Exp Brain Res (1991) 86:506-517 BrainR 9 Springer-Verlag 1991 Corticofugal modulation of the information processing in the auditory thalamus of the cat A.E.P. Villa, E.M. Rouiller*, G.M. Simm, P. Zurita, Y. de Ribaupierre, and F. de Ribaupierre Institut de Physiologie, Universit6 de Lausanne, Rue du Bugnon 7, CH-1005 Lausanne, Switzerland Received October 22, 1990 / Accepted April 24, 1991 Summary. Single unit activity of 355 cells was recorded in the auditory thalamus of anesthetized cats before, during, and after the inactivation by cooling of the ipsilateral primary auditory cortex (AI). Most of the units (n = 288) showed similar functional characteristics of firing before and after the cryogenic blockade of AI. The spontaneous firing rate remained unchanged by cooling in 20% of the units and decreased in the majority of them (60%). In some regions, i.e. dorsal division of the medial geniculate body (MGB), lateral part of the posterior group of the thalamus, and auditory sector of the reticular nucleus of the thala- mus, the maximum firing rate evoked by white noise bursts was generally affected by cooling in the same direction and to the same extent as the spontaneous activity. Units in the ventral division of MGB showed a characteristic increase of signal-to-noise ratio during cortical cooling. The corti- cofugal modulation led to the appearance or disappear- ance of the best frequency of tuning in 51 units and changed it by more than 0.5 octave in 34 units. The bandwidths of different response patterns to pure tones stimulation were used to define a set of functional proper- ties. During cryogenic blockade of AI, two cortically modulated sub-populations of units were usually dis- tinguished that exhibited changes for a given functional property. The complexity and diversity of the effects of cortical inactivation suggest that the corticothalamic pro- jection may be the support for selective operations such as an adaptive filtering of the incoming acoustic signal at the thalamic level adjusted as a function of cortical activity. Key words: Cryogenic blockade - Corticofugal modu- lation - Spontaneous activity - Acoustically driven activ- ity Temporal response pattern Adaptive filtering - Cat * Present address: Institut de Physiotogie, Universit6 de Fribourg, P6rolles, CH-1700 Fribourg, Switzerland Offprint requests to: A.E.P. Villa (address see above) Introduction The medial geniculate body (MGB) is the main nucleus of the auditory thalamus (Rose and Galambos 1952; Morest 1964). Based on cytoarchitectonics, the MGB of the cat has been subdivided into dorsal, ventral, and medial divisions. These subdivisions roughly correspond to par- allel ascending auditory pathways (Calford and Aitkin 1983; Winer 1988). The dorsal division (D) sends its projections mainly to the secondary auditory cortex (AII) (Winer et al. 1977; Andersen et al. 1980). The ventral division of the MGB is known to be tonotopically organ- ized (Purser and Whitfield 1972; Aitkin and Webster 1972; Morel et al. 1987) and it is subdivided into pars lateralis (LV) and pars ovoidea (OV). The cortical targets of LV abd OV are the tonotopically organized primary (AI), anterior, and posterior auditory fields (Andersen et at. 1980; Morel and Imig 1987). The medial division of MGB (M) projects to all the auditory cortical fields (Morel and Imig 1987; Rouiller et al. 1989). The laminar distribution of this projection is very different from that of the ventral and dorsal divisions because the relay cells of M send axons into the cortical layer I, whereas the relay cells of the other divisions send their axons to cortical layers IV and VI (Mitani et al. 1987). All divisions of the MGB receive descending influences directly by corticofugal projections (Andersen et al. 1980) and via the reticular nucleus of the thalamus (RE) (Jones 1975; Rouiller et al. 1985; Villa 1990). The other thalamic nuclei related to the auditory pathway are the lateral part of the posterior group of the thalamus (POL) (Heath and Jones 1971; Morel and Imig 1987), the suprageniculate nucleus (SG) (Winer 1988), and the nucleus of the brachium of the inferior colliculus (BIN) (Morest 1964). Thalamocortical and corticothalamic pathways gen- erally establish reciprocal connections (Andersen et al. 1980), although local discontinuities have been reported (Winer 1988). The role and nature of corticofugal projec- tions have been extensively investigated but controversial data have been reported in the literature of the auditory pathway. Several authors suggested an inhibitory role of507 the corticofugal projections (Desmedt and Mechelse 1958; Watanabe et al. 1966; Amato et al. 1969), whereas others did not report any corticofugal effect on the thalamus (Aitkin and Dunlop 1969). Complex effects, mixing excita- tions, and inhibitions have been reported (Ryugo and Weinberger 1976) and a clearly excitatory or facilitatory role has also been suggested (Orman and Humphrey 1981). Thalamo-cortical integration and cortico-thalamic feedback represent a general feature of the sensory chan- nels in the central nervous system. Parallel pathways in the sensory systems might be described to some extent (Dia- mond 1983). It is of interest to notice that evidence from studies in the visual (Kalil and Chase 1970; Singer 1977; Tsumoto et al. 1978) and somatic (Macchi et al. 1986; Yuan et al. 1986) systems show that corticofugal fibers excite the principal sensory nuclei of the thalamus. The purpose of the present study is to clarify the controversy on the nature of the corticothalamic projec- tions in the auditory thalamus by reversibly inactivating the primary auditory cortex (AI) by means of cortical cooling while recording single unit responses in histologi- cally identified thalamic nuclei. The spontaneous and acoustically driven activity of each unit was studied before, during, and after the cortical blockade. New forms of data presentation are introduced in order to investigate in more detail than previously the functional significance of the corticothalamic projection. The data have been acquired by simultaneous recordings from independently driven microelectrodes (Villa 1988). This study focuses on