Rapid and Reversible Recruitment of Early Visual Cortex for Touch

Abstract

BackgroundThe loss of vision has been associated with enhanced performance in non-visual tasks such as tactile discrimination and sound localization. Current evidence suggests that these functional gains are linked to the recruitment of the occipital visual cortex for non-visual processing, but the neurophysiological mechanisms underlying these crossmodal changes remain uncertain. One possible explanation is that visual deprivation is associated with an unmasking of non-visual input into visual cortex.Methodology/Principal FindingsWe investigated the effect of sudden, complete and prolonged visual deprivation (five days) in normally sighted adult individuals while they were immersed in an intensive tactile training program. Following the five-day period, blindfolded subjects performed better on a Braille character discrimination task. In the blindfold group, serial fMRI scans revealed an increase in BOLD signal within the occipital cortex in response to tactile stimulation after five days of complete visual deprivation. This increase in signal was no longer present 24 hours after blindfold removal. Finally, reversible disruption of occipital cortex function on the fifth day (by repetitive transcranial magnetic stimulation; rTMS) impaired Braille character recognition ability in the blindfold group but not in non-blindfolded controls. This disruptive effect was no longer evident once the blindfold had been removed for 24 hours.Conclusions/SignificanceOverall, our findings suggest that sudden and complete visual deprivation in normally sighted individuals can lead to profound, but rapidly reversible, neuroplastic changes by which the occipital cortex becomes engaged in processing of non-visual information. The speed and dynamic nature of the observed changes suggests that normally inhibited or masked functions in the sighted are revealed by visual loss. The unmasking of pre-existing connections and shifts in connectivity represent rapid, early plastic changes, which presumably can lead, if sustained and reinforced, to slower developing, but more permanent structural changes, such as the establishment of new neural connections in the blind.

Neuroimaging Data From a Single Participant Before and After a Meditation Retreat: a Proof of Concept Study

“…Primary visual areas in the occipital lobes were subject to less routine stimulation. Previous studies show rapid and profound occipital neuroplastic changes under visual deprivation (Merabet et al 2008). We believe that the same mechanism may underlie our findings.…”

Cross-modal associations between vision, touch, and audition influence visual search through top-down attention, not bottom-up capture

“…Consistent with this suggestion, studies have demonstrated that the visual cortex of blind individuals is activated during tasks such as Braille reading (Cohen et al, 1997;Sadato et al, 1996) and haptic object recognition (Amedi, Raz, Azulay, Malach, & Zohary, 2010). Moreover, the existence of networks between vision and touch in normally sighted individuals is supported by neuroimaging studies; visual areas have been shown to be activated during tactile orientation discrimination (Sathian & Zangaladze, 2002;Sathian, Zangaladze, Epstein, & Grafton, 1999), haptic object recognition (Amedi, Jacobson, Hendler, Malach, & Zohary, 2002;Amedi et al, 2010;Deibert, Kraut, Kremen, & Hart, 1999;James, Humphrey, Gati, Servos, Menon, & Goodale, 2002;Pietrini et al, 2004), and Braille reading in sighted subjects following 5 days of complete visual deprivation (Merabet et al, 2008). Furthermore, there is behavioral evidence for the influence of tactile inputs on visual perception.…”

Tactile Spatial Acuity Enhancement in Blindness: Evidence for Experience-Dependent Mechanisms

“…Thus, a plausible prediction of the tactile experience hypothesis is that the most pronounced acuity enhancement will occur on skin areas receiving the greatest daily stimulation. In contrast, prolonged blindfolding of sighted participants reportedly enhances finger tactile acuity (Kauffman et al, 2002;Facchini and Aglioti, 2003;Merabet et al, 2008) and acuity of other skin areas (Zubek et al, 1964), even without training. Thus, a plausible prediction of the visual deprivation hypothesis is that blind participants will show enhanced acuity throughout the body surface.…”

“…This happens in blindfolded sighted participants (Merabet et al, 2007(Merabet et al, , 2008 and blind participants (Sadato et al, 1996(Sadato et al, , 1998(Sadato et al, , 2002(Sadato et al, , 2004Cohen et al, 1999;Burton et al, 2002Burton et al, , 2006Ptito et al, 2005;Stilla et al, 2008). Several lines of evidence suggest a functional role for cross-modal plasticity: a congenitally blind Braille reader developed alexia for Braille after suffering a bilateral occipital stroke , occipital transcranial magnetic stimulation (TMS) impairs blind participants' tactile performance (Cohen et al, 1997(Cohen et al, , 1999Kupers et al, 2007), and occipital TMS elicits sensations on the fingers in some participants (Ptito et al, 2008).…”