Preparatory activity in occipital cortex in early blind humans predicts auditory perceptual performance

Abstract

Early onset blindness leads to a dramatic alteration in the way the world is perceived, a change that is detectable in the organization of the brain. Several studies have confirmed that blindness leads to functional alterations in occipital cortices that normally serve visual functions. These reorganized brain regions respond to a variety of tasks and stimuli, but their specific functions are unclear. In sighted individuals, several studies have reported preparatory activity in retinotopic areas, which enhances perceptual sensitivity. "Baseline shifts," changes in activity associated with a cue predicting an upcoming event, provides a marker for attentional modulation. Here we demonstrate that, in early blind subjects, medial occipital areas produced significant blood oxygenation level-dependent (BOLD) responses to a cue signaling an auditory discrimination trial but not to a cue indicating a no-trial period. Furthermore, the amplitude of the BOLD response in the anterior calcarine sulcus of early blind subjects correlated with their discrimination performance on the auditory backward masking task. Preparatory BOLD responses also were present in auditory cortices, although they were more robust in blind than sighted control subjects. The pattern of response in visual areas is similar to preparatory effects observed during visual selective attention in sighted subjects and consistent with the hypothesis that the mechanisms implicated in visual attention continue to modulate occipital cortex in the early blind. A possible source of this top-down modulation may be the frontoparietal circuits that retain their connectivity with the reorganized occipital cortex and as a result influence processing of nonvisual stimuli in the blind.

Figure 1.

Schematic of the three trial conditions used in the fMRI study. a, Auditory backward recognition masking trial structure. b, During scanning, a trial cue (dark square with black line rising left to right) preceded the trial by one volume acquisition, and the trials were presented during the silent period between acquisitions. Trials were separated by three, four, five, or seven volume acquisitions. c, d, Trial-cue alone trials (c) and no-trial cue (d) (dark square with black line falling left to right) trials, were followed by a variable intertrial interval. e, EB and SC performance on the 40 and 160 ms mask delay conditions during scanning.

Figure 2.

a, b, Two regions of interest identified in the early onset blind subjects in the anterior (a) (blue arrows) and posterior (b) calcarine sulcus (yellow arrow) produced event-related BOLD response with a differential response to the TCA and NTC conditions. c, d, In contrast, the SC subjects had small event-related responses to both TCA and NTC conditions in the anterior (c) and posterior (d) calcarine sulcus. L, Left; R, right.

Figure 3.

a, b, Scatter plots and best-fit lines showing the correlation between early blind individuals' averaged performance on the 40 and 160 ms ABRM trials and percentage signal change 4.6 s after the expected trial onset for the trial-cue alone condition (a) and the no-trial cue (b).

Figure 4.

a, Regions with significantly greater signal to the trial-cue alone than to the no-trial cue within the left and right temporal lobes in the early blind (orange) and sighted control (green) groups. b–e, Event-related response plots for the left and right planum temporale and superior temporal sulcus in early blind (b, d) and sighted control (c, e) groups.*p < 0.05.