The role of GABA-mediated inhibition in the rat ventral posterior medial thalamus. I. Assessment of receptive field changes following thalamic reticular nucleus lesions.

1. Changes in the receptive field (RF) properties of thalamic VPM neurons were assessed quantitatively using single-unit recording techniques following a selective excitotoxic lesion of the ipsilateral thalamic reticular nucleus (TRN). The response profiles to controlled deflections of the contralateral vibrissae were obtained from 97 VPM neurons in normal and 102 VPM neurons in TRN-lesioned animals. 2. Histological signs of TRN lesions were detectable in Nissl-stained sections as early as 20 h after the release of kainic acid into TRN. 3. The average RF size of VPM neurons in normal animals was 2.39 +/- 0.18 whiskers (mean +/- SE). Immediately after the lesion of TRN, the average RF size in VPM was enlarged significantly and remained expanded for as long as 1 mo after the destruction of TRN (7.64 +/- 0.47 whiskers, P < 0.001). 4. Subsequent lesions of trigeminal subnucleus interpolaris (SpVi) in TRN-lesioned animals produced a marked reduction in the RF size of VPM neurons. The average VPM RF size for TRN/SpVi lesioned animals was 2.14 +/- 0.64 whiskers. 5. The loss of inhibition from TRN increased the average response probability and magnitude to the center RF whisker by 38 and 34%, respectively. The response probability and magnitude of the surround RF whiskers increased by 64 and 69%, respectively. The average response latencies to the center and surround RF whiskers were significantly longer after the lesion of TRN; subsequent lesions of SpVi in TRN-lesioned cases reduced the average response latencies of VPM neurons to those seen in normal animals. 6. The RF of VPM neurons in both normal and TRN lesioned cases displayed a strong anterior-posterior ("row") preference. Immediately adjacent anterior-posterior whiskers were twice as likely to elicit a response in VPM than immediately adjacent dorsal-ventral whiskers. 7. VPM units were tested for a preferential response to whisker movement in one of four directions (up, down, backward, and forward). The majority of the neurons in both normal and TRN-lesioned cases showed direction-selective responses, mostly in the up direction. Thus gamma-aminobutyric acid (GABA)-mediated inhibition in rat VPM does not appear to be responsible for direction selectivity of VPM neurons. 8. Virtually all neurons in rat VPM after TRN lesions displayed responses that were sustained for the duration of the stimulus (25.5% in normal vs. 88.2% in TRN-lesioned cases). VPM units showing sustained (tonic) responses maintained a high rate of spontaneous activity and, on average, responded to 2-3 times more whiskers than phasically responding units.(ABSTRACT TRUNCATED AT 400 WORDS)