Shape perception reduces activity in human primary visual cortex

Abstract

Visual perception involves the grouping of individual elements into coherent patterns that reduce the descriptive complexity of a visual scene. The physiological basis of this perceptual simplification remains poorly understood. We used functional MRI to measure activity in a higher object processing area, the lateral occipital complex, and in primary visual cortex in response to visual elements that were either grouped into objects or randomly arranged. We observed significant activity increases in the lateral occipital complex and concurrent reductions of activity in primary visual cortex when elements formed coherent shapes, suggesting that activity in early visual areas is reduced as a result of grouping processes performed in higher areas. These findings are consistent with predictive coding models of vision that postulate that inferences of high-level areas are subtracted from incoming sensory information in lower areas through cortical feedback.O ne of the extraordinary capabilities of the human visual system is its ability to rapidly group elements in a complex visual scene, a process that can greatly simplify the description of an image. For example, a collection of parallel lines can be described as a single texture pattern without specifying the location, length, and orientation of each element within the pattern. Such grouping processes are reflected in the activities of neurons at various stages of the visual system. For example, the response of a neuron in primary visual cortex (V1) to a single visual element can be suppressed if the element in its receptive field shares the same orientation as surrounding elements, or enhanced if orientations differ (1). These pattern context effects in V1 are thought to be mediated by both local connections (2) and interactions with higher areas (3).In natural scenes, elements are often grouped when they are perceived as belonging to the same object. This case is particularly interesting from a physiological perspective because object shape is a feature that is represented only in higher stages of the visual system, so any influence of perceived shape on lower areas would require feedback processes. Although feedback is generally thought of as a process where activity in lower areas is enhanced by activity occurring in higher areas, recent work on probabilistic models has pointed to the importance of a phenomenon termed ''explaining away'': a competition that occurs between alternative hypotheses when attempting to infer the probable cause of an event (4). When applied to models of visual perception, perceptual hypotheses are thought to compete via feedback connections from higher visual areas projecting their predictions about the stimulus to lower stages, where they are then subtracted from incoming data. According to such predictive coding models, the activity of neurons in lower stages will decrease when neurons in higher stages can ''explain'' a visual stimulus (5, 6). These models can be contrasted with traditional feature-detection models, which posit that...

Predictive processing increases intelligibility of acoustically distorted speech: Behavioral and neural correlates

“…Thus, these counteracting effects may cancel each other out and, as a result, no changes would be observed within the auditory cortices. In contrast, our results suggest that brain activity can, indeed, decrease in the auditory cortex and surrounding areas when a stimulus becomes disambiguated, similarly as observed in the visual cortex in a related study (Murray, Kersten, Olshausen, Schrater, & Woods, 2002). As an alternative explanation for the lack of modulation effects, the detection power of the event‐related designs of the previous studies may have been insufficient to reveal decreased activity.…”

Predictive coding explains binocular rivalry: An epistemological review

“…The posterior probability depends on the likelihood (i.e., how well the hypothesis predicts the input); and on the prior probability of the hypothesis (i.e., how probable the hypothesis was before the input) (Friston, 2002;Kersten et al, 2004;Murray, Kersten, Olshausen, Schrater, & Woods, 2002). These prior expectations are constructed hierarchically and are context-sensitive.…”

Learning and inference in the brain

“…Friston (2002a,b) presented a number of examples from functional neuroimaging that demonstrated the contextsensitivity of evoked brain responses and the use of effective connectivity to establish interactions between bottom-up and top-down influences. Recent neuroimaging studies have addressed predictive coding explicitly, with some compelling results: Murray, Kersten, Olshausen, Schrater, and Woods (2002) used functional MRI to measure responses in V1 and a higher object processing area, the lateral occipital complex, to visual elements that were either grouped into objects or arranged randomly. They "observed significant activity increases in the lateral occipital complex and concurrent reductions of activity in primary visual cortex when elements formed coherent shapes, suggesting that activity in early visual areas is reduced as a result of grouping processes performed in higher areas.…”