Luminance contrast: stimulus energy or basic feature? Evidence for non-monotonic luminance contrast tuning and contrast-invariant behaviour in V4 neurons

Contrast is an important element of the visual world. It is one of the fundamental properties needed for image perception; the visual features that allow the cerebral representation of an object are shape, colour, texture, position, depth and movement; contrast is involved in the elaboration of all these properties. A particular form of contrast is luminance contrast, the physical quantity that specifies the relative variation in luminance of a visual stimulus compared to its averaged level or to the averaged level of the background. Most cortical visual neurons display a sigmoidal increase of their response with respect to the luminance contrast of a stimulus falling on their receptive field, and contrast has therefore been considered as a modulation of stimulus energy. However, behavioural and psychophysical evidence suggests that at least a fraction of cortical visual neurons might show a non-monotonic tuning profile in response to varying contrast levels. We aimed to further explore the contrast response function (CRF) of neurons in macaque area V4, an intermediate node along the ventral pathway of cortical visual processing. To pursue this goal, our approach mainly focused on a fine characterization of the CRF of individual neurons, as we believe that this may represent a critical factor to be taken into account in order to achieve a full understanding of the meaning of luminance contrast in the visual system. Luminance contrast, as a key factor to determine salience of a visual stimulus, is also an ideal candidate to study the interplay between exogenous and endogenous attention is. A typical visual scene contains a great deal more information than we can process, but when we open our eyes we have the clear impression of understanding what we see. This requires selecting relevant information out of the irrelevant noise. Visual selective attention is the neuro-cognitive mechanism that ensures selection of behaviourally relevant information to guide behaviour. A number of psychophysical and neurophysiological studies have shown that directing attention to a stimulus increases perceptual and neuronal sensitivity, so that responses to an attended stimulus are increased as they would be if stimulus intensity were increased. Other studies have instead reported a multiplicative effect of attention, namely a rescaling (or gain increase) of responses proportional to stimulus intensity. Deployment of visual selective attention can be controlled in two principal ways. On the one hand, attention can be deployed due to intrinsic properties of the retinal input, especially the relative salience of items in the visual field, that can be manipulated through changes in luminance contrast; this attentional mechanism is known as exogenous or bottom-up or transient control. On the other hand, attention can be deployed volitionally, on the basis of an internal or endogenous strategy, known as top-down or sustained control. Much is known about the neuronal mechanisms underlying these two forms of attentional deployment, but we are still far from a full understanding of the way in which they interact with one other. Therefore, we aimed also to further explore the effects of endogenous attention on the contrast response function (CRF) of V4 neurons as we believe that the fine characterization of the CRF of individual neurons may represent a critical factor to be taken into account in order to understand the interplay between endogenous attention and stimulus contrast. We recorded the responses of individual neurons from the brain of one behaving macaque, and tested the neurons with a set of stimuli that spanned the complete range of stimulus contrasts (from zero to nearly maximal) during different states of attention. Besides neurons with traditional CRFs, we were able to demonstrate the presence of neurons which were not appreciably modulated by contrast - a candidate correlate for the phenomenon of contrast invariance in object recognition - and, more importantly, of cells showing a non-monotonic tuning profile in response to varying stimulus contrast. The latter two types of neurons have been completely overlooked in past explorations of CRFs in area V4. Importantly, for non-monotonic tuned neurons, contrast is to be considered as a feature of the stimulus instead of a factor determining stimulus strength, and the interplay between contrast and attention should be especially reconsidered for this class of neurons.