPs and IPSPs were smaller when evoked with CB stimulation than with NCB stimulation. For most durations of denervation, a similar bias (i.e., smaller responses with CB stimulation) for PSPs and IPSPs was observed at the site of the novel reorganized border, while no such bias was observed at the suppressed original border site. Thus changes in local circuit properties (excitation and inhibition) can reflect larger-scale changes in cortical organization. However, specific dissociations between these local circuit properties and the presence of the novel border at certain durations of denervation were also observed, suggesting that there are several intracortical processes contributing to cortical reorganization over time and that excitation and inhibition may contribute differentially to them.
Hickmott
Peter W
PW
Department of Psychology, University of California, Riverside 92521, USA. Peter.hickmott@ucr.edu
Merzenich
Michael M
MM
D000818:Animals; D001931:Brain Mapping; D003714:Denervation; D004594:Electrophysiology; D005528:Foot / Q000294:innervation / Q000502:physiology; D005552:Forelimb / Q000294:innervation / Q000502:physiology; D066298:In Vitro Techniques; D007568:Jaw / Q000502:physiology; D009434:Neural Pathways / Q000502:physiology; D009473:Neuronal Plasticity / Q000502:physiology*; D051381:Rats; D017207:Rats, Sprague-Dawley; D013003:Somatosensory Cortex / Q000502:physiology*; D009435:Synaptic Transmission / Q000502:physiology