Tonotopic Control of Auditory Thalamus Frequency Tuning by Reticular Thalamic Neurons

Abstract

GABAergic cells of the thalamic reticular nucleus (TRN) can potentially exert strong control over transmission of information through thalamus to the cerebral cortex. Anatomical studies have shown that the reticulo-thalamic connections are spatially organized in the visual, somatosensory, and auditory systems. However, the issue of how inhibitory input from TRN controls the functional properties of thalamic relay cells and whether this control follows topographic rules remains largely unknown. Here we assessed the consequences of increasing or decreasing the activity of small ensembles of TRN neurons on the receptive field properties of medial geniculate (MG) neurons. For each MG cell, the frequency tuning curve and the rate-level function were tested before, during, and after microiontophoretic applications of GABA, or of glutamate, in the auditory sector of the TRN. For 66 MG cells tested during potent pharmacological control of TRN activity, group data did not reveal any significant effects. However, for a population of 20/66 cells (all but 1 recorded in the ventral, tonotopic, division), the breadth of tuning, the frequency selectivity and the acoustic threshold were significantly modified in the directions expected from removing, or reinforcing, a dominant inhibitory input onto MG cells. Such effects occurred only when the distance between the characteristic frequency of the recorded ventral MG cell and that of the TRN cells at the ejection site was <0.25 octaves; they never occurred for larger distances. This relationship indicates that the functional interactions between TRN cells and ventral MG cells rely on precise topographic connections.