Motion processing after sight restoration: No competition between visual recovery and auditory compensation

Neuroimage. 2018 Feb 15;167:284-296. doi: 10.1016/j.neuroimage.2017.11.050. Epub 2017 Nov 23.

Abstract

The present study tested whether or not functional adaptations following congenital blindness are maintained in humans after sight-restoration and whether they interfere with visual recovery. In permanently congenital blind individuals both intramodal plasticity (e.g. changes in auditory cortex) as well as crossmodal plasticity (e.g. an activation of visual cortex by auditory stimuli) have been observed. Both phenomena were hypothesized to contribute to improved auditory functions. For example, it has been shown that early permanently blind individuals outperform sighted controls in auditory motion processing and that auditory motion stimuli elicit activity in typical visual motion areas. Yet it is unknown what happens to these behavioral adaptations and cortical reorganizations when sight is restored, that is, whether compensatory auditory changes are lost and to which degree visual motion processing is reinstalled. Here we employed a combined behavioral-electrophysiological approach in a group of sight-recovery individuals with a history of a transient phase of congenital blindness lasting for several months to several years. They, as well as two control groups, one with visual impairments, one normally sighted, were tested in a visual and an auditory motion discrimination experiment. Task difficulty was manipulated by varying the visual motion coherence and the signal to noise ratio, respectively. The congenital cataract-reversal individuals showed lower performance in the visual global motion task than both control groups. At the same time, they outperformed both control groups in auditory motion processing suggesting that at least some compensatory behavioral adaptation as a consequence of a complete blindness from birth was maintained. Alpha oscillatory activity during the visual task was significantly lower in congenital cataract reversal individuals and they did not show ERPs modulated by visual motion coherence as observed in both control groups. In contrast, beta oscillatory activity in the auditory task, which varied as a function of SNR in all groups, was overall enhanced in congenital cataract reversal individuals. These results suggest that intramodal plasticity elicited by a transient phase of blindness was maintained and might mediate the prevailing auditory processing advantages in congenital cataract reversal individuals. By contrast, auditory and visual motion processing do not seem to compete for the same neural resources. We speculate that incomplete visual recovery is due to impaired neural network turning which seems to depend on early visual input. The present results demonstrate a privilege of the first arriving input for shaping neural circuits mediating both auditory and visual functions.

Keywords: Auditory motion processing; Beta oscillations; Congenital cataracts; Event-related potentials; Sight restoration; Visual motion processing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Alpha Rhythm / physiology
  • Auditory Perception / physiology*
  • Beta Rhythm / physiology*
  • Blindness / congenital
  • Blindness / physiopathology
  • Blindness / surgery
  • Cataract / congenital
  • Cataract / physiopathology*
  • Cataract Extraction
  • Cerebral Cortex / physiopathology*
  • Child
  • Evoked Potentials / physiology*
  • Female
  • Humans
  • Male
  • Motion Perception / physiology*
  • Vision Disorders / congenital
  • Vision Disorders / physiopathology*
  • Vision Disorders / surgery
  • Young Adult