Daniel D. Dilks

Functional magnetic resonance imaging has revealed a set of regions selectively engaged in visual scene processing: the parahippocampal place area (PPA), the retrosplenial complex (RSC), and a region around the transverse occipital sulcus (previously known as “TOS”), here renamed the “occipital place area” (OPA). Are these regions not only preferentially activated by, but also causally involved in scene perception? Although past neuropsychological data imply a causal role in scene processing for PPA and RSC, no such evidence exists for OPA. Thus, to test the causal role of OPA in human adults, we delivered transcranial magnetic stimulation (TMS) to the right OPA (rOPA) or the nearby face-selective right occipital face area (rOFA) while participants performed fine-grained perceptual discrimination tasks on scenes or faces. TMS over rOPA impaired discrimination of scenes but not faces, while TMS over rOFA impaired discrimination of faces but not scenes. In a second experiment, we delivered TMS to rOPA, or the object-selective right lateral occipital complex (rLOC), while participants performed categorization tasks involving scenes and objects. TMS over rOPA impaired categorization accuracy of scenes but not objects, while TMS over rLOC impaired categorization accuracy of objects but not scenes. These findings provide the first evidence that OPA is causally involved in scene processing, and further show that this causal role is selective for scene perception. Our findings illuminate the functional architecture of the scene perception system, and also argue against the “distributed coding” view in which each category-selective region participates in the representation of all objects.

Electrophysiological and behavioral studies in many species have demonstrated mirror-image confusion for objects, perhaps because many objects are vertically symmetric (e.g., a cup is the same cup when seen in left or right profile). In contrast, the navigability of a scene changes when it is mirror reversed, and behavioral studies reveal high sensitivity to this change. Thus, we predicted that representations in object-selective cortex will be unaffected by mirror reversals, whereas representations in scene-selective cortex will be sensitive to such reversals. To test this hypothesis, we ran an event-related functional magnetic resonance imaging adaptation experiment in human adults. Consistent with our prediction, we found tolerance to mirror reversals in one object-selective region, the posterior fusiform sulcus, and a strong sensitivity to these reversals in two scene-selective regions, the transverse occipital sulcus and the retrosplenial complex. However, a more posterior object-selective region, the lateral occipital sulcus, showed sensitivity to mirror reversals, suggesting that the sense information that distinguishes mirror images is represented at earlier stages in the object-processing hierarchy. Moreover, one scene-selective region (the parahippocampal place area or PPA) was tolerant to mirror reversals. This last finding challenges the hypothesis that the PPA is involved in navigation and reorientation and suggests instead that scenes, like objects, are processed by distinct pathways guiding recognition and action.

Visual perceptual distortion (i.e., elongation) has been demonstrated in a single case study after several months of cortical deprivation after a stroke. Here we asked whether similar perceptual elongation can be observed in healthy participants after deprivation and, crucially, how soon after deprivation this elongation occurs. To answer this question, we patched one eye, thus noninvasively and reversibly depriving bottom-up input to the region of primary visual cortex (V1) corresponding to the blind spot (BS) in the unpatched eye, and tested whether and how quickly elongation occurs after the onset of deprivation. Within seconds of eye patching, participants perceived rectangles adjacent to the BS to be elongated toward the BS. We attribute this perceptual elongation to rapid receptive field expansion within the deprived V1 as reported in electrophysiological studies after retinal lesions and refer to it as “referred visual sensations” (RVS). This RVS is too fast to be the result of structural changes in the cortex (e.g., the growth of new connections), instead implicating unmasking of preexisting connections as the underlying neural mechanism. These findings may shed light on other reported perceptual distortions, as well as the phenomena of “filling-in.”

Recent work has shown that foveal cortex, deprived of its normal bottom-up input as a result of macular degeneration (MD), begins responding to stimuli presented to a peripheral retinal location. However, these studies have only presented stimuli to the “preferred retinal location,” or PRL, a spared part of the peripheral retina used by individuals with MD for fixating, face recognition, reading, and other visual tasks. Thus, previous research has not yet answered a question critical for understanding the mechanisms underlying this reorganization: Does formerly foveal cortex respond only to stimuli presented at the PRL, or does it also respond to other peripheral locations of similar eccentricity? If foveal cortex responds to stimuli at PRL because it is the long-term habitual use of this region as a functional fovea that drives the formerly foveal cortex to respond to stimuli presented at the PRL (the “use-dependent reorganization” hypothesis), then foveal cortex will not respond to stimuli presented at other locations. Alternatively, it may be that foveal cortex responds to any peripheral retinal input, independent of whether input at that retinal location has been chronically attended for months or years (the “use-independent reorganization” hypothesis). Using fMRI, we found clear activation of formerly foveal cortex to stimuli presented at either the PRL or an isoeccentric non-PRL location in two individuals with MD, supporting the use-independent reorganization hypothesis. This finding suggests that reorganization is driven by passive, not use-dependent mechanisms.

Evidence suggests that visual processing is divided into the dorsal (‘how’) and ventral (‘what’) streams. We examined the normal development of these streams and their breakdown under neurological deficit by comparing performance of normally developing children and Williams syndrome individuals on two tasks: a visually guided action (‘how’) task, in which participants posted a card into an oriented slot, and a perception (‘what’) task, in which they matched a card to the slot's orientation. Results showed that all groups performed worse on the action task than the perception task, but the disparity was more pronounced in WS individuals and in normal 3–4‐year‐olds than in older children. These findings suggest that the ‘how’ system may be relatively slow to develop and more vulnerable to breakdown than the ‘what’ system.

Neural and behavioral evidence for cortical reorganization in the adult somatosensory system after loss of sensory input (e.g., amputation) has been well documented. In contrast, evidence for reorganization in the adult visual system is far less clear: neural evidence is the subject of controversy, behavioral evidence is sparse, and studies combining neural and behavioral evidence have not previously been reported. Here, we report converging behavioral and neuroimaging evidence from a stroke patient (B.L.) in support of cortical reorganization in the adult human visual system. B.L.'s stroke spared the primary visual cortex (V1), but destroyed fibers that normally provide input to V1 from the upper left visual field (LVF). As a consequence, B.L. is blind in the upper LVF, and exhibits distorted perception in the lower LVF: stimuli appear vertically elongated, toward and into the blind upper LVF. For example, a square presented in the lower LVF is perceived as a rectangle extending upward. We hypothesized that the perceptual distortion was a consequence of cortical reorganization in V1. Extensive behavioral testing supported our hypothesis, and functional magnetic resonance imaging (fMRI) confirmed V1 reorganization. Together, the behavioral and fMRI data show that loss of input to V1 after a stroke leads to cortical reorganization in the adult human visual system, and provide the first evidence that reorganization of the adult visual system affects visual perception. These findings contribute to our understanding of the human adult brain's capacity to change and has implications for topics ranging from learning to recovery from brain damage.