The role of pattern vision in the development ofcortico‐cortical connections

Abstract

The development of cortico-cortical connections was studied in kittens deprived of vision by binocular eyelid suture during the formation of axonal arbors and synaptogenesis, i.e. between the second postnatal week and the end of the third postnatal month. Axons originating in area 17 and terminating either in ipsilateral or contralateral visual areas were visualized with biocytin. In ipsilateral areas 17 and 18, distinct clusters of branches begin to form, distally from the injection, during the second half of the first postnatal month, independently of pattern vision. More proximal clusters differentiate during the second postnatal month, and this seems to involve elimination of exuberant axonal branches. In kittens deprived of vision for 3 or more months, beginning before natural eye opening, the distal clusters regress and the proximal ones fail to differentiate. In extrastriate areas, distinct clusters of branches have segregated by the end of the second postnatal month, independently of visual experience; however, in kittens deprived of vision for 2 or more months, one of the clusters was selectively eliminated. In contralateral areas 17 and 18, we found stunted terminal arbors in kittens continuously deprived of vision. This was already noticeable at the end of the first postnatal month. Apparently, in the absence of pattern vision, most axons undergo only limited growth and do not form their characteristic terminal columns. Many of these axons are subsequently eliminated. In contrast, 8 days of vision beginning at natural eye opening and followed by visual deprivation caused a nearly normal development of intrahemispheric and interhemispheric connections. In conclusion, pattern vision appears to validate connections at early stages of their development; this validation is necessary for their further growth and differentiation that can then continue autonomously.

Schizophrenia, neurodevelopment and corpus callosum

“…[64][65][66][67] The decreased size of pyramidal neurons in layer 3 of the prefrontal cortex 68,69 provides some support to the hypothesis that cortico-cortical connections are defective in schizophrenics since these neurons are an important source, as well as target, of corticocortical connections. However, the hypothesis can be more directly tested by studies of callosal connections.…”

“…33,39 Obviously, a deficit of callosal connections cannot by itself explain the pathophysiology of S. Rather, abnormalities in callosal connections are likely to be an indicator of a more diffuse impairment of corticocortical networks since the developmental rules that apply to callosal connections seem to apply to other cortico-cortical connections as well. 67,71 Indeed, intraareal excitatory connections in the prefrontal cortex might also be altered in S. 72 One decisive advantage of studying callosal connections as a way of testing the hypothesis of defective cortical connections in S is the existence of a large relevant literature covering morphological, electrophysiological and neuropsychological issues in normal individuals, callosally split patients and schizophrenics. Much of the latter literature was reviewed previously.…”

“…16,33 These developmental processes are partially under the control of epigenetic factors. Indeed, they can be altered by sensory deprivation, fetal alcohol, thyroid-hormone deficiency, epilepsy, cytoarchitectonic abnormalities, early lesions and perinatal ischemia (for data and references, see Innocenti,16,34,64 Parnas et al, 20 McCasland et al, 66 Zufferey et al 67 and Kennedy et al 71 ). This list is not exhaustive and some of the same factors have also been implicated in S. Some of the factors affecting the development of callosal connections appear to operate through 'instructions' reaching the cerebral cortex from the thalamus.…”

“…In these areas, not all the cortico-cortical axons appear to be equally sensitive to visual deprivation. 67 In particular, axons from the deep layers are less sensitive than those originating in the upper layers. 64 This highlights another facet of the misconnectivity hypothesis.…”

Interhemispheric connections between primary visual areas: beyond the midline rule

“…34,35). d) As is the case for long-range horizontal connections, callosal connections are selected during development according to experience-dependent rules (6,15,36). Accordingly, their architecture is presumed to reflect frequently occurring constellations of features (37,38).…”