Tonotopic Control of Auditory Thalamus Frequency Tuning by Reticular Thalamic Neurons

Abstract

Cotillon-Williams N, Huetz C, Hennevin E, Edeline J-M. Tonotopic control of auditory thalamus frequency tuning by reticular thalamic neurons. J Neurophysiol 99: 1137-1151, 2008. First published December 26, 2007 doi:10.1152/jn.01159.2007. 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 reticulothalamic 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 Ͻ0.25 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. I N T R O D U C T I O NThe thalamus is often considered as a "gate" for the transfer of information to neocortex. Understanding the key factors controlling this gate has been the subject of intense research, but several points remain unresolved. The reticular nucleus of the thalamus (TRN) has a key anatomical position and chemical composition to modulate thalamocortical activity. It receives inputs from both thalamus and cortex and sends outputs back to the thalamus (Jones 1975). Exclusively composed of GABAergic neurons (Arcelli et al. 1997; Benson et al. 1991;Houser et al. 1980), it is a major source of inhibition for all thalamic nuclei . In some species and for some sensory modalities, it is the quasi-exclusive source of inhibition in the thalamus, whereas in others it shares this role with local inhibitory interneurons (reviewed in Jones 1985; Sherman and Guillery 2001). The lateral geniculate nucleus possesses around 20% of inhibitory interneurons in all species (Barbaresi et al. 1986; Benson et al. 1992). The somatosensory thalamus and the auditory thalamus possess 20 -25% of inhibitory interneurons in primate and cat (Benson e...

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