Double dissociation of 'what' and 'where' processing in auditory cortex

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Abstract

Studies of cortical connections or neuronal function in different cerebral areas support the hypothesis that parallel cortical processing streams, similar to those identified in visual cortex, may exist in the auditory system. However, this model has not yet been behaviorally tested. We used reversible cooling deactivation to investigate whether the individual regions in cat nonprimary auditory cortex that are responsible for processing the pattern of an acoustic stimulus or localizing a sound in space could be doubly dissociated in the same animal. We found that bilateral deactivation of the posterior auditory field resulted in deficits in a sound-localization task, whereas bilateral deactivation of the anterior auditory field resulted in deficits in a pattern-discrimination task, but not vice versa. These findings support a model of cortical organization that proposes that identifying an acoustic stimulus ('what') and its spatial location ('where') are processed in separate streams in auditory cortex.

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Figure 1: Lateral view of the left hemisphere of the cat cerebrum showing the auditory areas.
Figure 2: Cooling loops in contact with areas AAF and PAF of the left hemisphere at the time of implantation.
Figure 3: Polar plots of sound-localization performance.
Figure 4: Scatter plots showing accuracy and errors on the sound-localization task.
Figure 5: Mean temporal pattern-discrimination performance (mean ± s.e.m.) for each cat (A, B and C) before and following cooling deactivation (pre/post, white), during bilateral cooling of PAF cortex (light gray) and during bilateral cooling of AAF cortex (dark gray).
Figure 6: Mean acoustic stimulus–detection performance (mean ± s.e.m.) for each cat (A, B and C) before and following cooling deactivation (pre/post, white), during bilateral cooling of PAF cortex (light gray) and during bilateral cooling of AAF cortex (dark gray).
Figure 7: Deactivation reconstructions for the AAF cooling loop in the left hemisphere and the PAF cooling loop in the right hemisphere.

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Acknowledgements

We thank A.J. Hall for assistance with training and testing the cats, E.M. Woller and A.J. Hall for assistance with preparing the figures and J.G. Mellott for assistance with the tissue processing. We are grateful to M. Mishkin and M. Goodale for very helpful suggestions on an earlier version of this manuscript. This work was supported by grants from the Canadian Institutes of Health Research, the Natural Science and Engineering Research Council of Canada and The Hearing Foundation of Canada. S.M. was supported by a Predoctoral Training Award from the US National Institute for Deafness and Other Communication Disorders.

Author information

S.G.L. conceived and designed the experiments and carried out all of the surgical procedures. S.G.L. and S.M. conducted the behavioral training and testing. S.G.L. analyzed the data and supervised the histological processing of the tissue. S.G.L. and S.M. drafted and edited the manuscript.

Correspondence to Stephen G Lomber.

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