Organization and development of thalamocortical pathways in the rabbit auditory system.

Abstract

Thalamocortical relations in the rabbit auditory system were investigated by calcium-binding protein immunohistochemistry and neuroanatomical tracing techniques. The differential distribution of the calcium-binding proteins parvalbumin and calbindin delineated four major subdivisions of the medial geniculate body (MGB): the ventral, dorsal, medial and internal nuclei. In addition, several subnuclei that are not easily distinguished by routine Niss1 stains alone were clearly identified. A comparison with previous studies of MGB connectivity suggests that parvalbumin expression is highest in subdivisions that receive substantial input from the central nucleus of the inferior colliculus and that project to primary auditory cortex (AI). In contrast, calbindin expression characterizes nuclei that receive input primarily from other sources and that project to secondary auditory cortex. Anterograde axonal tracing experiments demonstrated that thalamocortical axons originating from coincident cell groups in the ventral division of the MGB (MGV) terminated primarily within patches occupying the full depth of layer IV and the bottom of layer III in primary auditory cortex. Less dense zones of termination were located in layers I and VI. The intermittent distribution of the patches seen in the coronal plane was similar to the distribution of binaural interaction regions in AI. Furthermore, the patches were elongated in the rostral-caudal axis forming bands that parallel the isofrequency contours in AI. Double-labeling experiments employing PV-immunohistochemistry and neuroanatomical tracing indicate that PV is expressed in biochemically distinct thalamocortical and corticothalamic pathways between the MGV and AI. These results are consistent with a model of MGV organization containing functionally distinct, parallel anatomical pathways to primary auditory cortex. Finally, anterograde axonal tracing studies in neonatal animals indicate that the thalamocortical axons segregate into patches in the absence acoustically driven activity. The morphology of individual axons and patches in neonates, however, suggests significant axonal remodeling during postnatal maturation that may be activity dependent. These results are discussed in terms of contribution of thalamocortical afferents to the formation of the functional architecture in auditory neocortex.