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Supranormal orientation selectivity of visual neurons in orientation-restricted animals.

ABSTRACT: Altered sensory experience in early life often leads to remarkable adaptations so that humans and animals can make the best use of the available information in a particular environment. By restricting visual input to a limited range of orientations in young animals, this investigation shows that stimulus selectivity, e.g., the sharpness of tuning of single neurons in the primary visual cortex, is modified to match a particular environment. Specifically, neurons tuned to an experienced orientation in orientation-restricted animals show sharper orientation tuning than neurons in normal animals, whereas the opposite was true for neurons tuned to non-experienced orientations. This sharpened tuning appears to be due to elongated receptive fields. Our results demonstrate that restricted sensory experiences can sculpt the supranormal functions of single neurons tailored for a particular environment. The above findings, in addition to the minimal population response to orientations close to the experienced one, agree with the predictions of a sparse coding hypothesis in which information is represented efficiently by a small number of activated neurons. This suggests that early brain areas adopt an efficient strategy for coding information even when animals are raised in a severely limited visual environment where sensory inputs have an unnatural statistical structure.

SUBMITTER: Sasaki KS

PROVIDER: S-EPMC4644951 | biostudies-other | 2015

REPOSITORIES: biostudies-other

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Project description:Motion boundaries (local changes in visual motion direction) arise naturally when objects move relative to an observer. In human visual cortex, neuroimaging studies have identified a region (the kinetic occipital area [KO]) that responds more strongly to motion-boundary stimuli than to transparent-motion stimuli. However, some functional magnetic resonance imaging (fMRI) studies suggest that KO may encompass multiple visual areas and single-unit studies in macaque visual cortex have identified neurons selective for motion-boundary orientation in areas V2, V3, and V4, implying that motion-boundary selectivity may not be restricted to a single area. It is not known whether fMRI responses to motion boundaries are selective for motion-boundary orientation, as would be expected if these responses reflected the population activity of motion-boundary-selective neurons. We used an event-related fMRI adaptation protocol to measure orientation-selective responses to motion boundaries in human visual cortex. On each trial, we measured the response to a probe stimulus presented after an adapter stimulus (a vertical or horizontal motion-boundary grating). The probe stimulus was either a motion-boundary grating oriented parallel or orthogonal to the adapter stimulus or a transparent-motion stimulus. Orientation-selective adaptation for motion boundaries--smaller responses for trials in which test and adapter stimuli were parallel to each other--was observed in multiple extrastriate visual areas. The strongest adaptation, relative to the unadapted responses, was found in V3A, V3B, LO1, LO2, and V7. Most of the visual areas that exhibited orientation-selective adaptation in our data also showed response preference for motion boundaries over transparent motion, indicating that most of the human visual areas previously shown to respond to motion boundaries are also selective for motion-boundary orientation. These results suggest that neurons selective for motion-boundary orientation are distributed across multiple human visual cortical areas and argue against the existence of a single region or area specialized for motion-boundary processing.

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Supranormal orientation selectivity of visual neurons in orientation-restricted animals.

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