Eye Movement & Visual Selection

National Eye Institute

Investigators

Linked publications, trials & patents

Abstract

Introduction Our section investigates several inter-related fundamental brain functions: the selection of relevant visual signals, the active ignoring of irrelevant signals, and the ability to adaptively use visual signals to control appropriate actions. Disruptions of these functions are implicated in a variety of disorders, including attention deficit hyperactivity disorder (ADHD) and autism. Scientists in my section investigate the neuronal circuits involved in these visual functions using a range of techniques, in both non-human primates and mice, in order to understand how these neuronal circuits operate under normal conditions, to identify how breakdowns in these mechanisms cause disorders of sensory-motor coordination, and to uncover how mechanisms of learning and plasticity establish normal function and possible recovery of function. Standard models of these visual functions emphasize the role of the cerebral cortex. In contrast, our results demonstrate that higher-order functions like visual selective attention are built on top of conserved subcortical circuits in the superior colliculus (SC), thalamus and basal ganglia, that play a central role in action selection. Our aims are to understand the operation of the subcortical structures and how they interact with the cortex, with the long-term goal of identifying the detailed neuronal circuit so that more specific therapeutic interventions can be developed. 1) Neuronal circuits for the control of selective attention in primates Much of our work is done using non-human primates, whose close homology with humans makes them the best animal model of human visual attention. 1a) Microsaccades are a marker, not a cause for attention-related modulation in the brain When primates shift their attention to a new spatial location, they typically make a saccadic eye movement to align their fovea with the attended location. However, even when we dont shift our gaze but continue looking straight ahead, we often make very small saccades microsaccades that mark the direction and timing of how our attention has shifted covertly (i.e., without overtly looking). Recent studies have speculated that our ability to shift attention might be causally dependent on the occurrence of these small eye movements. If so, this would upend years of research studies that have carefully documented changes in the activity of visual neurons with attention if those changes are a consequence of microsaccades, then they would be a byproduct of eye movements rather than a key part of the mechanisms for attention. An alternative interpretation is that both the microsaccades and the changes in activity of visual neurons are due to changes in the state of attention in effect, two different measurable effects driven by a shared factor, namely the state of attention. We recently tested these ideas by measuring attention-related modulation in the midbrain superior colliculus during a visual task in which we carefully measured and documented the occurrence of microsaccades. Our results (published in eLife) demonstrate that attention-related modulation occurs even in the absence of microsaccades, showing that the modulation of these visual neurons is indeed part of the mechanism for attention rather than a byproduct of eye movements. Moreover, we confirmed that the occurrence of microsaccades also causes other types of modulation of visual neurons in particular, saccade-related visual suppression but these effects apply in addition to the effects of visual attention. These results are an important addition to our understanding because they show that microsaccades are not necessary for attention-related modulation but that they provide an additional marker for the state of attention, and can be especially informative at times when attention is shifting from one spatial location to another. 2) Role of subcortical neuronal circuits in visual detection and attention in mice Mice provide opportunities to work out the details of neuronal circuits in ways that are not yet possible in nonhuman primates and will help us identify worthwhile genetic and molecular targets in primates. 2a) Attention-related modulation of visual neurons in mice Building on our results in monkeys, in which we have demonstrated the importance of subcortical circuits in the control of visual attention, we predicted that visual neurons in subcortical brain structures in mice would also be implicated in the control of attention. This prediction was not certain, because visual attention has only recently been demonstrated in the mouse (e.g., our 2018 Current Biology paper) and there are many differences in the organization of the visual circuits between mice and primates. As a step toward using the mouse to functionally dissect these circuits for visual attention, we recently identified how neuronal activity in the midbrain superior colliculus are modulated during the allocation of visual attention and the performance of a learned visually guided task (published in Scientific Reports). Specifically, we found that spatial cueing modulated both firing rates and spike-count correlations, which have been implicated as a key factor that limits the efficiency of reading out activity from populations of neurons. We unexpectedly also found that this attention-related modulation was primarily due to enhancement at the cued location rather than suppression of activity at the uncued location, which points toward a circuit mechanism that selectively facilitates processing at the expected spatial location through this midbrain circuit. These results show how activity in the SC of the mouse can contribute to visual spatial attention and points toward specific circuit mechanisms. 2b) Stimulus-driven attention in mice In a related study in mice, we tested how unexpected visual events alter the state of visual attention. In human and nonhuman primates, it has been extensively documented that the occurrence of an unexpected visual event disrupts and shapes the allocation of visual attention. In particular, abrupt visual events tend to attract visual attention, at least briefly, an effect referred to as stimulus-driven attention. In a study published earlier this year (Journal of Vision), we tested whether similar effects on the state of attention also applied to the mouse. We found that task-irrelevant visual stimuli strongly altered visual task performance of mice, with a distinctive time course similar to that observed in primates. However, the effects we found in mice did not show the same spatial selectivity as what has been found in primates. These results show that a form of stimulus-driven attention exists in mice, validating the value of using mice to study these effects, but the differences in the details of the behavioral effects also caution against drawing overly generally conclusions about the similarity of the functional circuits between mice and primates.