Audition differently activates the visual system in neonatally enucleated mice compared with anophthalmic mutants

Abstract

The occipital cortex, normally visual, can be activated by auditory or somatosensory tasks in the blind. This cross-modal compensation appears after early or late onset of blindness with differences in activation between early and late blind. This could support the hypothesis of a reorganization of sensory pathways in the early blind that does not occur in later onset blindness. Using immunohistochemistry of the c-Fos protein following a white noise stimulus and injections of the anterograde tracer dextran-biotin in the inferior colliculus, we studied how the occurrence of blindness influences cross-modal compensation in the mutant anophthalmic mouse strain and in C57BL/6 mice enucleated at birth. We observed, in mutant mice, immunolabeled nuclei in the visual thalamus - the dorsal lateral geniculate nucleus - in the primary visual area (V1) and a few labeled nuclei in the secondary visual area (V2). In enucleated mice, we observed auditory activity mainly in V2 but also sparsely in V1. No labeled cells could be found in the visual thalamus. Tracing studies confirmed the difference between anophthalmic and birth-enucleated mice: whereas the first group showed inferior colliculus projections entering both the dorsal lateral geniculate and the latero-posterior nuclei, in the second, auditory fibers were found only within the latero-posterior thalamic nucleus. None was found in controls with intact eyes. We suggest that the prenatal period of spontaneous retinal activity shapes the differences of the sensory reorganization in mice.

Cortical GABAergic Interneurons in Cross-Modal Plasticity following Early Blindness

“…Similar anatomical and electrophysiological findings have been reported in early postnatal and adult enucleated mice and rabbits [41–43]. Enucleation at birth or congenital microphthalmia in kittens induces auditory activation of the visual cortex, principally area V1 [44, 45], which has also been shown in hamsters, opossums, and mice [46–49]. …”

Cortical plasticity within and across lifetimes: how can development inform us about phenotypic transformations?

“…Further, cortex in the expected location of V1 received aberrant inputs from somatosensory and auditory structures of the cortex and thalamus (Karlen et al, 2006; Figure 8B). Studies in anophthalmic mice have also demonstrated alterations in subcortical connections and large changes in functional organization of “visual cortex” (Godement et al, 1979; Chabot et al, 2007), and studies of congenitally deaf mice show that auditory cortex is taken over by the visual and somatosensory systems (Hunt et al, 2006). Work in experimentally deafened cats supports these data.…”

How does the Visual Cortex of the Blind Acquire Auditory Responsiveness?

“…This suggests that auditory inputs from the LGN do not drive V1 activation in blind humans, presumably reflecting the absence of IC–LGN connections. Agreeing closely with this conclusion, Chabot et al (2007) did not observe anatomical connections from the IC to LGN in neonatally enucleated mice. Note, however, that these peculiar connections have been observed in mutant congenitally eyeless mice (Chabot et al, 2007, 2008) and neonatally enucleated hamsters (Izraeli et al, 2002).…”