Abstract
Visual attention dramatically improves subjects’ ability to see and also modulates the responses of visual and oculomotor neurons. Despite hundreds of studies demonstrating the co-occurrence of behavioral and neuronal effects of attention 1, the relationship between neuronal modulations and improved performance remains unknown. There are three dominant hypotheses (Figure 1A): that attention 1) improves visual information coding 2,3, 2) improves communication between visual and oculomotor brain areas 4, or 3) reduces uncontrolled fluctuations in the animals’ cognitive state, thereby improving performance and rendering observed effects of attention on response variability as epiphenomena 5. Here we show that none of these hypotheses account for observed perceptual improvements and we provide evidence for a novel hypothesis: that the well known effects of attention on firing rates and shared response variability in visual cortex reshape the representation of attended stimuli such that they more effectively drive downstream neurons and guide decisions without explicitly changing the weights relating sensory responses to downstream neurons or behavior (Figure 1B). We assessed each hypothesized mechanism by recording simultaneously from groups of neurons in two stages of visuomotor processing: area MT, which encodes motion information 6 and the superior colliculus (SC), where neuronal responses are either visual, oculomotor, or intermediate 7-9 and have been hypothesized to be involved in computing perceptual decisions 10. Constraining our analyses by the animals’ behavior and the simultaneous recordings from both areas allowed us to reject each prior hypothesis and greatly clarified the relationship between attention, neuronal responses and behavior. Our results suggest a path toward understanding the neural underpinnings of perception and cognition in health and disease by analyzing neuronal responses in ways that are constrained by behavior and interactions between brain areas.
Main We compared evidence for and against three hypothesized attention mechanisms using neuronal responses collected while two rhesus monkeys performed a widely studied motion direction change-detection task Figure 1C; 11,12,13. The animals’ performance was greatly affected (Figure 1D) by a cue instructing them to shift spatial attention between a stimulus within the same or opposite hemifield as the joint receptive fields of several dozen neurons that were recorded on multielectrode probes in MT (Figure 1E, red points) and the SC (blue points). MT and the SC represent different stages of perceptual decision-making and therefore provide the opportunity to evaluate each hypothesized attention mechanism. MT contributes to motion perception 6,14. The SC is thought to play many roles in visually guided tasks 7-9, decision-making 10,15 and attention16.