The Effect of Onset Age of Visual Deprivation on Visual Cortex Surface Area Across-Species

Abstract

Blindness early in life induces permanent alterations in brain anatomy, including reduced surface area of primary visual cortex (V1). Bilateral enucleation early in development causes greater reductions in primary visual cortex surface area than at later times. However, the time at which cortical surface area expansion is no longer sensitive to enucleation is not clearly established, despite being an important milestone for cortical development. Using histological and MRI techniques, we investigated how reductions in the surface area of V1 depends on the timing of blindness onset in rats, ferrets and humans. To compare data across species, we translated ages of all species to a common neuro-developmental event-time (ET) scale. Consistently, blindness during early cortical expansion induced large (~40%) reductions in V1 surface area, in rats and ferrets, while blindness occurring later had diminishing effects. Longitudinal measurements on ferrets confirmed that early enucleation disrupted cortical expansion, rather than inducing enhanced pruning. We modeled the ET associated with the conclusion of the effect of blindness on surface area at maturity (ETc), relative to the normal conclusion of visual cortex surface area expansion, (ETdev). A final analysis combining our data with extant published data confirmed that ETc occurred well before ETdev.

Structural brain plasticity induced by early blindness

“…Similar findings were observed using histological analyses for V1, V2M and sc. These results are consistent with previous histological studies in anophthalmic and enucleated mice (Masse et al., 2014), anophthalmic rats (Bravo & Inzunza, 1994), enucleated rats (Andelin et al., 2018; Laing et al., 2012) as well as histological (Bock et al., 2012) and MRI (Andelin et al., 2018) studies in enucleated ferrets showing a smaller V1 (volume or area) in blind compared with sighted animals. Studies in early blind humans have also shown smaller visual structures.…”

“…Studies in early blind humans have also shown smaller visual structures. For example, V1 area was smaller in anophthalmic compared with normally sighted individuals (Andelin et al., 2018). Moreover, congenitally blind humans showed smaller volumes compared with sighted controls for the optic tracts, DLG, optic chiasm, V1 and V2 (Noppeney et al., 2005; Pan et al., 2007; Park et al., 2009; Ptito et al., 2008).…”

“…Andelin et al. (2018) showed that the effect of blindness on the structure of visual areas in rodents and humans ends before cortical expansion is complete, highlighting the critical period of cortical development.…”

“…As visual experience is the principal driver of neuronal maturation in visual areas, the absence of visual input leads to a lack of maturation and reduced expansion (Kolb & Whishaw, 1998). Moreover, the earlier the blindness occurs, the smaller the visual areas (Andelin et al., 2018; Laing et al., 2012; Lazzouni & Lepore, 2014; Park et al., 2009). Thus, it could be presumed that the present results are the most extreme case of structural plasticity induced by blindness.…”

Closing the gap from transcription to the structural connectome enhances the study of connections in the human brain

“…The second hypothesis seems intuitive as the protracted development of pathway maturation can expand territory into the postnatal ages, which can subsequently be shaped by environmental input. 140 These different hypotheses were proposed several years ago but the limitations of methods available to study the evolution of connections precluded their investigation in much detail.…”