Receptive-field properties of different classes of neurons in visual cortex of normal and dark-reared cats

Leventhal, Audie G.; Hirsch, Helmut V. B.

doi:10.1152/jn.1980.43.4.1111

Cited by 113 publications

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“…before eye opening (Hubel & Wiesel, 1963). Second, maturation of orientation selective neurons is rather independent of visual experience up to the third week of age (Leventhal & Hirsch, 1980;Mower et al, 1981;Frégnac & Imbert, 1984; for a recent review see Henry et al, 1994) and also the sequence regularity characteristic for a columnar arrangement gets expressed in the absence of experience (Wiesel & Hubel, 1974). Third, isoorientation maps can develop in the absence of visual experience and remain unchanged even if thalamocortical input connections get rearranged as a consequence of manipulated visual experience (Mioche & Singer, 1989;Gödecke & Bonhoeffer, 1996;Gödecke et al, 1997).…”

Section: Discussionmentioning

confidence: 99%

The layout of orientation and ocular dominance domains in area 17 of strabismic cats

Löwel¹,

Schmidt²,

Kim³

et al. 1998

Eur J Neurosci

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In the primary visual cortex of strabismic cats, the elimination of correlated activity between the two eyes enhances the segregation of the geniculocortical afferents into alternating ocular dominance domains. In addition, both tangential intracortical fibres and neuronal synchronization are severely reduced between neurons activated by different eyes. Consequently, ocular dominance columns belonging to different eyes are functionally rather independent. We wondered whether this would also affect the organization of orientation preference maps. To this end, we visualized the functional architecture of area 17 of strabismic cats with both optical imaging based on intrinsic signals and double labelling of orientation and ocular dominance columns with [ 14 C]2-deoxyglucose and [ 3 H]proline. As expected, monocular iso-orientation domains had a patchy appearance and differed for the two eyes, leading to a clear segregation of the ocular dominance domains. Comparison of 'angle maps' revealed that orientation domains exhibit a pinwheel organization as in normally reared cats. Interestingly, the map of orientation preferences did not show any breaks at the borders between ocular dominance columns: iso-orientation domains were continuous across these borders. In addition, iso-orientation contours tended to cross the borders of adjacent ocular dominance columns at right angles. These data suggest that the basic relations between the layout of orientation maps and ocular dominance columns are not disturbed by artificial decorrelation of binocular input. Therefore in cat area 17, the orientation map does not seem to be modified by experience-dependent changes of thalamic input connections. This suggests the possibility that usedependent rearrangement of geniculocortical afferents into ocular dominance columns is due to Hebbian modifications whereby postsynaptic responsivity is constrained by the scaffold of the orientation map.

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Section: Discussionmentioning

confidence: 99%

The layout of orientation and ocular dominance domains in area 17 of strabismic cats

Löwel¹,

Schmidt²,

Kim³

et al. 1998

Eur J Neurosci

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“…Blakemore & Van Sluyters (1975) suggested that the distinctive class of 'simple' orientationselective cells found in area 17 in very young kittens might receive projections mainly from geniculate X cells, and that cortical cells dominated by Y cell inputs mature later during normal post-natal development. Little is known about the normal maturation of cortical cells with afferents arising from W cells, but it is possible that these neurones are not orientation selective at birth (Leventhal & Hirsch, 1980). It has been suggested, then, that at least some cortical cells receiving X cell inputs are innately orientation selective, whereas neurones innervated principally by geniculate Y and W cells require visual experience to develop orientation selectivity (Blakemore & Van Sluyters, 1975;Leventhal & Hirsch, 1980).…”

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confidence: 99%

“…Little is known about the normal maturation of cortical cells with afferents arising from W cells, but it is possible that these neurones are not orientation selective at birth (Leventhal & Hirsch, 1980). It has been suggested, then, that at least some cortical cells receiving X cell inputs are innately orientation selective, whereas neurones innervated principally by geniculate Y and W cells require visual experience to develop orientation selectivity (Blakemore & Van Sluyters, 1975;Leventhal & Hirsch, 1980). Both areas 17 and 18 already have topographically organized input from appropriate cell types in the l.g.n.…”

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confidence: 99%

The organization and post‐natal development of area 18 of the cat's visual cortex.

Blakemore¹,

Price²

1987

The Journal of Physiology

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SUMMARY1. We made extracellular recordings from 1176 single units in area 18 of adult cats and kittens aged between 7 days and 10 weeks, and from 137 single units in area 17 in kittens aged between 12 days and 10 weeks.2. All cells examined in area 18 of adult cats were visually responsive, 84 % being orientation selective, 9 % orientation biased and 700 non-oriented. Orientation columns and ocular dominance columns were identified. There was an over-all bias towards horizontal and vertical in the distribution of preferred orientations in the rostal part of area 18, where we were recording.3. In area 18 of 7-day-old, visually inexperienced kittens the majority of cells (60 %) were visually unresponsive; the remainder were either non-oriented (250) or orientation biased (15 %), and no orientation-selective units were found. Nevertheless there seemed to be a rudimentary columnar system, even in the youngest animals, in that orientation-biased cells tended to occur in clusters with neighbouring neurones having similar orientation preferences. In normal animals of 3 weeks and younger we found that the distribution of preferred orientations of a sample of neurones in area 18 with receptive fields scattered over much of the left lower quadrant of the visual hemifield was biased to oblique orientations. 4. As in adult cats, most cells in area 18 in young kittens were binocularly driven, and periodic alternation of dominance along oblique penetrations, characteristic of ocular dominance columns, was sometimes seen, even at the earliest ages.5. Many of the developmental changes that we observed in area 18 occurred during the first 4 post-natal weeks. Orientation selectivity, orientation tuning, directionality and responsiveness of neurones matured rapidly over this period. The proportions of simple and complex cells were similar in kittens aged 4 weeks or more to those in adult cats, whereas prior to this most neurones that displayed an orientation preference appeared to be immature simple cells.6. A laminar analysis revealed that very few units in the superficial layers (I, II and III) in area 18 are visually responsive in kittens during their first and second weeks, but orientation selectivity rapidly develops during the third week. By contrast, even in very young, visually inexperienced kittens, the majority of neurones found in deeper laminae (IV, V and VI) are visually responsive and a few of them * To whom correspondence should be addressed.C. BLAKEMORE AND D. J. PRICE already show an orientation preference; however, the subsequent appearance of larger proportions of orientation-selective cells in these lower layers is a more prolonged process than in upper laminae.7. Comparison of the development of areas 17 and 18 suggests that, although the processes of maturation are generally similar in the two regions, there are some differences, which may be related to differences in the types of afferent input.

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“…However, if the animal is reared in total darkness from birth to the age of 6 weeks (DR), then none or few orientation-selective cells are recorded (from 0 to 15%, depending on the authors and the classification criteria); however, the distribution of ocular dominance seems unaffected (Blakemore and Mitchell, 1973;Imbert and Buisseret, 1975;Blakemore and Van Sluyters, 1975;Buisseret and Imbert, 1976;Leventhal and Hirsch, 1980;Fregnac and Imbert, 1978). In animals whose eyelids have been sutured at birth and which are thus binocularly deprived of pattern vision (BD), a somewhat higher proportion (from 12 to 50%) of the visually excitable cells are still orientation selective at 6 weeks (and even beyond 24 months of age) and the proportion of binocular cells is less than normal Blakemore and Van Sluyters, 1975;Kratz and Spear, 1976;Leventhal and Hirsch, 1977;Watkins et al, 1978).…”

Section: Development Under Different Rearing Conditions: Comparisomentioning

confidence: 99%

Theory for the Development of Neuron Selectivity : Orientation Specificity and Binocular Interaction in Visual Cortex

1995

How We Learn; How We Remember: Toward an Understanding of Brain and Neural Systems

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The development of stimulus selectivity in the primary sensory cortex of higher vertebrates is considered in a general mathematical framework. A synaptic evolution scheme of a new kind is proposed in which incoming patterns rather than converging afferents compete. The change in the efficacy of a given synapse depends not only on instantaneous pre-and postsynaptic activities but also on a slowly varying time-averaged value of the postsynaptic activity. Assuming an appropriate nonlinear form for this dependence, development of selectivity is obtained under quite general conditions on the sensory environment. One does not require nonlinearity of the neuron's integrative power nor does one need to assume any particular form for intracortical circuitry. This is first illustrated in simple cases, e.g., when the environment consists of only two different stimuli presented alternately in a random manner. The following formal statement then holds: the state of the system converges with probability 1 to points of maximum selectivity in the state space. We next consider the problem of early development of orientation selectivity and binocular interaction in primary visual cortex. Giving the environment an appropriate form, we obtain orientation tuning curves and ocular dominance comparable to what is observed in normally reared adult cats or monkeys. Simulations with binocular input and various types of normal or altered environments show good agreement with the relevant experimental data. Experiments are suggested that could test our theory further.It has been known for some time that sensory neurons at practically all levels display various forms of stimulus selectivity. They may respond preferentially to a tone of a given frequency, a light spot of a given color, a light bar of a certain length, retinal disparity, orientation, etc. We might, therefore, regard stimulus selectivity as a general property of sensory neurons and conjecture that the development of such selectivity obeys some general rule. Most attractive is the idea that some of the mechanisms by which selectivity develops in embryonic or early postnatal life are sufficiently general to allow a unifying theoretical treatment.

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Receptive-field properties of different classes of neurons in visual cortex of normal and dark-reared cats

Cited by 113 publications

References 0 publications

The layout of orientation and ocular dominance domains in area 17 of strabismic cats

The layout of orientation and ocular dominance domains in area 17 of strabismic cats

The organization and post‐natal development of area 18 of the cat's visual cortex.

Theory for the Development of Neuron Selectivity : Orientation Specificity and Binocular Interaction in Visual Cortex

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