2018Journal of NeuroscienceOpen access

Neural Correlate of Visual Familiarity in Macaque Area V2

Ge Huang, Suchitra Ramachandran, Tai Sing Lee, Carl R. Olson

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Abstract

Neurons in macaque inferotemporal cortex (ITC) respond less strongly to familiar than to novel images. It is commonly assumed that this effect arises within ITC because its neurons respond selectively to complex images and thus encode in an explicit form information sufficient for identifying a particular image as familiar. However, no prior study has examined whether neurons in low-order visual areas selective for local features also exhibit familiarity suppression. To address this issue, we recorded from neurons in macaque area V2 with semichronic microelectrode arrays while monkeys repeatedly viewed a set of large complex natural images. We report here that V2 neurons exhibit familiarity suppression. The effect develops over several days with a trajectory well fitted by an exponential function with a rate constant of ∼100 exposures. Suppression occurs in V2 at a latency following image onset shorter than its reported latency in ITC. SIGNIFICANCE STATEMENT Familiarity suppression, the tendency for neurons to respond less strongly to familiar than novel images, is well known in monkey inferotemporal cortex. Suppression has been thought to arise in inferotemporal cortex because its neurons respond selectively to large complex images and thus explicitly to encode information sufficient for identifying a particular image as familiar. No previous study has explored the possibility that familiarity suppression occurs even in early-stage visual areas where neurons are selective for simple features in confined receptive fields. We now report that neurons in area V2 exhibit familiarity suppression. This finding challenges our current understanding of information processing in V2 as well as our understanding of the mechanisms that underlie familiarity suppression.

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Neurons in macaque inferotemporal cortex (ITC) respond less strongly to familiar than to novel images. It is commonly assumed that this effect arises within ITC because its neurons respond selectively to complex images and thus encode in an explicit form information sufficient for identifying a particular image as familiar. However, no prior study has examined whether neurons in low-order visual areas selective for local features also exhibit familiarity suppression. To address this issue, we recorded from neurons in macaque area V2 with semichronic microelectrode arrays while monkeys repeatedly viewed a set of large complex natural images. We report here that V2 neurons exhibit familiarity suppression. The effect develops over several days with a trajectory well fitted by an exponential function with a rate constant of ∼100 exposures. Suppression occurs in V2 at a latency following image onset shorter than its reported latency in ITC. SIGNIFICANCE STATEMENT Familiarity suppression, the tendency for neurons to respond less strongly to familiar than novel images, is well known in monkey inferotemporal cortex. Suppression has been thought to arise in inferotemporal cortex because its neurons respond selectively to large complex images and thus explicitly to encode information sufficient for identifying a particular image as familiar. No previous study has explored the possibility that familiarity suppression occurs even in early-stage visual areas where neurons are selective for simple features in confined receptive fields. We now report that neurons in area V2 exhibit familiarity suppression. This finding challenges our current understanding of information processing in V2 as well as our understanding of the mechanisms that underlie familiarity suppression.

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Available abstract

Neurons in macaque inferotemporal cortex (ITC) respond less strongly to familiar than to novel images. It is commonly assumed that this effect arises within ITC because its neurons respond selectively to complex images and thus encode in an explicit form information sufficient for identifying a particular image as familiar. However, no prior study has examined whether neurons in low-order visual areas selective for local features also exhibit familiarity suppression. To address this issue, we recorded from neurons in macaque area V2 with semichronic microelectrode arrays while monkeys repeatedly viewed a set of large complex natural images. We report here that V2 neurons exhibit familiarity suppression. The effect develops over several days with a trajectory well fitted by an exponential function with a rate constant of ∼100 exposures. Suppression occurs in V2 at a latency following image onset shorter than its reported latency in ITC. SIGNIFICANCE STATEMENT Familiarity suppression, the tendency for neurons to respond less strongly to familiar than novel images, is well known in monkey inferotemporal cortex. Suppression has been thought to arise in inferotemporal cortex because its neurons respond selectively to large complex images and thus explicitly to encode information sufficient for identifying a particular image as familiar. No previous study has explored the possibility that familiarity suppression occurs even in early-stage visual areas where neurons are selective for simple features in confined receptive fields. We now report that neurons in area V2 exhibit familiarity suppression. This finding challenges our current understanding of information processing in V2 as well as our understanding of the mechanisms that underlie familiarity suppression.

Key concepts: Macaque, Neuroscience, Psychology, Visual cortex, Visual system, Cognitive psychology, Communication

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