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Auditory corticocortical interconnections in the cat: evidence for parallel and hierarchical arrangement of the auditory cortical areas

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Summary

The origin and laminar arrangement of the homolateral and callosal projections to the anterior (AAF), primary (AI), posterior (PAF) and secondary (AII) auditory cortical areas were studied in the cat by means of electrophysiological recording and WGA-HRP tracing techniques. The transcallosal projections to AAF, AI, PAF and AII were principally homotypic since the major source of input was their corresponding area in the contralateral cortex. Heterotypic transcallosal projections to AAF and AI were seen, originating from the contralateral AI and AAF, respectively. PAF received heterotypic commissural projections from the opposite ventroposterior auditory cortical field (VPAF). Heterotypic callosal inputs to AII were rare, originating from AAF and AI. The neurons of origin of the transcallosal connections were located mainly in layers II and III (70–92%), and less frequently in deep layers (V and VI, 8–30%). Single unit recordings provided evidence that both homotypic and heterotypic transcallosal projections connect corresponding frequency regions of the two hemispheres. The regional distribution of the anterogradely labeled terminals indicated that the homotypic and heterotypic auditory transcallosal projections are reciprocal. The present data suggest that the transcallosal auditory interconnections are segregated in 3 major parallel components (AAF-AI, PAF-VPAF and AII), maintaining a segregation between parallel functional channels already established for the thalamocortical auditory interconnections. For the intrahemispheric connections, the analysis of the retrograde tracing data revealed that AAF and AI receive projections from the homolateral cortical areas PAF, VPAF and AII, whose neurons of origin were located mainly in their deep (V and VI) cortical layers. The reciprocal interconnections between the homolateral AAF and AI did not show a preferential laminar arrangement since the neurons of origin were distributed almost evenly in both superficial (II and III) and deep (V and VI) cortical layers. On the contrary, PAF received inputs from the homolateral cortical fields AAF, AI, AII and VPAF, originating predominantly from their superficial (II and III) layers. The homolateral projections reaching AII originated mainly from the superficial layers of AAF and AI, but from the deep layers of VPAF and PAF. The laminar distribution of anterogradely labeled terminal fields, when they were dense enough for a confident identification, was systematically related to the laminar arrangement of neurons of origin of the reciprocal projection: a projection originating from deep layers was associated with a reciprocal projection terminating mainly in layer IV, whereas a projection originating from superficial layers was associated with a reciprocal projection terminating predominantly outside layer IV. This laminar distribution indicates that the homolateral auditory cortical interconnections have a feed-forward/feed-back organization, corresponding to a hierarchical arrangement of the auditory cortical areas, according to criteria previously established in the visual system of primates. The principal auditory cortical areas could be ranked into 4 distinct hierarchical levels. The tonotopically organized areas AAF and AI represent the lowest level. The second level corresponds to the non-tonotopically organized area AII. Higher, the tonotopically organized areas VPAF and PAF occupy the third and fourth hierarchical levels, respectively.

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Abbreviations

AAF:

anterior auditory cortical area

AI:

primary auditory cortical area

AII:

secondary auditory cortical area

BF:

best frequency

C:

cerebral cortex

CA:

caudate nucleus

CL:

claustrum

D:

dorsal nucleus of the dorsal division of the MGB

ea:

anterior ectosylvian sulcus

ep:

posterior ectosylviansulcus

IC:

internal capsule

LGN:

lateral geniculate nucleus

LV:

pars lateralis of the ventral division of the MGB

LVe:

lateral ventricule

M:

pars magnocellularis of the medial division of the MGB

MGB:

medial geniculate body

MGBv:

ventral division of the MGB

OT:

optic tract

OV:

pars ovoidea of the ventral division of the MGB

PAF:

posterior auditory cortical area

PH:

parahippocampal cortex

PO:

lateral part of the posterior group of thalamic nuclei

PU:

putamen

RE:

reticular complex of thalamus

rs:

rhinal sulcus

SG:

suprageniculate nucleus of the dorsal division of the MGB

ss:

suprasylvian sulcus

TMB:

tetrametylbenzidine

VBX:

ventrobasal complex

VLa:

ventrolateral complex

VL:

ventro-lateral nucleus of the ventral division of the MGB

WGA-HRP:

wheat germ agglutinin conjugated to horse-radish peroxidase

WM:

white matter

VPAF:

ventro-posterior auditory cortical area

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Authors and Affiliations

  1. Department of Physiology, University of Lausanne, Rue du Bugnon 7, CH-1005, Lausanne, Switzerland

    E. M. Rouiller, G. M. Simm, A. E. P. Villa, Y. de Ribaupierre & F. de Ribaupierre

  2. Department of Physiology, University of Fribourg, Rue du Musée 5, CH-1700, Fribourg, Switzerland

    E. M. Rouiller

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  1. E. M. Rouiller
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  2. G. M. Simm
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  3. A. E. P. Villa
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  4. Y. de Ribaupierre
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  5. F. de Ribaupierre
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Rouiller, E.M., Simm, G.M., Villa, A.E.P. et al. Auditory corticocortical interconnections in the cat: evidence for parallel and hierarchical arrangement of the auditory cortical areas. Exp Brain Res 86, 483–505 (1991). https://doi.org/10.1007/BF00230523

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