Introduction The ability to selectively process visual inputs and generate appropriate actions is a crucial function of the primate brain, and one that is implicated in a variety of disorders, including attention deficit hyperactivity disorder (ADHD) and autism. Scientists in my section investigate the neuronal circuits involved in this visual function using a range of techniques, in both non-human primates and mice, in order to understand how these neuronal circuits operate under normal conditions and to identify how breakdowns in these mechanisms cause disorders of sensory-motor coordination. Although standard models of visual attention emphasize the role of the cortex, we discovered that the Superior Colliculus (SC) contributes to visual attention through mechanisms that are independent of the visual cortex. Consequently, we proposed that even though attention is considered a high-order brain function, it is built on top of conserved subcortical circuits in the midbrain, 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 Most 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) SC activity is necessary for effects of selective attention on perception Improving performance with spatial cues is one of the defining features of visual selective attention. Countless studies are built on the basic observation that telling subjects where the visual stimulus will appear leads to better and faster performance compared to when subjects are obliged to spread their attention across multiple locations. But which brain areas are responsible for these behavioral effects? Despite the many decades of studies that use this basic method to investigate the neural correlates of attention, there is no direct evidence that activity in any brain region is necessary to obtain the behavioral benefits of spatial cues. A study we published this past year in PNAS provides the first clear answer to this question. Using a combination of visual psychophysics and pharmacologic manipulation in monkeys, we showed that suppressing neuronal activity in the superior colliculus eliminates the behavioral benefits of spatial cues. This demonstrates that midbrain activity is necessary for this defining aspect of selective attention, and that cortical activity alone is not sufficient. 1b) Color-change detection activity in the primate superior colliculus To explore how midbrain and cortical signals interact, we recorded SC neuronal activity during an attention task using color, a visual feature dimension not traditionally associated with the SC. Using this color-based spatial attention task, we found substantial cue-related modulation in all categories of visually responsive neurons in the intermediate layers of the SC. Notably, near-threshold changes in color saturation both increases and decreases evoked phasic bursts of activity with magnitudes as large as those evoked by stimulus onset. This change-detection activity had two distinctive features: activity for hits was larger than for misses, the timing of change-detection activity accounted for 67% of joystick release latency. This work, published this past year in eNeuro, demonstrates that SC activity denotes the behavioral relevance of the stimulus regardless of feature dimension, and that phasic event-related SC activity is suitable to guide the selection of manual responses as well as saccadic eye movements. 1c) Covert selective attention and the primate basal ganglia The basal ganglia are known to be important for action selection, but we have proposed that they also play a central role in the control of selective attention. We have now completed a test of this idea by recording neuronal activity in the caudate nucleus while animals performed a covert spatial attention task. We found that caudate neurons strongly select the spatial location of the relevant stimulus throughout the task even in the absence of any overt action. This spatially selective activity was dependent on task and visual conditions, and could be dissociated from goal-directed actions. Caudate activity was also sufficient to correctly identify every epoch in the covert attention task. These results, which are now submitted for publication, provide a novel perspective on mechanisms of attention by demonstrating that the basal ganglia are involved in spatial selection and tracking of behavioral states even in the absence of overt orienting movements. 1d) Comparing frontal eye fields and SC contributions to covert spatial attention The roles of the frontal eye fields (FEF) and superior colliculus (SC) in spatial selective attention have been studied extensively but separately their causal contributions have not been directly compared. Reversible inactivation is an established method for testing causality, but comparing results between FEF and SC is complicated by the fact that the two brain regions differ in size and morphology. In work that is being prepared for publication, we exploited the fact that reversible inactivation of FEF and SC also changes the metrics of saccadic eye movements, providing an independent benchmark for the effective strength of the causal manipulation. Using monkeys trained to covertly perform a visual motion-change detection task, we found that inactivation of either FEF or SC could cause deficits in attention-task performance. However, SC-induced attention deficits were found with saccade changes half the size needed to get FEF-induced attention deficits, indicating that attention-task performance was much more sensitive to disruption of SC activity. 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) Activation of striatal neurons causes a perceptual decision bias The availability of genetic tools in mice make it possible to perform specific tests of our ideas about the role of the basal ganglia in selective attention. In work that is now submitted for publication, we tested the causal role of the basal ganglia by manipulating neuronal activity in the dorsal striatum of mice performing a visual orientation-change detection task. Brief unilateral optogenetic stimulation caused large changes in task performance, shifting psychometric curves upward by increasing the probability of yes responses with only minor changes in sensitivity. For the direct pathway, these effects were significantly larger when the visual event was expected in the contralateral visual field, demonstrating a lateralized bias in evaluating sensory inputs rather than a generalized increase in action initiation. For both direct and indirect pathways, the effects were specific to task epochs in which choice-relevant visual stimuli were present. These results indicate that the causal link between striatal activity and decision-making includes an additive perceptual bias in favor of expected or valued visual events.
| Bollimunta, Anil; Bogadhi, Amarender R; Krauzlis, Richard J (2018) Comparing frontal eye field and superior colliculus contributions to covert spatial attention. Nat Commun 9:3553 |
| Wang, Lupeng; Rangarajan, Krsna V; Gerfen, Charles R et al. (2018) Activation of Striatal Neurons Causes a Perceptual Decision Bias during Visual Change Detection in Mice. Neuron 97:1369-1381.e5 |
| Wang, Lupeng; Krauzlis, Richard J (2018) Visual Selective Attention in Mice. Curr Biol 28:676-685.e4 |
| Krauzlis, Richard J; Bogadhi, Amarender R; Herman, James P et al. (2018) Selective attention without a neocortex. Cortex 102:161-175 |
| Krauzlis, Richard J; Goffart, Laurent; Hafed, Ziad M (2017) Neuronal control of fixation and fixational eye movements. Philos Trans R Soc Lond B Biol Sci 372: |
| Lovejoy, Lee P; Krauzlis, Richard J (2017) Changes in perceptual sensitivity related to spatial cues depends on subcortical activity. Proc Natl Acad Sci U S A 114:6122-6126 |
| Herman, James P; Krauzlis, Richard J (2017) Color-Change Detection Activity in the Primate Superior Colliculus. eNeuro 4: |
| Rucci, Michele; McGraw, Paul V; Krauzlis, Richard J (2016) Fixational eye movements and perception. Vision Res 118:1-4 |
| Herman, James P; Bogadhi, Amarender R; Krauzlis, Richard J (2015) Effects of spatial cues on color-change detection in humans. J Vis 15:3 |
| Perrone, John A; Krauzlis, Richard J (2014) Simulating component-to-pattern dynamic effects with a computer model of middle temporal pattern neurons. J Vis 14: |
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