Neural basis of visual attention in the primate brain

PROJECT SUMMARY Natural scenes are cluttered with multiple objects that compete for neural representation due to limited processing capacity. Mechanisms for selective processing, broadly referred to as visual attention, are therefore needed to prioritize relevant stimuli. Classic studies of spatial attention have largely ignored its temporal

dynamics, assuming that associated neural and behavioral effects were continuous for the duration of attentional deployment. Recent studies, however, have provided compelling evidence, in both humans and monkeys, that spatial attention fluctuates over time, sampling the environment in theta-rhythmic cycles (~4-8 Hz), associated

with alternating periods of either enhanced or diminished perceptual sensitivity. We have begun to uncover the neural basis for the rhythmic properties of spatial attention, both in humans and monkeys, across the large-scale network that subserves attention. We found that the phase of intrinsic theta rhythms across fronto-parietal cortex

and, in macaques, also in the pulvinar, predicted behavioral outcome. Neural evidence suggests that theta rhythms organize neural population activity into two alternating states: One that promotes sampling visual information from the presently attended location, and another one that promotes shifting attention to a new

location in the visual field. We have synthesized our findings and previous evidence into a novel framework, a rhythmic theory of attention. Based on this framework, our central hypothesis for the proposed project is that low-frequency rhythms serve as a clocking mechanism to coordinate sensory and motor processes in the

attention system and that these rhythms flexibly adjust to changing behavioral demands (e.g., varying cueing context). Using identical attention tasks in humans and macaques, we will establish common behavioral patterns and relate them to intracranial neural activity in both species. This approach aids in developing models for human

brain function, bridging the mesoscopic level of human intracranial EEG to cell-type specific neural population dynamics (e.g., laminar recordings) and causal manipulations (e.g., electrical microstimulation) obtainable in an animal model. Further, our studies will be among the first to record from the human thalamus. We will use

‘behavior-as-glue’ to guide our comparison of neural mechanisms across primate species and levels of analyses. Specifically, we will (i) investigate mechanisms for coordinating functional conflicts between visual and motor processes across the human brain and in functionally specialized populations of neurons in macaque FEF, LIP

and pulvinar, (ii) investigate mechanisms for fronto-parietal and thalamic control in organizing visual processes (including in macaque V4 at the laminar level), and (iii) investigate a causal role for pulvino-cortical interactions in shaping attention behaviors. Impairments of selective attention have devastating consequences on human

health (e.g., after stroke, and in neuropsychiatric diseases, such as schizophrenia). The significance of the proposed research is that it will test hypotheses from a novel and potentially paradigm-shifting framework using innovative and cutting-edge approaches at the level of cognitive large-scale networks and linked to behavior.