The effects of bilateral enucleation in the primate fetus on the parcellation of visual cortex

Dehay, Colette; Horsburgh, Gwynn M.; Berland, Michel; Killackey, Herbert P.; Kennedy, Henry

doi:10.1016/0165-3806(91)90199-s

Cited by 61 publications

(36 citation statements)

References 18 publications

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“…The contribution of peripheral innervation to some aspects of cortical organization has been demonstrated previously in macaque monkeys (37)(38)(39)(40) and mice and rats (41)(42)(43)(44) that underwent bilateral enucleations relatively early in development, but at a later stage than in the current study. These previous studies also report that area 17 could be recognized by its architectonic appearance, but that it was smaller than in normal animals (37,38) and that callosal connectivity was relatively normal (38,41,43,44).…”

Section: Discussionmentioning

confidence: 47%

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.

127

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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Section: Discussionmentioning

confidence: 47%

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.

127

105

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“…It appears, therefore, that somatosensory cortex may be enlarged at the expense of other cortical areas. Atrophy of the visual cortex has indeed been demonstrated after early binocular enucleation in monkeys (15)(16)(17) and after dark-rearing in mice (18). In the latter case, a concomitant hypertrophy of auditory cortex has also been reported.…”

Section: Discussionmentioning

confidence: 70%

Crossmodal changes in the somatosensory vibrissa/barrel system of visually deprived animals.

Rauschecker

Tian

Körte

et al. 1992

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

128

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Cats deprived of vision from birth adapt remarkably well to their situation and show little behavioral impairment. They seem to compensate for their lack of vision by relying more on their auditory and tactile senses. We report here that the facial vibrissae, which are most important for tactile orientation in many animals, show supernormal growth in both cats and mice that have been deprived of vision from birth. Furthermore, the whisker representation in the somatosensory cortical barrel field shows a concomitant enlargement in binocularly enucleated mice: individual barrels are expanded in size by up to one-third. The increased use of the vibrissae in visually deprived animals may stimulate both their own growth and, via activation of the respective neural pathways, the expansion of their central representation.Kittens are born with their eyes closed. When normal eye opening is prevented surgically by means of lid suture, the lids grow together permanently, which precludes all pattern vision (1). Despite their lack of vision, these cats learn to move around with little impairment and show such a high degree of behavioral normality that uninformed observers would hardly guess they could not see (1, 2). Similar compensatory plasticity has been described in young monkeys with early vision impairment (3).There is evidence that visually deprived cats have improved auditory capacities (4,5) and that they make very efficient use oftheir vibrissae (6-8). From casual observation it also appeared to us that the vibrissae were on average longer in lid-sutured cats than in normal cats. We therefore decided to determine whisker lengths and diameters quantitatively in both groups of animals.To reduce the variance of data between animals within each group, it would be advantageous to study animals from the same litter. The small litter size in cats, however, makes this practically impossible. We decided, therefore, to study the effects of visual deprivation also on the vibrissae system in the mouse, which not only has larger litters and less genetic variability but in addition has a distinct anatomical representation of its whiskers in the central somatosensory system, the barrel field (9). We hoped that this might allow us to test for a central change in the vibrissa/barrel system possibly related to somatosensory compensation. MATERIALS AND METHODSVibrissae Measurements in Cats. Whisker lengths were measured in 13 cats that had been deprived of vision by means of binocular lid suture until at least 6 months of age, and in 19 normal control animals of comparable age and weight. In addition, whisker diameter at the base was measured in 12 cats, 6 chosen randomly from each of these groups. Lid sutures had been performed by a standard procedure (1) at the Max-Planck-Institut in Tubingen, Germany, around the time of eye opening, under ketamine/ xylazine anesthesia (25 mg/kg).Whisker lengths were determined in situ, while the cats were anesthetized with ketamine and xylazine. Each vibrissa was stretched with a forceps a...

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“…For instance, animals enucleated bilaterally early in development have a reduced LGN and inferior pulvinar in the thalamus, and a reduced striate cortex, V1 [DeHay et al, 1991[DeHay et al, , 1996. In mice selectively bred for supernumerary whiskers, the primary somatosensory area, S1, becomes larger than in normal mice [Welker and Van der Loos, 1986].…”

Section: Discussionmentioning

confidence: 99%

Arealization of the Neocortex in Mammals: Genetic and Epigenetic Contributions to the Phenotype

Krubitzer

Huffman²

2000

Brain Behav Evol

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The neocortex is composed of areas that are functionally, anatomically and histochemically distinct. In comparison to most other mammals, humans have an expanded neocortex, with a pronounced increase in the number of cortical areas. This expansion underlies many complex behaviors associated with human capabilities including perception, cognition, language and volitional motor responses. In the following review we consider data from comparative studies as well as from developmental studies to gain insight into the mechanisms involved in arealization, and discuss how these mechanisms may have been modified in different lineages over time to produce the remarkable degree of organizational variability observed in the neocortex of mammals. Because any phenotype is a result of the complex interactions between genotypic influences and environmental factors, we also consider environmental, or epigenetic, contributions to the organization of the neocortex.

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The effects of bilateral enucleation in the primate fetus on the parcellation of visual cortex

Cited by 61 publications

References 18 publications

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

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

Crossmodal changes in the somatosensory vibrissa/barrel system of visually deprived animals.

Arealization of the Neocortex in Mammals: Genetic and Epigenetic Contributions to the Phenotype

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