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, especially those involved in action selection. We are investigating how these subcortical circuits contribute to visual selection and attention, and how subcortical and cortical circuits interact, 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 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) Detection-related activity in the primate SC and action selection Dr. Herman has now completed a project investigating how the SC contributes to the performance of an attention-to-color task. One of the novel observations he has made is that SC neurons respond vigorously to changes in the saturation of a color stimulus, and that this activity is also predictive of the animals behavioral response. Specifically, the trial-to-trial variability in when SC neurons respond to the color change is predictive of when the monkey will release a joystick to indicate his answer. This result is surprising for several reasons. First, it demonstrates that the SC likely contributes to the detection of any behaviorally relevant visual event, regardless of feature dimension. Second, the SC is well known to be important for the generation of saccadic eye movements, but these results indicate that SC activity is also important for the triggering of the hand movements needed to move the joystick in this task. This indicates that event-detection by the SC plays a more general role in coordinating responses to relevant events in the environment, not restricted to the classic role in orienting movements of the eyes and head. 1b) Investigating the contribution of the striatum to visual attention During the past year, Dr. Arcizet has completed a series of physiology experiments demonstrating that neurons in the caudate nucleus, a major component of the subcortical basal ganglia, are not only involved in action selection but are also important for visual selective attention. Specifically, he has documented cue-related modulation during a covert attention task and response-related activity that depends on the behavioral context. For example, caudate neurons exhibit strong phasic activity when the subject releases a joystick to indicate a change in the attended visual stimulus, but do not change their activity when the joystick is released outside the context of the task. This context-specific activity is consistent with the idea that the caudate nucleus is not only important for action selection, as has long been appreciated, but that it is also important for identifying the behavioral context associated with the action. 1c) Contributions of SC and frontal eye field to covert spatial attention One of the central goals of our work is to understand how cortical and subcortical structures contribute and interact to visual attention. The midbrain SC and the cortical frontal eye fields are both known to contribute to covert spatial attention. However, direct comparison of their contributions to attention by measuring the deficits caused by reversible inactivation is confounded by the differences in the amount of the pharmacological agent required to cause the deficit, and by differences in the size and organization of these two brain areas. During the past year, Dr. Bollimunta has taken advantage of the fact that reversible inactivation also causes changes in metrics of saccadic eye movements. This has allowed him to measure the contribution of SC and FEF to covert spatial attention relative to their contribution to saccades. His results show that the probability of observing a deficit in the attention task during FEF inactivation requires a saccade deficit that was about twice as large as during SC inactivation. Hence, relative to saccades, covert spatial attention appears to be more dependent on activity from the SC than from FEF. 1d) fMRI and visual attention in primates In collaboration with David Leopold in the NIF, we are using fMRI in nonhuman primates to identify the complete network of cortical and subcortical areas involved in the allocation of attention during visual attention tasks. During the past year, Drs. Bogadhi and Bollimunta successfully completed an extensive series of experiments combining reversible SC inactivation during visual attention task performance in the fMRI scanner. These experiments involved upwards of 150 scanning sessions each lasting about 3 hours. In two monkeys, we have now demonstrated a significant drop in the attention-related BOLD modulation in fronto-parietal areas implicated in the control of spatial attention, during the attention deficits caused by SC inactivation. Surprisingly, the biggest reduction in the attention-related BOLD modulation was observed in area FST in the superior temporal sulcus. At the same time, several sub-cortical areas (pulvinar, caudate) showed a significant reduction in attentional modulation on the side of the injection. These results identify area FST as a potentially important node in the cortical and sub-cortical network for the control of spatial attention. Moreover, control experiments demonstrate the role of area FST generalizes across selective attention to different visual features (motion, orientation). 2) Role of subcortical neuronal circuits in visual detection and attention in mice Given current tools, 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) Optogenetic stimulation of striatum in mice during a visual detection task We hypothesized that the striatum, the input nucleus to the basal ganglia, plays a crucial role in identifying the sensory and behavioral context associated with valued actions. This hypothesis predicts that artificial activation of striatal neurons will bias visual detection, and that this effect will depend on the particular behavioral context. In experiments completed this past year, Dr. Wang has now confirmed this prediction. We optogenetically activated specific neuronal populations in the striatum of mice trained to report changes in the orientation of drifting visual gratings embedded against noise background. We found that activation of the striatal direct pathway causes a spatially biased shift in decision criterion during a visual detection task, and that these changes in decision criterion depend on the behavioral context. These results are consistent with our hypothesis about how subcortical circuits contribute to visual attention, and will be presented in a nanosymposium at the upcoming Society for Neuroscience meeting.

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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:
ZĂ©non, Alexandre; Krauzlis, Rich (2014) [Superior colliculus as a subcortical center for visual selection]. Med Sci (Paris) 30:637-43
Krauzlis, Richard J; Bollimunta, Anil; Arcizet, Fabrice et al. (2014) Attention as an effect not a cause. Trends Cogn Sci 18:457-64
Eckstein, Miguel P; Mack, Stephen C; Liston, Dorion B et al. (2013) Rethinking human visual attention: spatial cueing effects and optimality of decisions by honeybees, monkeys and humans. Vision Res 85:5-19
Carrasco, Marisa; Eckstein, Miguel; Krauzlis, Rich et al. (2013) Attentional modulation: target selection, active search and cognitive processing. Vision Res 85:1-4

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