Impact of Deprivation and Preferential Usage on Functional Connectivity Between Early Visual Cortex and Category-Selective Visual Regions

Abstract

Human behavior can be remarkably shaped by experience, such as the removal of sensory input. Many studies of conditions such as stroke, limb amputation, and vision loss have examined how removal of input changes brain function. However, an important question yet to be answered is: when input is lost, does the brain change its connectivity to preferentially use some remaining inputs over others? In individuals with healthy vision, the central portion of the retina is preferentially used for everyday visual tasks, due to its ability to discriminate fine details. When central vision is lost in conditions like macular degeneration, peripheral vision must be relied upon for those everyday tasks, with some portions receiving "preferential" usage over others. Using resting-state fMRI collected during total darkness, we examined how deprivation and preferential usage influence the intrinsic functional connectivity of sensory cortex by studying individuals with selective vision loss due to late stages of macular degeneration. Specifically, we examined functional connectivity between category-selective visual areas and the cortical representation of three areas of the retina: the lesioned area, a preferentially used region of the intact retina, and a non-preferentially used region. We found that cortical regions representing spared portions of the peripheral retina, regardless of whether they are preferentially used, exhibit plasticity of intrinsic functional connectivity in macular degeneration. Cortical representations of spared peripheral retinal locations showed stronger connectivity to MT, a region involved in processing motion. These results suggest that the long-term loss of central vision can produce widespread effects throughout spared representations in early visual cortex, regardless of whether those representations are preferentially used. These findings support the idea that connections to visual cortex maintain the capacity for change well after critical periods of visual development.

Keywords: FFA; MT; V1; fMRI; functional connectivity; lesion projection zone; macular degeneration; plasticity; sensory deprivation; visual cortex.

FIGURE 1

Schematic of early visual cortex ROI Definition. The perceptual experience of individuals with macular degeneration in comparison to healthy vision is shown in (A). In macular degeneration, a lesion forms in the center of the retina, rendering patients unable to see in the center of the visual field (gray patch). Retinal imaging was first conducted using microperimetry separately in both eyes (B). The PRL (preferred retinal locus), URL (un‐preferred retinal locus), and lesion are then determined (C). Using this information, a retinotopic atlas of visual cortex is then is used (D—left) to map the cortical representations of these three loci in early visual cortex (V1, V2, V3), shown on the right (D).

FIGURE 2

Individual participant retinal images. Retinal images from microperimetry are shown for 4 representative individuals. PRL locations are shown in yellow. URL locations are shown in green. Microperimetry images for left and right eyes are shown in upper corners of each panel. Center images show combined image of left and right retinal images. Mapping onto left and right cortical surfaces are shown in bottom corners of each panel.

FIGURE 3

Connectivity to fusiform face area. Panel A shows the corresponding regions in visual space of the three early visual cortex regions of interest: The lesion projection zone (LPZ) in blue, the cortical representation of the preferred retinal locus (cPRL) and the cortical representation of the un‐preferred retinal locus (cURL). These regions were defined in early visual cortex using the methods described in Figure 1. Functional connectivity was measured between these regions and fusiform face area (FFA), shown in panel B. Fisher's Z‐transformed connectivity values between the three early visual cortex ROIs and FFA are shown for healthy controls (HC) and macular degeneration patients (MD) in panel C (color‐coded based on panel A). Connectivity to FFA was significantly higher for the LPZ, relative to the cPRL and cURL, in both groups (C). Group means for each ROI are shown in D. Error bars in both figures represent the standard error of the mean. Stars (*) denote statistical significance levels based on the following conventions: *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001.

FIGURE 4

Connectivity to parahippocampal area. Panel A shows the corresponding regions in visual space of the three early visual cortex regions of interest: The lesion projection zone (LPZ) in blue, the cortical representation of the preferred retinal locus (cPRL) and the cortical representation of the un‐preferred retinal locus (cURL). These regions were defined in early visual cortex using the methods described in Figure 1. Functional connectivity was measured between these regions and parahippocampal area (PHA), shown in panel B. Fisher's Z‐transformed connectivity values between the three early visual cortex ROIs and PHA are shown for healthy controls (HC) and macular degeneration patients (MD) in panel C (color‐coded based on panel A). A two‐way, repeated measures ANOVA revealed a significant main effect of early visual cortex ROI, such that LPZ connectiviy was higher relative to cortical representations of the PRL and URL in both groups (C). Group means for each ROI are shown in D. Error bars in both figures represent the standard error of the mean. Stars (*) denote statistical significance levels based on the following conventions: *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001.

FIGURE 5

Connectivity to middle temporal area. Panel A shows the corresponding regions in visual space of the three early visual cortex regions of interest: The lesion projection zone (LPZ) in blue, the cortical representation of the preferred retinal locus (cURL). These regions were defined in early visual cortex using the methods described in Figure 1. Functional connectivity was measured these regions and middle temporal area (MT) are shown in panel B for visualization purposes only. Fisher's Z‐transformed connectivity values between the three early visual cortex ROIs and MT are shown for healthy controls (HC) and macular degeneration patients (MD) in panel C (color‐coded based on panel A). Group means are shown in D.

FIGURE 6

Central versus peripheral connectivity to middle temporal area. Wilcoxon rank sum tests revealed that PRL connectivity (A) and URL connectivity (B) relative to central (LPZ) connectivity were significantly greater in MD participants realtive to healthy vision controls (both p < 0.01). Similar results were found when examining the mean of the two perpiheral ROIs (cPRL and cURL) realtive to central (LPZ) connectivity (C). Stars (*) denote statistical significance levels based on the following conventions: *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001.

FIGURE 7

Generalizability of peripheral connectivity difference. Connectivity of all peripheral regions to MT was calculated in order to probe the generalizability of the previous observed effects. Schematic of the all peripheral regions (yellow) and lesion region (blue) are shown (A). Connectivity between each early visual cortex ROI and MT are shown in (B). A direct comparison of “all peripheral” minus LPZ difference scores are also shown (C), revealing greater peripheral relative to central connectivity in MD participants (p < 0.0.01). Statistical analysis in (C) was performed using a Wilcoxon rank sum test. Error bars for all figures represent the standard error of the mean. Stars (*) denote statistical significance levels based on the following conventions: *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001.