Connections of cat auditory cortex: I. Thalamocortical system

Abstract

Despite the functional importance of the medial geniculate body (MGB) in normal hearing, many aspects of its projections to auditory cortex are unknown. We analyzed the MGB projections to thirteen auditory areas in the cat using two retrograde tracers to investigate thalamocortical nuclear origins, topography, convergence, and divergence. MGB divisions and auditory cortex areas were defined independently of the connectional results using architectonic, histochemical, and immunocytochemical criteria. Each auditory cortex area received a unique pattern of input from several MGB nuclei; and these patterns of input identify four groups of cortical areas distinguished by their putative functional affiliations: tonotopic, non-tonotopic, multisensory, and limbic. Each family of areas received projections from a functionally related set of MGB nuclei; some nuclei project to only a few a few areas (e.g., the MGB ventral division to tonotopic areas), and others project to all areas (e.g., the medial division input to every auditory cortical areas and to other regions). Projections to tonotopic areas had fewer nuclear origins than those to multisensory or limbicaffiliated fields. All projections were organized topographically, even those from non-tonotopic nuclei. The few divergent neurons (mean: 2%) are consistent with a model of multiple segregated streams ascending to auditory cortex. The expanded cortical representation of MGB auditory, multisensory, and limbic affiliated streams appears to be a primary facet of forebrain auditory function. The emergence of several auditory cortex representations of characteristic frequency may be a functional multiplication of the more limited maps in the MGB. This expansion suggests emergent cortical roles consistent with the divergence of thalamocortical connections.

Cortico‐cortical connectivity within ferret auditory cortex

“…Like the primate CM (Recanzone, 2000), both the cat and ferret AAFs have shorter response latencies relative to the A1 and an under‐representation of mid‐frequencies (Imaizumi et al, 2004; Bizley et al, 2005). The AAF in the cat is innervated predominantly by the rostral pole of the MGB and the dorsal division of the MGB, with smaller inputs from the MGBv and MGBm (Imig and Morel, 1983; Morel and Imig, 1987; Lee and Winer, 2008a). Drawing further analogies between the AAF in the ferret and other species therefore awaits detailed investigations of the thalamocortical connectivity.…”

“…Both are innervated by the A1, AAF, A2, and dorsal zone (DZ) of the auditory cortex, although the projection from the AAF and DZ is stronger to the PAF than to the VPAF (Rouiller et al, 1991; Imig and Reale, 1980). The PAF is innervated by the dorsal suprageniculate nucleus, as well as the ventral and dorsal MGB divisions (Lee and Winer, 2008a). Injections in the cat VPAF label projections originating in the caudal MGBv, as well as the laterodorsal nucleus, ventrolateral nucleus, and MGBm (Lee and Winer, 2008a).…”

“…The PAF is innervated by the dorsal suprageniculate nucleus, as well as the ventral and dorsal MGB divisions (Lee and Winer, 2008a). Injections in the cat VPAF label projections originating in the caudal MGBv, as well as the laterodorsal nucleus, ventrolateral nucleus, and MGBm (Lee and Winer, 2008a). Projections from the PAF and VPAF are largely similar, connecting strongly with other tonotopic fields.…”

Connections of cat auditory cortex: III. Corticocortical system

“…Thus, we investigated whether single corticocortical neurons project to more than one area. In the thalamocortical (Lee and Winer, 2008a) and commissural (Lee and Winer, 2008b) systems, we found little such divergence, suggesting that thalamic nuclei and commissural projections are highly specific, even in non-primary areas or in regions devoid of tonotopic organization (Lee et al, 2004a). We also examined projection topography (Lee and Winer, 2005), which orders input and might be reduced in areas without tonotopic maps.…”

“…Understanding how these thalamic and corticocortical inputs contribute to AC computations is challenging without a connectional framework for the many auditory cortical regions, particularly those without systematic representations of characteristic frequency (CF). In cat AC, five areas have such representations (Merzenich et al, 1973;Reale and Imig, 1980;Loftus and Sutter, 2001), and eight more have acoustically responsive cells (Woolsey, 1960;Schreiner and Cynader, 1984;Clarey and Irvine, 1990a;He et al, 1997) and robust auditory thalamic affiliations (Bowman and Olson, 1988b;Shinonaga et al, 1994;Clascá et al, 1997;Lee and Winer, 2008a) without a corresponding CF organization (Schreiner and Winer, 2007). A principled understanding of AC processing must address how such diverse physiological properties are integrated to derive the auditory scene, and how these different computational metrics are established and organized by their connections.…”