The thalamocortical and corticothalamic conections of AI, AII, and the anteriior auditory field (AFF) in the cat: Evidence ofr two largely sergregarted systems of connections

Abstract

The thalamocortical and corticothalamic connections of the three cortical auditory fields—first (AI), second (AII), and anterior (AAF)—were defined using anterograde and retrograde tracing techniques. Microinjections of tracers were placed at one or two different physiologically identified loci after these fields had been mapped using microelectrode recording techniques. This approach ensured that the injections were well within the borders of each field that was studied. By making injections at different positions in the cochleotopic representations in A1 and AAF the systematic topographies of the connections between these cortical fields and the medial geniculate body subdivisions were determined. The thalamocortical and corticothalamic reciprocal projections of single loci in AI were from and to single columns passing rostrocaudally through the deep dorsal nucleus (Dd) and medial division (M) of the medial geniculate body (MGB) and from and to folded sheets of labelled neurons passing rostrocaudally through pars lateralis (VI) and pars ovoidea (Vo) of the ventral division. The connections of AI with VI and Vo were very strong. There were also thalamocortical and corticothalamic connections between the lateral division of the posterior group of thalamus (Pol) and single loci in AI. The thalamocortical and corticothalamic reciprocal connections of AAF with the auditory thalamus were similar to the A1 connections with the exception that the connections with the ventral division of the MGB were relatively weaker and, in the case of the thalamocortical projection, more discontinuous. AII loci are thalamocortically and corticothalamically connected with the caudal dorsal nucleus (Dc), the ventral lateral nucleus (VL), and the medial division (M). The topography of all connections of AAF and A1 with the MGB varied systematically and was consistent with a cochleotopic organization of connections between the MGB and the two cortical fields. Since the thalamocortical and corticothalamic connections of these three cortical fields are reciprocal, we were able to compare directly their connections in individual cats by introducing anterograde tracer in one field and retrograde tracer in another. While AI and AAF were connected to the same subdivisions of the MGB and had the same systematic topography of connections, the connections of AII and AI (or AAF) were largely segregated (with the only overlap occurring in M). Results of injections introduced into other cortical fields in this study and the results of previous studies by other investigators (Rose and Woolsey, '58; Graybiel, '73; Casseday et al., '76; Winer et al., '77) are consistent with the interpretation that there are two largely segregated connectional systems between the auditory thalamus and cortex: a “cochleotopic system” that includes AI and AAF and a “diffuse system” that includes AII. Small injections of anterograde tracers at higher‐frequency representational sites in AI or AAF, or of retrograde tracer in AI, produced a discontinuous, periodic pattern of dense and light labelling in VI. Reconstructions showed that these discontinuities of label, in three dimensions, formed parallel columns oriented rostrocaudally.