Experimental Brain Research

, Volume 86, Issue 3, pp 483–505

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

  • E. M. Rouiller
  • G. M. Simm
  • A. E. P. Villa
  • Y. de Ribaupierre
  • F. de Ribaupierre
Article

DOI: 10.1007/BF00230523

Cite this article as:
Rouiller, E.M., Simm, G.M., Villa, A.E.P. et al. Exp Brain Res (1991) 86: 483. doi:10.1007/BF00230523

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.

Key words

Auditory cortex Corticocortical projections Cortical layers Hearing WGA-HRP tracing Tonotopy Cat 

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

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • E. M. Rouiller
    • 1
    • 2
  • G. M. Simm
    • 1
  • A. E. P. Villa
    • 1
  • Y. de Ribaupierre
    • 1
  • F. de Ribaupierre
    • 1
  1. 1.Department of PhysiologyUniversity of LausanneLausanneSwitzerland
  2. 2.Department of PhysiologyUniversity of FribourgFribourgSwitzerland
  3. 3.Department of PhysiologyFribourgSwitzerland