Visual Attention and the Role of Normalization

Abstract

Visual perception can be improved by the intentional allocation of attention to specific visual components. This “top-down” attention can improve perception of specific locations in space, or of specific visual features at all locations in space. Both spatial and feature attention are thought to involve the feedback of attention signals from higher cortical areas to visual cortex, where it modulates the firing rates of specific sensory neurons. However, the mechanisms that determine how top-down attention signals modulate the firing rates of visual neurons are not fully understood. Recently, a sensory mechanism called normalization has been implicated in mediating neuronal modulations by attention. Normalization is a form of gain control that adjusts the dynamic range of neuronal responses, particularly when more than one stimulus lies within a neuron's receptive field. Models of attention propose that this sensory mechanism affects how attention signals modulate the firing rates of sensory neurons, but it remains unclear exactly how normalization is related to the different forms of top-down attention. Here we use single unit electrophysiological recordings from the middle temporal area (MT) of rhesus monkeys to measure the firing rates of sensory neurons. We ask the monkeys to perform a behavioral task that directs their attention to a particular location or feature, allowing us to independently measure modulations to firing rates due to normalization, spatial attention, or feature attention. We report that variations in the strength of normalization across neurons can be explained by an extension of conventional normalization: tuned normalization. Modulation by spatial attention depends greatly on the extent to which the normalization of a neuron is tuned, explaining a neuron-by-neuron correlation between spatial attention and normalization modulation strengths. Tuned normalization also explains a pronounced asymmetry in spatial attention modulations, in which neurons are more modulated by attention to their preferred, versus their non-preferred, stimulus. However, feature attention differs from spatial attention in its relationship to the normalization mechanism. We conclude that while spatial and feature attention appear to be mediated by a common top-down attention mechanism, they are differently influenced by the sensory mechanism of normalization.