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The transformation of association cortex into sensory cortex
Brain Research Bulletin, Vol. 50, Nos. 5/6, p. 425, 1999 Copyright © 1999 Elsevier Science Inc. Printed in the USA. All rights reserved 0361-9230/99/$–see front matter
PII S0361-9230(99)00176-8
The transformation of association cortex into sensory cortex Jon H. Kaas* Department of Psychology, Vanderbilt University, Nashville, TN, USA [Received 10 May 1999; Accepted 15 May 1999] these findings are profound. First, we can conclude that complex brains evolved from simpler brains, not by adding vast amounts of general purpose association cortex, but by expanding the sensory and motor hierarchies to include more areas for sensory processing and motor control. Second, for both simple and complex brains, most of the processing is modality specific, rather than multimodal. Multimodal regions do exist, but they occupy much less of neocortex than we previously supposed. Third, the ways complex brains evolved in different lines of descent is similar in that new areas were added, but unique in the ways the systems were expanded. This allows for tremendous diversity in brain organization and the abilities that brains mediate. Finally, large brains are highly modular. Processing is spatially distributed, and complex tasks are likely decomposed to many subtasks involving, to various extents, different cortical areas. Thus, over the last 30 years or so, we have greatly changed our views of how brains are organized, differ across species, and process information [3].
As a student, I was exposed to the common textbook figures showing that neocortex of mammals consists of a few primary and secondary sensory and motor areas surrounded by association cortex. Small-brained mammals had proportionately less association cortex, while large brained mammals had more. Brain evolution in mammals largely consisted of increasing the amount of this all-purpose association cortex, where sensory modalities mixed to allow complex, higher-order functions. The primary and secondary areas of sensory and motor cortex were identified by recording brain potentials evoked by the sudden onset of sensory stimuli or evoking movements with electrical stimulation of the brain surface. In deeply anesthetized animals, much of the cortex was unresponsive to sensory stimuli, and unresponsive or “silent” zones of cortex were assumed to be association cortex. This picture of cortical organization and evolution started to change in the 1960s when Hubel and Wiesel [2] provided convincing evidence for a third visual area, V3, in cats and Kuypers et al. [5] provided evidence from connection patterns for additional visual areas in monkeys. Soon additional visual, somatosensory, auditory, and motor areas were being identified in laboratory after laboratory. Although investigators still disagree on the precise number of nonprimary sensory and motor areas, as more areas are being discovered and some proposed fields are in question, we have good agreement that visual cortex of monkeys includes over 30 visual areas, somatosensory cortex has at least 10, auditory cortex has 12 or more, and frontal cortex contains approximately 8 to 10 motor areas [1,4]. Cats also have multiple sensory and motor areas in the former territory of association cortex [6], while the small-brained mammals, formerly shown with little association cortex, have few sensory and motor representations, but they occupy most of neocortex [3,4]. There are several major consequences of this change in the way we understand the organization of neocortex. The implications of
REFERENCES 1. Felleman, D. V.; Van Essen, D. C. Distributed hierarchial processing in primate cerebral cortex. Cereb. Cortex 1:1– 47; 1991. 2. Hubel, D. H.; Wiesel, T. N. Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. J. Neurophysiol. 30:1561–1573; 1965. 3. Kaas, J. H. Why does the brain have so many visual areas? J. Cog. Neurosci. 1:121–135; 1989. 4. Kaas, J. H. The evolution of isocortex. Brain Behav. Evol. 46:187–196; 1995. 5. Kuypers, H. G. J. M.; Szwarchart, M. K.; Mishkin, M.; Rosvold, H. E. Occipitotemporal corticocortical connections in the rhesus monkey. Exp. Neurol. 11:245–262; 1965. 6. Scannell, J. W.; Young, M. P.; Blakemore, C. Analysis of connectivity in the cat cerebral cortex. J. Neurosci. 15:1463–1483; 1995.
* Address for correspondence: Prof. Jon H. Kaas, Dept. of Psychology, Vanderbilt University, 301 Wilson Hall, 111 21st Avenue South, Nashville, TN 37240, USA. Fax: 615-343-8449; E-mail: [email protected]
425
PII S0361-9230(99)00176-8
The transformation of association cortex into sensory cortex Jon H. Kaas* Department of Psychology, Vanderbilt University, Nashville, TN, USA [Received 10 May 1999; Accepted 15 May 1999] these findings are profound. First, we can conclude that complex brains evolved from simpler brains, not by adding vast amounts of general purpose association cortex, but by expanding the sensory and motor hierarchies to include more areas for sensory processing and motor control. Second, for both simple and complex brains, most of the processing is modality specific, rather than multimodal. Multimodal regions do exist, but they occupy much less of neocortex than we previously supposed. Third, the ways complex brains evolved in different lines of descent is similar in that new areas were added, but unique in the ways the systems were expanded. This allows for tremendous diversity in brain organization and the abilities that brains mediate. Finally, large brains are highly modular. Processing is spatially distributed, and complex tasks are likely decomposed to many subtasks involving, to various extents, different cortical areas. Thus, over the last 30 years or so, we have greatly changed our views of how brains are organized, differ across species, and process information [3].
As a student, I was exposed to the common textbook figures showing that neocortex of mammals consists of a few primary and secondary sensory and motor areas surrounded by association cortex. Small-brained mammals had proportionately less association cortex, while large brained mammals had more. Brain evolution in mammals largely consisted of increasing the amount of this all-purpose association cortex, where sensory modalities mixed to allow complex, higher-order functions. The primary and secondary areas of sensory and motor cortex were identified by recording brain potentials evoked by the sudden onset of sensory stimuli or evoking movements with electrical stimulation of the brain surface. In deeply anesthetized animals, much of the cortex was unresponsive to sensory stimuli, and unresponsive or “silent” zones of cortex were assumed to be association cortex. This picture of cortical organization and evolution started to change in the 1960s when Hubel and Wiesel [2] provided convincing evidence for a third visual area, V3, in cats and Kuypers et al. [5] provided evidence from connection patterns for additional visual areas in monkeys. Soon additional visual, somatosensory, auditory, and motor areas were being identified in laboratory after laboratory. Although investigators still disagree on the precise number of nonprimary sensory and motor areas, as more areas are being discovered and some proposed fields are in question, we have good agreement that visual cortex of monkeys includes over 30 visual areas, somatosensory cortex has at least 10, auditory cortex has 12 or more, and frontal cortex contains approximately 8 to 10 motor areas [1,4]. Cats also have multiple sensory and motor areas in the former territory of association cortex [6], while the small-brained mammals, formerly shown with little association cortex, have few sensory and motor representations, but they occupy most of neocortex [3,4]. There are several major consequences of this change in the way we understand the organization of neocortex. The implications of
REFERENCES 1. Felleman, D. V.; Van Essen, D. C. Distributed hierarchial processing in primate cerebral cortex. Cereb. Cortex 1:1– 47; 1991. 2. Hubel, D. H.; Wiesel, T. N. Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. J. Neurophysiol. 30:1561–1573; 1965. 3. Kaas, J. H. Why does the brain have so many visual areas? J. Cog. Neurosci. 1:121–135; 1989. 4. Kaas, J. H. The evolution of isocortex. Brain Behav. Evol. 46:187–196; 1995. 5. Kuypers, H. G. J. M.; Szwarchart, M. K.; Mishkin, M.; Rosvold, H. E. Occipitotemporal corticocortical connections in the rhesus monkey. Exp. Neurol. 11:245–262; 1965. 6. Scannell, J. W.; Young, M. P.; Blakemore, C. Analysis of connectivity in the cat cerebral cortex. J. Neurosci. 15:1463–1483; 1995.
* Address for correspondence: Prof. Jon H. Kaas, Dept. of Psychology, Vanderbilt University, 301 Wilson Hall, 111 21st Avenue South, Nashville, TN 37240, USA. Fax: 615-343-8449; E-mail: [email protected]
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