Hemispheric asymmetries in cerebral cortical ... - Semantic Scholar

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TRENDS in Neurosciences Vol.26 No.8 August 2003

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Hemispheric asymmetries in cerebral cortical networks Jeffrey Hutsler1 and Ralf A.W. Galuske2 1 2

Department of Psychology, Program in Neuroscience, University of Michigan, Ann Arbor, MI 48109-1109, USA Department of Neurophysiology, Max-Planck-Institute for Brain Research, Deutschordenstrasse 46, 60528 Frankfurt a.M., Germany

Since the middle of the 19th century it has been recognized that several higher cognitive functions, including language, are lateralized in cerebral cortex. Neuropsychological studies on patients with brain lesions and rapid developments in brain imaging techniques have provided us with an increasing body of data on the functional aspects of language lateralization, but little is known about the substrate on which these specializations are realized. Much attention has been focused on the gross size and shape of cortical regions involved, but recent findings indicate that the columnar and connectional structure within auditory and language cortex in the left hemisphere are distinct from those in homotopic regions in the right hemisphere. These findings concern parameters that are closely linked to the processing architecture within the respective regions. Thus, the comparison of these microanatomical specializations with their respective functional counterparts provides important insights into the functional role of cerebral cortical organization and its consequences for processing of cortical information in the implementation of complex cognitive functions. The idea that cortical areas are functionally specialized for specific tasks is a fundamental tenet in cerebral cortical research. It is conceivable that such functional specialization is partly based on the optimization of local microstructure for these tasks. This idea is well established in primary sensory and motor regions, but is less accepted for other cortical locations. Some of the strongest evidence for structural specialization within the neocortex comes from research on the anatomical features of regions from the two hemispheres that are homotopic but functionally distinct owing to lateralization. Here, the basic organization of cortical tissue is very similar and, thus, the detection of asymmetries in microstructure and circuitry is likely to be related to functional diversity. Therefore, these findings can teach us a great deal about the intimate relation between structure and function in the cerebral cortex. Locations associated with language functions have been the primary target of these efforts and there is a long history of examining gross morphological asymmetries in these regions [1] (Box 1). However, studies of potential asymmetries in cortical microcircuitry have only begun in the last two decades and are closely linked to Corresponding authors: Jeffrey Hutsler ([email protected]), Ralf A.W. Galuske ([email protected]).

elaboration of our understanding of the microanatomical and physiological organization of the neocortex. Most attempts to clarify these issues have focused upon the columnar organization of cerebral cortex. The columnar unit as an organizing principle of cortical structure A general principle of the anatomical and functional microstructure of cerebral cortex is formed by its modular organization. These modules can be seen to vertically traverse all cortical layers, forming a column-like order. Box 1. A history of area specialization Functional lateralization in the brain is, in essence, a more explicit version of regional specialization of mental processes within the cerebral cortex. Localization to the cerebral cortex itself is associated with several 17th century scientists, including Thomas Willis (1621–1675), who identified the cerebral convolutions as being involved in cognitive tasks, and Robert Boyle (1627–1691), who documented several case studies of specific behavioural anomalies associated with localized brain damage. Perhaps the best-known early theory offunctional specialization is the detailed version of localization put forth by Franz Joseph Gall (1757–1828) and later expanded upon by his contemporaries in the now derided phrenological tradition [54]. Although localization offunction gained wide popularity in Gall’s time, cerebral lateralization had not yet become a serious issue amongst scientists of the day. In Gall’s view, individual mental faculties existed as symmetrical copies in the two hemispheres, and this proved to be a convenient argument against the numerous cases of patients with unilateral lesions that did not seem to show a deficit in the faculties proposed by the phrenologists for those sites. Even though the rejection of Gall’s phrenology in the first half of the 19th century was accompanied by the temporary rejection of cortical localization as a whole, this idea would lie dormant for only a few decades. Jean-Baptiste Bouillard, a French cardiologist, is credited with arguing for a frontal lobe location of language functions and with continuing to document specific behavioural deficits following cortical injury. His efforts effectively bridged the demise of phrenology and Paul Broca’s famous pronouncements to the Socie´te´ d’Anthropoligie in the 1860s of a frontal lobe location specialized for language functions (1861) [55] and that this location was lateralized to the left hemisphere (1863) [56]. In Broca’s view, asymmetry was the important point but the direction of the asymmetry was irrelevant. Leftward asymmetry was a consequence of a slight developmental advantage in the left hemisphere. If, during development, the advantage of the left hemisphere was compromised, right hemisphere language abilities were the natural consequence [57]. About a decade after Broca, Carl Wernicke presented evidence that a posterior temporal lobe location, also lateralized to the left hemisphere, could produce aphasic deficits, and he proposed a model of language functions that incorporated both regions and was used to identify the loci of specific types of aphasia [58].

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Macrocolumn width 600–800 µm

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Fig. 1. Aspects of the microanatomical and columnar organization in the cerebral cortex that are altered in the homotopic areas of functionally lateralized cortical regions. The macrocolumnar values were taken from studies on intrinsic connections in posterior regions of the cerebral cortex [25], whereas the microcolumnar values represent averages over different studies from anterior, in addition to posterior, language regions [2]. Detailed values for the dendritic spread were omitted as they vary greatly between different areas and cell types.

These columns are not uniformly defined but their characterization depends crucially on the approach employed to identify them. There are several anatomical and physiological levels on which columns can be defined, and the size of the resulting columnar units varies among the different definitions and cortical areas studied (Fig. 1). In principle, three levels of definition can be considered: a microanatomical, a macroanatomical and a functional level. At the microanatomical level, columns are usually defined based upon the vertical arrangement of pyramidal neurons, a cell class that is characterized by its distinctive morphology and long-range connections. These anatomical ‘microcolumns’ have a diameter of 20 – 50 mm, depending on the species and cortical area [2]. The functional significance of these columnar systems is still unclear but several attempts have been made to identify these microcolumns as the anatomical correlate of the smallest processing unit in the cerebral cortex; however, further research will be required to unequivocally solve this issue [3]. By contrast, anatomical ‘macrocolumns’ can be defined by zones of axonal terminations that are formed by sets of thalamocortical [4], corticocortical [5] and intrinsic connections [6] (Fig. 2). These zones can also be distinguished by enzyme histochemistry, such as that using cytochrome oxidase [7,8] and NADPH-diaphorase [9]. Macrocolumns have diameters of 200–700 mm and are often linked to the third type of column, which is defined based on its function. Functional cortical columns have similarities in receptive field properties, such as ocular dominance, retinotopy or orientation preference in the visual system [10], binaurality [11], bandwidth [12] and frequency preference [13] in the auditory system, or somatotopy in the somatosensory system. Functional columns of similar preference are often linked by systems of long-range intrinsic and corticocortical connections, which result in spatial congruence between the anatomical and functional macrocolumnar systems [14– 17]. These various levels of structural organization and geometry within the cortex, http://tins.trends.com

although most clearly understood in animal studies of sensory regions, provide a crucial context for understanding asymmetries in the structure of languageassociated cortical regions and, more importantly, form the foundation for functional hypotheses regarding how such asymmetries might reflect altered cortical processing that is specific to language-related tasks. Microstructural interhemispheric asymmetries and their functional impact During the past two decades, several groups have undertaken the task of examining the cortex for asymmetries of neuronal circuitry in language-associated cortical regions. As illustrated in Fig. 1, these approaches can be categorized at three different structural levels: the geometry of the resident neurons, the primary organization of these neurons into microcolumns, and the layout of macrocolumnar systems as seen in studies of intra-area connectivity. Although asymmetries have been documented at all three structural levels, these levels are not independent. For example, asymmetries in individual cell geometry might also be evident when examining the organization into microcolumns, as well as when considering the layout of the macrocolumnar system. In addition, the processing of neural information in cortical areas can be affected by a third factor: the connectional embedding of the respective area into the wider network of higher and lower sensory and association areas. Anterior and posterior language-associated regions might also show differing patterns of asymmetries that are likely to be relevant to their different functional roles in language-associated tasks. The earliest studies exploring these issues were Seldon’s reports of quantitative differences between the two hemispheres in posterior language-associated cortical regions [18– 20]. His research demonstrated that the width of individual cortical columns, and the distance between those columns, is greater in the left hemisphere

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Fig. 2. Photomicrographs of microcolumnar and macrocolumnar structures in the human temporal cortex. (a) Nissl-stained section from area TA1 corresponding to Brodmann Area 22. Note the columnar arrangement of pyramidal cells especially in the upper cortical layers. (b) Bundles of afferent and efferent fibers traversing vertically through the upper cortical layers between the columns of pyramidal neurons in the same cortical area as in (a) [post-mortem tracing with 1,10 ,dioctade,dioctadecyl-3,3,30 30 -tetramethylindocarbocyanine perchlorate (DiI)]. (c) Patches of reciprocally interconnected neurons (arrows) in supragranular cortical layers (post-mortem tracing with DiI).

than in the right – a pattern of results that has recently been replicated [21]. Seldon found that this asymmetry in intercolumnar distance was present in multiple auditory regions but not in primary auditory cortex. In addition, he also examined the basal dendrites of pyramidal cells in the same material and demonstrated that their length compensated for the hemispheric differences in columnar spacing: changes in basilar dendritic lengths allowed individual pyramidal cells to contact a similar number of neighboring cell columns despite the changes in columnar spacing. This compensation was not, however, present in posterior left-hemisphere regions associated with language. Thus, in this location, pyramidal cells contacted fewer columnar units than did those on the right, despite their increased dendritic length [18 – 20]. Recent findings have replicated this result in small pyramidal cells that appear to have longer dendritic trees, increased branching and more dendritic spines in the left hemisphere [22]. The morphology of large layer-III pyramidal cells has also been examined in these posterior cortical regions http://tins.trends.com

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using markers for acetylcholinesterase [23]. The number of labeled cells in each hemisphere was found to be symmetrical; however, cell-size asymmetries were present in secondary and language-associated areas of the temporal auditory processing stream. Further work exploring this cell-size asymmetry using nonspecific staining methods has found that the left hemisphere contains a greater number of large pyramidal cells than the right hemisphere throughout the auditory processing stream, even in primary auditory cortex [24]. Recently, Galuske and colleagues have used lipophilic tract tracers (fluorescent tract tracers that can be applied in postmortem tissue to label dendrites and axons for several millimeters) to study the interconnectivity within Wernicke’s area (area 22). Individual tracer deposits in each hemisphere labeled several clusters of cells and dendritic processes at regular intervals, demonstrating a clearly defined patchy pattern of interconnectivity (Fig. 2c). A comparison of the size of these patches between the hemispheres revealed no asymmetries; however, the interpatch spacing was significantly greater in the left hemisphere than in the right in this study [25]. Within Broca’s area, the first studies examined the structure of the basal dendrites of pyramidal cells using Golgi methods. These early results reported a greater number of higher order dendritic branches in the left hemisphere when compared with the right. Higher order dendrites are those closest to the distal ends of a dendritic branch. It is known that the various classes of higher and lower order dendrites receive varying input patterns and differentially affect the neuronal computation process [26]. These findings could not be replicated in a more recent study of pyramidal cells but Hayes and Lewis did find a consistent difference in the size of layer-III pyramidal cells in area 45, with larger neurons located within layer III on the left than on the right [27]. As with cell-size asymmetries documented in auditory and posterior language-associated locations, this size difference is restricted to only the largest magnopyramidal cells [27– 29]. Many of the studies that have found asymmetries in the microcircuitry of human language cortex have naturally speculated as to the functional significance of such changes to the cortical circuitry and how these changes might specifically alter information processing in these cortical regions. Taken together, these various anatomical findings can be usefully regrouped into their implications for intra-area or inter-area neural processing, or for information processing on a more general scale. Asymmetries in intra-area connectivity Studies examining the spacing between cell columns, the diameter of cell columns and the tangential spread of the constituent neurons of columns have focused on the meaning of these asymmetries for the interactions between adjacent neurons, as well as between adjacent microcolumns. Even though both cell-column spacing and dendritic spread change in the same direction within the left hemisphere, within language-associated regions they do not change proportionally [18– 20]. Therefore, individual pyramidal cells in each hemisphere contact a different

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number of adjacent cell columns. In the left hemisphere, this asymmetry results in a smaller number of interconnected columns than in the right, and it has been suggested that this might indicate a more elaborate and less redundant pattern of local processing architecture in the left hemisphere This, in turn, might give rise to an improved separation of the local processing streams. The globally wider intercolumnar distance might indicate the addition of some constituent to the neuropil without altering the relationship between columns that are directly adjacent to one another. Given that the number of glial cells is apparently symmetrical in the two regions [22], short- and long-range connections could account for these asymmetries. In anterior regions, similar changes to the basilar dendrites have initially been reported [26] but more recent examinations of basilar-dendrite structure do not show a clear asymmetry [27]. In parallel with the interhemispheric differences in the local microcolumnar structures, macrocolumnar structures differ between the hemispheres in posterior language regions. Studies on long-range patchy intraareal connections demonstrate that the spacing of the interconnected clusters of neurons is significantly larger on the left, even though the clusters themselves have the same size in both hemispheres (Fig. 3). These data indicate that the left hemisphere contains a greater number of selectively interconnected macrocolumn systems than the right.

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Fig. 3. Comparison of asymmetries at the levels of microcolumn width, sizes of patches of reciprocally interconnected neurons and the distance between these patches within the same subjects. The value on the y-axis is the percentage of the advance of the left hemisphere over the right in Brodmann’s Area 22. Note the lack of asymmetry concerning the size of the interconnected clusters. Note further that for the other two parameters, in all cases the left hemisphere is largest and that there is no correlation between the size of the advance and the different categories. http://tins.trends.com

These varying patterns of intermediate-range intraarea connections, and the resulting arrangement of functional macrocolumns, give rise to reasonable speculation about interhemispheric differences in the functional processing architecture. Accepting the analogy to the visual cortex, in which these interconnected macrocolumns represent clusters of selectively interconnected neurons tuned to the same functional properties, the presence of a greater number of differently tuned macrocolumnar systems in the left posterior language cortex would allow for more distinctly tuned systems, which could analyze the incoming information on a finer scale than on the right side. As is the case for the microcolumnar and dendritic differences, preliminary data suggest that these asymmetries cannot be found in anterior language regions [30]. Thus, both microcolumnar and macrocolumnar differences give rise to the speculation that the left posterior language cortex contains a more refined processing architecture. This is even more pronounced when findings for the two levels of columns are combined, leading to the conclusion that macrocolumns that have the same size in both hemispheres would consequently contain a lower number of microcolumns on the left side. Asymmetries in inter-regional connectivity Direct evidence for asymmetries in inter-area connectivity is lacking, owing to technical limitations associated with tracing long-range connections in the human brain. Despite this, indirect evidence for asymmetries on this third level might be extracted from the following findings. First, the increased distance between microcolumns could partially be accounted for by interhemispheric differences in afferent and efferent connectivity, presumably by varying the number and/or diameter of incoming and outgoing connections. Second, it has long been recognized that there are consistent shape differences between the two hemispheres, especially in the perisylvian regions [31]. Both short-range and long-range axonal connections between cortical regions play an important role in determining the final gyral configurations [32]. Third, studies that have found greater numbers of magnopyramidal cells in layer III in both anterior and posterior language regions, as well as in primary and secondary auditory locations, of the left hemisphere have suggested that such asymmetries might be indicative of connectional asymmetries between the two hemispheres [23,24,27– 29]. The relationship between cell size and axonal elaboration and length has been established in several studies [33,34] and is best illustrated by the Betz cells of layer V in the motor strip, which have axonal connections directly to the motor neurons in the spinal cord and are the largest pyramidal cells in the cortical mantle. Moreover, it has been suggested that greater numbers of magnopyramidal cells in the left hemisphere might play an important role in specialization for temporal processing (see following discussion). Of course, a greater number of magnopyramidal cells in the left hemisphere could also be an epiphenomenon of the expanded neuropil between cell columns, the associated increases in basilar dendrite length, and higher order dendritic branching patterns.

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However, the relationship between cell size and dendritic architecture is not strict [27]. Finally, electron microscopy studies indicate a greater level of myelination within the left hemisphere [22]. Asymmetries in functional information processing Perhaps the most cited hemispheric difference that might be related to the various microanatomical asymmetries is the better ability of the left hemisphere to process temporal information. The suggestion of a temporal processing asymmetry has been documented in visual, auditory and tactile tasks [35,36]. Language, which typically relies on a serial stream of auditory information, might require such specialized abilities because timing appears to play such an important role in language comprehension. The temporal dependence of language is evident from studies of degraded speech showing that sufficient comprehension can be retained in the presence of only a limited amount of spectral information [37]. Additional evidence is seen in cases of language-learning impairment where children often show auditory perception deficits for brief, but not long, tones in specific sound contexts [38,39]. Other studies have shown that explicit training in tasks designed to improve temporal processing thresholds can improve speech discrimination and language comprehension in this population [40,41]. Direct evidence of a left hemisphere advantage in detecting brief temporal differences comes from implanted electrode studies [42], lesion studies [43], magnetic encephalography [44],

Box 2. Lateralization of communication functions in nonhuman species Lateralization of communication skills is not unique to the humans. On a psychophysical level it has been demonstrated that there is a left-brain advantage for the processing of species-specific vocalizations in nonhuman primates [59,60] and a limited amount of lateralization in chicks and mice [61,62]. Likewise, leftward lateralization of specialized brain structures for the production of song have been identified in the forebrain and brainstem of songbirds [63]; however, electrophysiological and lesion studies examining bilateral contributions to the production of bird song syllables argue against a direct analogy between neural lateralization of birdsong and human speech [64]. In nonhuman primates the neurobiological basis for the perception of vocalizations is formed by the primary and higher auditory areas in the temporal cortex, including area tpt at the temporoparietal junction [65]. These areas contain neurons responding to different classes of species-specific sounds [49] and lesions in this region strongly impair the perception of these sounds [66,67]. Nevertheless, the analysis of the anatomical substrate has still not progressed very far. There is, as in humans, evidence for gross morphological differences between the upper parts of the left and right temporal cortices, with the left planum temporale appearing larger in several non-human primates such as chimpanzees, gorillas, macaques [68,69] and even new-world monkeys [70,71]. However, on a finer scale, the evidence for a side-specific processing architecture is sparse. Only a few reports exist on differences in the neuronal circuitry in these regions [72] and there is no indication for an unequal distribution of neurons encoding species-specific vocalizations between the hemispheres. Thus, neural basis for communication perception in non-human species requires additional studies aimed at analyzing the functional and anatomical architecture in these brain areas. http://tins.trends.com

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positron emission tomography [45] and functional magnetic resonance imaging [46]. Indeed, it has even been suggested that the costs of a temporal delay associated with interhemispheric transfer might be the driving force behind language lateralization in the brain, given the time costs associated with interhemispheric transfer [47]. All these speculations on the physiological demand of language processing are additionally compatible with the findings presented above regarding the organization of macrocolumns and microcolumns. The separation of connectivity in both column types could be an important advantage of the left hemisphere for extracting crucial temporal information from the incoming stream of auditory inputs and, thus, analyzing these inputs under different conditions than the right hemisphere. Seeing less of this type of hemispheric specialization in the anterior language cortex is not unexpected, because many transformations might have already been performed in posterior cortical areas of the language system. Concluding remarks and outlook Until we have a clear view of the cerebral processing steps that are required to extract language-relevant content from acoustic and auditory input, we can only speculate about the functional consequences of structural asymmetries in language cortex. Studies in both primates (Box 2) and humans indicate that the analysis and evaluation of temporal relations in incoming auditory information is a crucial issue [48,49]. The fact that higher order auditory areas are specifically designed for such tasks is evident even in animals such as bats, which use the evaluation of temporal structures in acoustic signals for orientation and prey localization, and which have these features represented in a columnar manner in their auditory areas [50]. Therefore, it is tempting to assign these structural asymmetries to an optimization for similar tasks in the language-dominant hemisphere of humans. Even if this is true, one must still account for the lateralized ability to extract language-relevant content from visual information. Therefore, an understanding of how cortical circuits are functionally modified by changes in their structural geometry, and how these changes might be related to the neuronal processes underlying language perception and production, remain crucial. In addition, it is necessary to examine further how the different aspects of asymmetry in cerebral microcircuits influence each other. Studies of this issue indicate that asymmetries on the macrocolumnar and microcolumnar levels are variable within the same subject even though they occur in the same general direction (Fig. 3). Thus, microcolumnar and macrocolumnar asymmetries might rely on different factors. Even if one takes these doubts into account, one can still accept that the structural asymmetries described in this review reflect the optimization of cortical circuits for language processing. Such findings naturally lead to questions regarding the ontogeny of functional and anatomical asymmetries. An attractive hypothesis in this context is that structural asymmetries guide functional asymmetries. Indeed, functional studies on these issues indicate that language perception is already

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lateralized shortly after birth [51]. However, results from children treated with hemispherectomies suggest that there is still a capacity to reverse this functional pattern. How this dramatic reorganization guides regional structural specializations that, according to the hypothesis formulated above, should have been present at an earlier age is unknown. Nevertheless, these observations might indicate that early lateralization is fixed in the human brain. Based on the data on differences in the asymmetry of microcolumns and macrocolumns one might formulate the following hypothesis: early ontogenetic or genetically determined events might lead to a structural microcolumn asymmetry which, in turn, might guide functional lateralization. This lateralization might then shape macrocolumnar structures to optimize them for the language-relevant information processing. Given that long-range intrinsic connections in the visual system are susceptible to environmental changes such as visual deprivation and altered visual input [52,53], this hypothesis might also explain why an initial lateralization based on an early structural asymmetry might still be reversible given that the respective functional requirements are present during an early critical phase in life. References 1 Shapleske, J. et al. (1999) The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance. Brain Res. Rev. 29, 26– 49 2 Buxhoeveden, D.P. and Casanova, M.F. (2002) The minicolumn and evolution of the brain. Brain Behav. Evol. 60, 125 – 151 3 Jones, E.G. (2000) Microcolumns in the cerebral cortex. Proc. Natl. Acad. Sci. U. S. A. 97, 5019 – 5021 4 Levay, S. et al. (1978) Ocular dominance columns and their development in layer IV of the cat’s visual cortex. J. Comp. Neurol. 179, 223 – 224 5 Innocenti, G.M. (1986) General organization of callosal connections in the cerebral cortex. In Cerebral Cortex, Volume 5: Sensory Motor Areas and Aspects of Cortical Connectivity (Peters, A. and Jones, E.G., eds) pp. 291 – 353, Plenum Press 6 Rockland, K.S. and Lund, J.S. (1983) Intrinsic laminar lattice connections in primate visual cortex. J. Comp. Neurol. 216, 303 – 318 7 Wong-Riley, M. (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase. Brain Res. 171, 11 – 28 8 Rivier, F. and Clarke, S. (1997) Cytochrome oxidase, acetylcholinesterase and NADPH-diaphorase staining in human supratemporal and insular cortex: evidence for multiple auditory areas. Neuroimage 6, 288– 304 9 Barone, P. and Kennedy, H. (2000) Non-uniformity of neocortex: area l heterogeneity of NADPH-diaphorase reactive neurons in adult macaque monkeys. Cereb. Cortex 10, 160 – 174 10 Hubel, D.H. and Wiesel, T.N. (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J. Physiol. (Lond.) 160, 106 – 154 11 Imig, T.J. and Brugge, J.F. (1978) Sources and terminations of callosal axons related to binaural and frequency maps in primary auditory cortex of the cat. J. Comp. Neurol. 182, 637 – 660 12 Schreiner, C.E. and Mendelson, J.R. (1990) Functional topography of cat primary auditory cortex: distribution of integrated excitation. J. Neurophysiol. 64, 1442– 1459 13 Reale, R.A. et al. (1983) Geometry and orientation of neuronal processes in cat primary auditory cortex (A1) related to characteristic-frequency maps. Proc. Natl. Acad. Sci. U. S. A. 80, 5449 – 5453 14 Gilbert, C.D. and Wiesel, T.N. (1989) Local circuits and ocular dominance columns in monkey striate cortex. J. Neurosci. 9, 2432 – 2442 15 Livingstone, M.S. and Hubel, D.H. (1984) Specificity of intrinsic http://tins.trends.com

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