Organization of somatosensory cortex in three species of marsupials,Dasyurus hallucatus, Dactylopsila trivirgata,and Monodelphis domestica: Neural correlates of morphological specializations

Huffman, Kelly J.; Nelson, Jacob L.; Clarey, Janine C.; Krubitzer, Leah

doi:10.1002/(sici)1096-9861(19990105)403:1<5::aid-cne2>3.0.co;2-f

Cited by 82 publications

(79 citation statements)

References 77 publications

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“…Similar results have been obtained from the South American opossum (Monodelphis domestica), with the exception that clear evidence was not obtained for a PV that is distinct from S2 (Huffman et al, 1999;Catania et al, 2000b), while evidence for PV and S2 was obtained from the brush-tailed possum and the striped possum (Huffman et al, 1999). It appears from these and related results from other marsupials (Beck et al, 1996) that opossums and possums have five somatosensory areas in cortex.…”

Section: Early Mammalsmentioning

confidence: 97%

Evolution of somatosensory and motor cortex in primates

2004

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Inferences about how the complex somatosensory systems of anthropoid primates evolved are based on comparative studies of such systems in extant mammals. Experimental studies of members of the major clades of extant mammals suggest that somatosensory cortex of early mammals consisted of only a few areas, including a primary area, S1, bordered by strip-like rostral and caudal somatosensory fields, SR and SC. In addition, the second somatosensory area, S2, and the parietal ventral area, PV, were probably present. S1, S2, and PV were activated independently via parallel projections from the ventroposterior nucleus, VP. Little posterior parietal cortex existed, and it was unlikely that a separate primary motor area, M1, existed until placental mammals evolved. Early primates retained this basic organization and also had a larger posterior parietal region that mediated sensorimotor functions via connections with motor and premotor areas. The frontal cortex included M1, dorsal and ventral premotor areas, supplementary motor area, and cingulate motor fields. Ventroposterior superior and ventroposterior inferior nuclei were distinct from the ventroposterior nucleus in the thalamus. In early anthropoid primates, areas S1, SR, and SC had differentiated into the fields now recognized as areas 3b, 3a, and 1. Areas 3b and 1 contained parallel mirror-image representations of cutaneous receptors and a parallel representation in area 2 was probable. Serial processing became dominant, so that neurons in areas 1, S2, and PV became dependent on area 3b for activation. Posterior parietal cortex expanded into more areas that related to frontal cortex. Less is known about changes that might have occurred with the emergence of apes and humans, but their brains were larger and posed scaling problems most likely solved by increasing the number of cortical areas and reducing the proportion of long connections. © 2004 Wiley-Liss, Inc. Key words: galago; premotor; sensorimotor; tarsier; thalamus; ventroposterior nucleusHumans have exceptional sensorimotor skills that appear to be unique in the extent to which they can be individualized and specialized by experience and training. We commonly observe remarkable skills as we view highly trained athletes and musicians, and there are many examples from other activities as well. Such performances stand in contrast to the simple and sometimes clumsy sensorimotor behavior of opossums and laboratory rats. However, vast differences in abilities are to be expected if we consider the differences in the sensorimotor systems of various mammals.The first premise of this review is that early mammals had small brains in proportion to body size, and these brains contained rather simple sensorimotor systems. Furthermore, these simple sensorimotor systems have been retained with little modification in a range of distantly related extant mammals. By using the methods of modern neuroscience to study the sensorimotor systems of these mammals, together with a cladistic character anal-*Correspondence to:

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Section: Early Mammalsmentioning

confidence: 97%

Evolution of somatosensory and motor cortex in primates

2004

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“…Whatever the balance, the clearest evidence for species-specific brain and cognitive specializations comes from studies of the cortical architecture of evolutionarily related species that have different morphological and behavioral specializations (e.g., Barton, 1996;Barton & Dean, 1993;Barton, Purvis, & Harvey, 1995;Catania, 2000;Catania, Lyon, Mock, & Kaas, 1999;Dukas, 1998;Dunbar, 1993;Hof, Glezer, Nimchinsky, & Erwin, 2000;Huffman, Nelson, Clarey, & Krubitzer, 1999;Moss & Shettleworth, 1996;Moss & Simmons, 1996). The comparison of species with a recent common ancestor is important because existing differences cannot be attributed to their distant evolutionary history.…”

Section: Comparative Ecology and Brain Evolutionmentioning

confidence: 99%

Brain and cognitive evolution: Forms of modularity and functions of mind.

Geary¹,

Huffman²

2002

Psychological Bulletin

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208

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Genetic and neurobiological research is reviewed as related to controversy over the extent to which neocortical organization and associated cognitive functions are genetically constrained or emerge through patterns of developmental experience. An evolutionary framework that accommodates genetic constraint and experiential modification of brain organization and cognitive function is then proposed. The authors argue that 4 forms of modularity and 3 forms of neural and cognitive plasticity define the relation between genetic constraint and the influence of developmental experience. For humans, the result is the ontogenetic emergence of functional modules in the domains of folk psychology, folk biology, and folk physics. The authors present a taxonomy of these modules and review associated research relating to brain and cognitive plasticity in these domains.For several millennia, scholars have debated whether human traits largely result from our biological nature or are a reflection of nurture, specifically our developmental experiences. The debate continues to this day and has recently pervaded the cognitive neurosciences, at least with respect to theoretical models of brain and cognitive evolution (Elman et al

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“…§ The Monodelphis is born at an extremely immature stage of development compared with most other mammals, so that manipulations can be done ex utero. Equally important, the neocortex of these mammals is relatively small, the number of fields is limited, and the organization and connections of much of the sensory cortex have already been described for normal animals (31,32). Thus, the effects of the manipulations on all or most of the neocortex can be assessed in a single experiment.…”

mentioning

confidence: 99%

“…1), and the type of sensory stimuli that elicited a response, as well as the receptive field for neurons at all somatosensory sites, was documented. By examining response patterns and matching electrophysiological recordings to histologically processed tissue, sensory domain maps could be established, and cortical areas within these domains could be identified and compared with normal animals (31,32).…”

mentioning

confidence: 99%

Massive cross-modal cortical plasticity and the emergence of a new cortical area in developmentally blind mammals

Kahn

Krubitzer²

2002

Proc. Natl. Acad. Sci. U.S.A.

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129

105

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In the current investigation, the neurophysiological organization of the neocortex was examined in adult animals that were bilaterally enucleated very early in life, before the retino-geniculocortical pathway was established. Our results indicate that some aspects of development of cortical fields are not mediated by specific sensory inputs. However, the current study also demonstrates that peripheral innervation plays a large role in the organization of the neocortex, as cortical territories normally involved in visual processing are completely captured by the auditory and somatosensory system. Thus, a large degree of phenotypic variability in cortical organization can be accomplished solely by removing or modifying sensory inputs.bilateral enucleations ͉ electrophysiological recording ͉ development ͉ evolution U ntil recently, the notion that humans with a congenital loss of one sensory system become better at making discriminations with the remaining sensory systems was mostly anecdotal. However, studies in congenitally blind individuals indicate that there is a shorter detection time for auditory discrimination tasks (1) and that blind individuals process language faster than sighted individuals (2). Thus, there is a compensatory adaptation of the auditory system in the congenitally blind, presumably because of a reorganization of the neocortex. This hypothesis is supported by recent neuroimaging studies of blind individuals demonstrating that both auditory localization tasks (3) and Braille reading (4-6) activate regions of cortex normally involved in visual processing. Similar types of cross-modal plasticity also have been demonstrated in congenitally deaf individuals (7-9). These results indicate that the amount of cortex devoted to a particular sensory system, and possibly the number and organization of cortical areas, is determined in large part by peripheral innervation and activity patterns generated with use. Indeed, a number of studies in the adult mammalian neocortex have demonstrated that cortical maps of sensory receptor arrays (areas) can be contracted or expanded by loss of peripheral inputs, or by enhanced use (10-24), and that cross-modal plasticity is possible when the modifications in peripheral activity patterns occur early in life (25). Yet, the extent to which peripheral innervation at early developmental stages can sculpt the architecture and function of entire sensory systems is not known.The present investigation was prompted by two seemingly disparate observations related to this issue. First, developmental studies demonstrate that thalamocortical input is not required for the expression of molecules believed to be involved in some aspects of cortical field development (26,27). This suggests that cortical arealization, or the emergence of cortical fields in development, is mediated by intrinsic genetic mechanisms that can operate independent of activity from peripheral receptors. This notion is difficult to reconcile with observations from comparative studies which demonstrate that t...

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Organization of somatosensory cortex in three species of marsupials,Dasyurus hallucatus, Dactylopsila trivirgata,and Monodelphis domestica: Neural correlates of morphological specializations

Cited by 82 publications

References 77 publications

Evolution of somatosensory and motor cortex in primates

Evolution of somatosensory and motor cortex in primates

Brain and cognitive evolution: Forms of modularity and functions of mind.

Massive cross-modal cortical plasticity and the emergence of a new cortical area in developmentally blind mammals

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