TRANSNEURONAL CHANGES OF THE INHIBITORY CIRCUITRY IN THE MACAQUE SOMATOSENSORY THALAMUS FOLLOWING LESIONS OF THE DORSAL COLUMN NUCLEI

The inhibitory circuitry of the ventroposterolateral nucleus (VPL) of the macaque somatosensory thalamus was analyzed in normal animals and in those surviving for a few days or several weeks following a unilate ral lesion of the cuneate nucleus, the source of medial lemniscal (ML) axons carrying information from the contralateral upper extremity. In hibitory synaptic terminals in the VPL were defined as those that cont ain flattened or pleomorphic synaptic vesicles and that can be shown t o be immunoreactive for gamma-aminobutyric acid (GABA). There are two types of these profiles: F axon terminals that arise from neurons of t he thalamic reticular nucleus, and perhaps from VPL local circuit neur ons (LCNs); and the dendritic appendages of LCNs that form presynaptic dendrites (PSDs). ML terminals normally have extensive synaptic inter actions with PSDs but not with F axon terminals. Electron microscopic analyses revealed that cuneatus lesions resulted in a rapid loss of ML terminals and a statistically significant reduction in both F and PSD synaptic profiles. Confocal scanning microscopy also demonstrated a p rofound loss of GABA immunoreactivity in the deafferented VPL. These c hanges persisted for more than 20 weeks, without any evidence of react ive synaptogenesis of surviving sensory afferents or of inhibitory syn apses. The changes in GABA circuitry are transneuronal, and the possib le mechanisms that may underlie them are discussed. It is suggested th at the altered GABAergic circuitry of the VPL in the monkey may serve as a model for understanding changes in somatic sensation in the human following peripheral or central deafferentation. (C) 1996 Wiley-Liss, Inc.