Sensitive period for a multimodal response in human visual motion area MT/MST

Abstract

The middle temporal complex (MT/MST) is a brain region specialized for the perception of motion in the visual modality. However, this specialization is modified by visual experience: after long-standing blindness, MT/MST responds to sound. Recent evidence also suggests that the auditory response of MT/MST is selective for motion. The developmental time course of this plasticity is not known. To test for a sensitive period in MT/MST development, we used fMRI to compare MT/MST function in congenitally blind, late-blind, and sighted adults. MT/MST responded to sound in congenitally blind adults, but not in late-blind or sighted adults, and not in an individual who lost his vision between ages of 2 and 3 years. All blind adults had reduced functional connectivity between MT/MST and other visual regions. Functional connectivity was increased between MT/MST and lateral prefrontal areas in congenitally blind relative to sighted and late-blind adults. These data suggest that early blindness affects the function of feedback projections from prefrontal cortex to MT/MST. We conclude that there is a sensitive period for visual specialization in MT/MST. During typical development, early visual experience either maintains or creates a vision-dominated response. Once established, this response profile is not altered by long-standing blindness.

Figure 1

Activity in left and right MT/MST ROIs for sighted (green), congenitally blind (red) and late blind (blue). A: Activity to the high motion condition (footsteps) is shown in solid lines, and activity to the low-motion condition (tones) is shown in dashed line. The data reflect percent signal change relative to baseline, plotted as a function of time in seconds. Inset figures display the MT/MST ROIs overlaid on a normalized template. B: Percent signal change (PSC) in left and right MT/MST ROIs for individual subjects. On the left, PSC for the mean of the high and low motion conditions relative to rest. On the right, PSC difference between the high and low motion conditions. Each point represents a single subject. Congenitally Blind: CB (red), Late Blind: LB (blue), Sighted (green), EB is the single participant who lost his vision between the ages of 2 and 3 (black). In the box plots of the data the middle line marks the 50^th percentile (median), the lowest edge of the box marks the 25^th percentile and the upper edge of the box marks the 75^th percentile. The box whiskers terminate at 1.5 standard deviations away from the median (10^th and 90^th percentiles). The width of the boxplot indicates sample size. The boxplots illustrate that EB is different from the congenitally blind population, but not from the sighted or late blind populations in mean the high motion+low motion > rest contrast bilateral MT/MST, and in the high motion>low motion contrast of left MT/MST, but not right MT/MST.

Figure 2

Greater BOLD signal in the congenitally blind, relative to the sighted groups (A) and activity in congenitally blind and sighted groups separately (B) (in red). High and low motion conditions relative to rest (left) and in the high motion condition relative to the low motion condition (right) (p<.05, corrected). Activation during a visual motion task in a separate group of participants is presented in white. Overlap of activation during motion sound task and visual motion task appears pink. As can be seen in panels A and B, motion sound activation and visual motion activation overlap in the region of MT/MST. Additionally, MT/MST activation in the congenitally blind group is similar to previous reports of MT/MST activity in sighted individuals. The average coordinates from five representative studies fall within the auditory motion activation in the congenitally blind group (mean left MT/MST −45, −70, 4, mean right MT/MST 43, −69, 5 [, –13]). This overlap suggests similar MT/MST localization in the sighted and congenitally blind, but does not preclude the possibility that the location of functional area MT/MST is subtly different with respect to anatomy in congenitally blind individuals. For list of brain regions depicted in this figure, see Table S2.

Figure 3

Functional connectivity results from experiment 2. All maps are FDR corrected for multiple comparisons at p<.05. Regions more correlated with MT/MST across groups are shown in red, regions less correlated with MT/MST are shown in blue. A. Regions differentially correlated with MT/MST in the congenitally blind relative to sighted adults. B. Regions less correlated with MT/MST in late blind relative to sighted adults. C. Regions more correlated with MT/MST in the congenitally blind relative to late blind adults. Numbers correspond to approximate Brodmann areas in dorsolateral prefrontal and retinotopic visual areas. For a complete list of Brodmann areas see Table S3.