Alterations of visual cortical connections in cats following early removal of retinal input

doi:10.1016/0165-3806(91)90076-U

Developmental Brain Research

Volume 63, Issues 1–2, 19 November 1991, Pages 163-180

https://doi.org/10.1016/0165-3806(91)90076-U Get rights and content

Abstract

The major afferent pathways to the visual cortex were studied in cats enucleated at postnatal days 0, 15, 30 and 60 using the retrograde tracer wheat germ agglutin conjugated horseradish peroxidase (WGA-HRP). Following enucleation at days 0 and 15, the lateral gyrus was shrunken and cortical thickness was decreased, but the thickness of layer I was increased relative to normal adult cats. The laminar portion of the lateral geniculate complex occupied only half its normal volume, but the pathway from the intralaminar nuclei to visual cortex was doubled in volume. The ipsilateral and contralateral claustrum and ipsilateral medial septal nucleus also provided increased input to visual cortex. The changes in these projection patterns were not as dramatic in the cats enucleated at days 30 and 60. The callosal pathway between areas 17 and 18 was also significantly altered in cats enucleated on the day of birth and at day 15. Callosal cells were found in the infragranular layers throughout area 18. The number of supragranular callosal cells in the medial half of area 18 and in area 17 was reduced to approximately one third the normal adult number, but the mediolateral extent of this zone was not reduced. In the infragranular layers, the callosal cell number was approximately twice that in adult cats, and they occupied at least twice their normal mediolateral extent. Following bilateral enucleation at days 30 and 60, the cell numbers and mediolateral extent of the callosal cell zones approximated those in normal adult cats. Taken together, these results indicate that early deafferantiation of a cortical area can alter the thalamic, extrathalamic and callosal connections of that area.

References (103)

K. Albus
Hypothalamic and basal forebrain afferents to the cat's visual cortex: a study with horseradish peroxidase
Neurosci. Lett.
(1981)
N. Berman et al.
Alterations in connections of the corpus callosum following convergent and divergent strabismus
Brain Res.
(1983)
D.M. Berson et al.
Parallel thalamic zones in the LP-pulvinar complex of the cat, identified by their afferent and efferent connections
Brain Res.
(1978)
J.K. Brunso-Bechtold et al.
Effect of bilateral enucleation on the development of layers in the dorsal lateral geniculate nucleus
Neuroscience
(1981)
A.J. Elberger
Plasticity of claustroneocortical connections via the corpus callosum in the cat
Neurosci. Lett.
(1988)
D.O. Frost
Anomalous visual connections to somatosensory and auditory systems following brain lesions in early life
Dev. Brain Res.
(1982)
P. Godement et al.
Thalamic afferents to the visual cortex in congenitally anophthalmic mice
Neurosci. Lett.
(1979)
A.M. Graybiel
Some ascending connections of the pulvinar and nucleus lateralis posterior of the thalamus in the cat
Brain Res.
(1972)
R.W. Guillery
Survival of large cells in the dorsal lateral geniculate laminae after interruption of retino-geniculate afferents
Brain Res.
(1971)
R.W. Guillery et al.
The organization of the geniculocortical pathway that develops without retinal afferents
Dev. Brain Res.
(1985)

E.F.S. Kaufman et al.

Efferent projections of the thalamic intralaminar nuclei in the cat

Brain Res.

(1985)

J. Kiss et al.

Immunohistochemical localization of cells containing nerve growth factor receptors in the different regions of the adult rat forebrain

Neuroscience

(1988)

Y. Komatsu et al.

Electrophysiological and morphological correlates in the development of visual cortical circuitry in infant kittens

Dev. Brain Res.

(1985)

R.D. Lund et al.

Asymmetry in the visual callosal connections of strabismic cats

Brain Res.

(1979)

R.D. Lund et al.

Squint-induced modification callosal connections in cats

Brain Res.

(1978)

G. Macchi et al.

The basolateral amygdaloid projection to the neocortex in the cat

Neurosci. Lett.

(1978)

H.J. Neville et al.

Altered visual evoked potentials in congenitally deaf adults

Brain Res.

(1983)

M. Norita

Claustral neurons projecting to the visual cortical areas in the cat: a retrograde double-labeling study

Neurosci. Lett.

(1983)

J. Olavarria et al.

Widespread callosal connections in infragranular visual cortex of the rat

Brain Res.

(1983)

B.R. Payne et al.

Neocortical connections in fetal cats

Neurosci. Res.

(1988)

G. Rebillard et al.

Enhancement of the visual response on the primary auditory cortex of the cat after early destruction of cochlear receptors

Brain Res.

(1977)

R.W. Rhoades et al.

Altered catecholaminergic innervation of superior colliculus after enucleation in adult and neonatal hamsters

Brain Res.

(1983)

R.W. Rhoades et al.

Distribution of visual callosal projection neurons in hamsters subjected to transection of the optic radiations on the day of birth

Dev. Brain Res.

(1987)

J. Schlag et al.

Induction of oculomotor responses from thalamic internal medullary lamina in the cat

Exp. Neurol.

(1971)

C. Shaw et al.

Ontogenesis of muscarinic acetylcholine binding sites in cat visual cortex: reversal of specific laminar distribution during the critical period

Dev. Brain Res.

(1984)

A.M. Sillito et al.

Cholinergic modulation of the functional organization of the cat visual cortex

Brain Res.

(1983)

L.L. Symonds et al.

Projections of the pulvinar-lateral posterior complex to visual cortical areas in the cat

Neuroscience

(1981)

I. Tork et al.

Histochemical evidence for a catecholaminergic (presumably dopaminergic) projection from the ventral mesencephalic tegmentum to visual cortex in the cat

Neurosci Lett.

(1981)

C. Veraart et al.

Glucose utilization in human visual cortex is abnormally elevated in blindness of early onset but decreased in blindness of late onset

Brain Res.

(1990)

R.L. Anker

The prenatal development of some of the visual pathways in the cat

J. Comp. Neurol.

(1977)

M.R. Bear et al.

An investigation of cholinergic circuitry using acetylcholinesterase histochemistry

J. Comp. Neurol.

(1985)

M.R. Bear et al.

Postnatal changes in the distribution of acetylcholinesterase in kitten striate cortex

J. Comp. Neurol.

(1985)

M.F. Bear et al.

Modulation of visual cortical plasticity by acetylcholine and noradrenaline

Nature

(1986)

Berman, N.E.J. and Grant, S., Topographic organization, number and laminar distribution of callosal cells conecting...

N.E. Berman et al.

Development and plasticity of visual interhemispheric connections

N. Bonaventura et al.

Apparition au niveau du cortex visual de potentiels evoques d'origine auditive chez la souris privee de photorecepteurs

J. Physiol. (Paris)

(1968)

J.K. Brunso-Bechtold et al.

An ultrastructural and morphmetric study of the effect of removal of retinal input on the development of the dorsal lateral geniculate nucleus

J. Comp. Neurol.

(1990)

J.J.M. Chun et al.

Transient cells of the developing mammalian telencephalon are peptide-immunoreactive neurons

Nature

(1987)

B.G. Cragg

The development of synapses in the visual system of the cat

J. Comp. Neurol.

(1975)

M.J. Cullen et al.

Cytological organization of the dorsal lateral geniculate nuclei in mutant anophthalamic and postnatally enucleated mice

J. Neurocytol.

(1976)

E.T. Cunningham et al.

Laminar and synaptic organization of the projection from the thalamic nucleus centralis to primary visual cortex in the cat

J. Comp. Neurol.

(1986)

C.G. Cusick et al.

Modification of visual callosal projections in rats

J. Comp. Neurol.

(1982)

C. Dehay et al.

Maturation and connectivity of the visual cortex in monkey is altered by prenatal removal of retinal input

Nature

(1989)

R.W. Doty

Nongeniculate afferents to striate cortex in macaques

J. Comp. Neurol.

(1983)

H. Elias et al.

M.J. Friedlander et al.

Development of Y-axon innervation of cortical area 18 in the cat

J. Physiol.

(1989)

D.O. Frost et al.

Effects of sensory experience on the development of the visual callosal connections

D.O. Frost et al.

Effects of dark rearing on the development of visual callosal connections

Exp. Brain Res.

(1989)

L.L. Glenn et al.

Discharge rate and excitability of cortically projecting intralaminar thalamic neurons during waking and sleep states

J. Neurosci.

(1982)

S. Grant et al.

Delayed maturation of callosal connections between cortical areas 17 and 18 of Siamese compared to normal cats

Invest. Ophthalmol. Suppl.

(1987)

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Research reportAlterations of visual cortical connections in cats following early removal of retinal input

Abstract

Neurosci. Lett.

Brain Res.

Brain Res.

Neuroscience

Neurosci. Lett.

Dev. Brain Res.

Neurosci. Lett.

Brain Res.

Brain Res.

Dev. Brain Res.

Brain Res.

Neuroscience

Dev. Brain Res.

Brain Res.

Brain Res.

Neurosci. Lett.

Brain Res.

Neurosci. Lett.

Brain Res.

Neurosci. Res.

Brain Res.

Brain Res.

Dev. Brain Res.

Exp. Neurol.

Dev. Brain Res.

Brain Res.

Neuroscience

Neurosci Lett.

Brain Res.

The prenatal development of some of the visual pathways in the cat

J. Comp. Neurol.

An investigation of cholinergic circuitry using acetylcholinesterase histochemistry

J. Comp. Neurol.

Postnatal changes in the distribution of acetylcholinesterase in kitten striate cortex

J. Comp. Neurol.

Modulation of visual cortical plasticity by acetylcholine and noradrenaline

Nature

Development and plasticity of visual interhemispheric connections

Apparition au niveau du cortex visual de potentiels evoques d'origine auditive chez la souris privee de photorecepteurs

J. Physiol. (Paris)

An ultrastructural and morphmetric study of the effect of removal of retinal input on the development of the dorsal lateral geniculate nucleus

J. Comp. Neurol.

Transient cells of the developing mammalian telencephalon are peptide-immunoreactive neurons

Nature

The development of synapses in the visual system of the cat

J. Comp. Neurol.

Cytological organization of the dorsal lateral geniculate nuclei in mutant anophthalamic and postnatally enucleated mice

J. Neurocytol.

Laminar and synaptic organization of the projection from the thalamic nucleus centralis to primary visual cortex in the cat

J. Comp. Neurol.

Modification of visual callosal projections in rats

J. Comp. Neurol.

Maturation and connectivity of the visual cortex in monkey is altered by prenatal removal of retinal input

Nature

Nongeniculate afferents to striate cortex in macaques

J. Comp. Neurol.

Development of Y-axon innervation of cortical area 18 in the cat

J. Physiol.

Effects of sensory experience on the development of the visual callosal connections

Effects of dark rearing on the development of visual callosal connections

Exp. Brain Res.

Discharge rate and excitability of cortically projecting intralaminar thalamic neurons during waking and sleep states

J. Neurosci.

Delayed maturation of callosal connections between cortical areas 17 and 18 of Siamese compared to normal cats

Invest. Ophthalmol. Suppl.

Research report
Alterations of visual cortical connections in cats following early removal of retinal input