Abstract
Extrastriate area V4 is a critical component of visual form processing in both humans and non-human primates. Previous studies have shown that the tuning properties of V4 neurons demonstrate an intermediate level of complexity that lies between the narrow band orientation and spatial frequency tuning of neurons in primary visual cortex and the highly complex object selectivity seen in inferotemporal neurons. However, the nature of feature selectivity within this cortical area is not well understood, especially in the context of natural stimuli. Specifically, little is known about how the tuning properties of V4 neurons, measured in isolation, translate to feature selectivity within natural scenes. In this study, we assessed the degree to which preferences for natural image components can readily be inferred from classical orientation and spatial frequency tuning functions. Using a psychophysically-inspired method we isolated and identified the specific visual “driving features” occurring in natural scene photographs that reliably elicited spiking activity from single V4 neurons. We then compared the measured driving features to those predicted based on the spectral receptive field (SRF), estimated from responses to narrowband sinusoidal grating stimuli. This approach provided a quantitative framework for assessing the degree to which linear feature selectivity was preserved during natural vision. First, we found evidence of both spectrally and spatially tuned suppression within the receptive field, neither of which were present in the linear SRF. Second, we found driving features that were stable during translation of the image across the receptive field (due to small fixational eye movements). The degree of translation invariance fell along a continuum, with some cells showing nearly complete invariance across the receptive field and others exhibiting little to no position invariance. This form of limited translation invariance could indicate that a subset of V4 neurons are insensitive to small fixational eye movements, supporting perceptual stability during natural vision.
Highlights
A fundamental challenge in visual neuroscience is to understand and model the relationship between arbitrary complex visual stimuli and the corresponding patterns of activity they evoke in visual neurons
In this study we used neurophysiological responses to partially masked natural scene stimuli to explore the origins of feature selectivity in spectrally complex natural scene stimuli in area V4 of the primate
Our results indicate feature selectivity in V4 is highly non-linear, and while the quasi-linear spectral receptive field (SRF) model can predict a substantial fraction of V4 response variance under some conditions, it is not sufficient to fully model selectivity for spectrally complex stimuli (Oleskiw et al, 2014)
Summary
A fundamental challenge in visual neuroscience is to understand and model the relationship between arbitrary complex visual stimuli and the corresponding patterns of activity they evoke in visual neurons. Some have questioned whether the visual features that drive neuronal activity during natural vision are the same. Despite the fact that V1 neurons exhibit a number of well-established static and dynamic non-linearities [e.g., spiking thresholds (Chichilnisky, 2001) and contrast gain control (Ohzawa et al, 1982; Heeger, 1992)], in many instances the linear SRF accurately predicts responses to both narrowband (i.e., sinusoidal gratings) and more complex natural scene stimuli (Theunissen et al, 2001; David et al, 2004). Consistent with this, Felsen et al (2005) demonstrated that in V1 the SRF, even when computed from responses to simple stimuli, can be used to readily identify key features in natural scenes that drive neurons to spike
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