Neural activity in early visual cortex reflects behavioral experience and higher-order perceptual saliency

Lee, Tai Sing; Yang, Cindy F.; Romero, R.; Mumford, David

doi:10.1038/nn0602-860

Cited by 193 publications

(153 citation statements)

References 36 publications

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“…In contrast, the activity in higher visual areas (in particular in parietal areas) was not affected by lighting direction (left vs. right), but instead reflected the perceived shape (convex vs. concave). Past studies had already highlighted several regions of the shape-from-shading network, in particular early visual areas (5)(6)(7)(8)(9) and to a lesser extent higher extrastriate (10) and parietal areas (11). Our study helps delineating the functions mediated by these different cortical areas.…”

Section: Discussionsupporting

confidence: 51%

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Prior knowledge of illumination for 3D perception in the human brain

Gerardin

Kourtzi

Mamassian

2010

Proc. Natl. Acad. Sci. U.S.A.

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In perceiving 3D shape from ambiguous shading patterns, humans use the prior knowledge that the light is located above their head and slightly to the left. Although this observation has fascinated scientists and artists for a long time, the neural basis of this "light from above left" preference for the interpretation of 3D shape remains largely unexplored. Combining behavioral and functional MRI measurements coupled with multivoxel pattern analysis, we show that activations in early visual areas predict best the light source direction irrespective of the perceived shape, but activations in higher occipitotemporal and parietal areas predict better the perceived 3D shape irrespective of the light direction. These findings demonstrate that illumination is processed earlier than the representation of 3D shape in the visual system. In contrast to previous suggestions, we propose that prior knowledge about illumination is processed in a bottom-up manner and influences the interpretation of 3D structure at higher stages of processing.functional MRI | multi-voxel pattern analysis | shape-from-shading | visual cortex | bottom-up processing A lthough the perception of 3D shape is critically important for actions and interactions in the environments we inhabit, most depth cues are ambiguous. As a result, the brain requires additional information based on previous experience with the environment to infer 3D shape from depth cues. In particular, the inference of 3D shape from shading patterns (i.e., using image luminance intensity variations to derive the shape of a surface) relies on the assumption that the scene illuminant is above our heads and slightly to the left (1, 2). Understanding the illumination of a visual scene has fascinated artists and scientists for a long time (3, 4), but the neural basis of this "light from above left" preference for the interpretation of 3D shape remains largely unexplored. Although the light-from-above preference is consistent with an ecological explanation, the left bias remains entirely unexplained. More generally, the light-from-above preference provides a simple example of the way the brain represents prior knowledge and opens the door for the investigation of other types of prior knowledge related to our perception of the motion, shape, and color of objects.Previous neurophysiological and imaging studies have implicated several brain regions in the processing of shape-fromshading: primary visual cortex (V1) (5-9), areas in the caudal inferior temporal gyrus (10) and the inferior parietal sulcus (11). However, the functions mediated by these different cortical areas may differ. In particular, interpreting shape-from-shading may involve at least two different stages of processing. At the first stage, the contrast polarity of edges in the image (dark or bright) is analyzed and related to the light direction so that left and right light directions can be discriminated. At the second stage, contrast edges are grouped together to form 3D shapes so that convex and concave shapes can be dis...

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Section: Discussionsupporting

confidence: 51%

“…Previous neurophysiological and imaging studies have implicated several brain regions in the processing of shape-fromshading: primary visual cortex (V1) (5)(6)(7)(8)(9), areas in the caudal inferior temporal gyrus (10) and the inferior parietal sulcus (11). However, the functions mediated by these different cortical areas may differ.…”

mentioning

confidence: 99%

Prior knowledge of illumination for 3D perception in the human brain

Gerardin

Kourtzi

Mamassian

2010

Proc. Natl. Acad. Sci. U.S.A.

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“…It is also known that V1 neurons are also influenced by the surrounding context of the stimuli [3][4][5][6]. The interpretations of the contextual modulations in these studies have been mostly limited to low-level mechanistic description in terms of facilitation and inhibition, or to subjective perceptual interpretations such as the neural correlate of contour processing, pop-out or figure-ground saliency [4,5,7,8]. Some of the observed contextual modulations likely arise from the feedback mediated by the massive amount of recurrent connections from the extrastriate areas to V1.…”

Section: Early Visual Cortexmentioning

confidence: 99%

“…In the second experiment [8], we asked two questions. First, does 3D shape from shading information, presumably computed in the higher visual areas, influence the processing in V1?…”

Section: Evidence Ii: Modulation By Shape From Shadingmentioning

confidence: 99%

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Top-down influence in early visual processing: a Bayesian perspective

Lee

2002

Physiology & Behavior

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Traditional views of visual processing suggest that early visual neurons are static spatiotemporal filters that extract local features by feedforward computation. The extracted information is then fed forward through a chain of modules to successively higher visual areas for further analysis. Recording from early visual neurons in awake behaving monkeys, we revealed there are many levels of complexity in the information processing of the early visual cortex. We found that the early visual neurons not only are sensitive to features within their receptive fields (RFs) but also to the global context of a visual scene, the behavioral relevance of the stimuli and the experience of the animals. These findings suggest that the early visual cortex (V1 and V2) is tightly coupled to and highly interactive with the rest of the visual system. The top-down interaction, mediated by recurrent feedback connections, introduces contextual information to influence the perceptual inference in the early visual cortex. D

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Differential depression of inhibitory synaptic responses in feedforward and feedback circuits between different areas of mouse visual cortex

Dong

Shao

Nerbonne

et al. 2004

J of Comparative Neurology

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Recordings of synaptic responses of pyramidal neurons to feedback (FB) inputs from higher to lower areas of visual cortex show that excitatory synaptic responses are only weakly opposed by disynaptic inhibition. Whether weak inhibition is preserved at high frequencies remains unknown. Whole-cell recordings were performed in pyramidal cells of mouse visual cortex to study the frequency dependence of excitatory and inhibitory postsynaptic currents (EPSCs, IPSCs) elicited by feedforward (FF) input from the primary visual cortex (V1) to the higher lateromedial area (LM) and by FB input from the LM to V1. EPSCs showed similar frequency dependencies in FF and FB pathways; the amplitudes decreased during stimulus trains, and the depression was larger at higher frequencies. IPSCs decreased during repetitive stimulation, and the depression increased at higher frequencies. At >20 Hz, the depression of IPSCs in the FB pathway was greater than in the FF pathway. Thus, unlike FF circuits, FB circuits provide balanced excitatory and inhibitory inputs across a wide range of frequencies. This property was shown to be critically important in cortical circuits that modulate the gain of pyramidal cell firing (Chance et al. [2002] Neuron 35:773-782).

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Neural activity in early visual cortex reflects behavioral experience and higher-order perceptual saliency

Cited by 193 publications

References 36 publications

Prior knowledge of illumination for 3D perception in the human brain

Prior knowledge of illumination for 3D perception in the human brain

Top-down influence in early visual processing: a Bayesian perspective

Differential depression of inhibitory synaptic responses in feedforward and feedback circuits between different areas of mouse visual cortex

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