Introduction Visual attention is crucial for performing many tasks reading, driving, social interactions, etc. Conversely, disruptions of attention (such as ADHD) are extremely common, typically emerging as a neurodevelopmental problem in school children, and often persisting into adulthood. However, the neuronal circuits targeted by current clinical treatments are largely unknown. Our current efforts build on our recent demonstration (Zenon &Krauzlis, 2012) that the control of attention is not limited to the cerebral cortex, as often assumed, but includes the Superior Colliculus (SC), an evolutionarily conserved structure in the midbrain. The key finding was that perturbing activity in the SC does not change the response properties of neurons in visual cortex, even though this manipulation causes major deficits in visual attention. This dissociation between behavioral deficits and response properties in visual cortex shows that the SC acts through circuits downstream from the well-known sites for attention in visual cortex. We are now working to identify which other brain regions are involved, with the long-term goal of identifying the detailed neuronal circuit so that more specific therapeutic interventions can be developed. 1) Role of subcortical neuronal circuits in 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) Developing an alternate model of visual attention During the past year, we developed and presented and alternate framework that explains how subcortical circuits might control visual attention. The central idea in this new framework is that the properties of attention arise as a byproduct of circuits involved in value-based decision-making. Drawing on results from physiological, anatomical, computational and clinical work, we make the argument that this mechanism involves an evolutionarily conserved circuit motif consisting of the superior colliculus, thalamus and basal ganglia. This novel viewpoint emphasizes the important relationship between visual attention and learning, which has implications for possible behavioral therapies. This work was recently published in Trends in Cognitive Sciences. 1b) Using fMRI to identify the complete network of areas involved in attention To obtain an objective measure of which brain regions are implicated in the control of visual attention, we are using fMRI in nonhuman primates to identify the complete network of cortical and subcortical areas involved in the allocation of attention during our attention task. Dr. Bogadhi has now obtained an extensive set of BOLD data during our visual attention task, as well as during control blocks, in one monkey. His results show activation in the cortical areas you might have expected since the task involves attention to visual motion, he has found activation in portions of the visual cortex dedicated to processing visual motion signals, but he also found BOLD activation in several subcortical brain regions, including the superior colliculus, portions of the thalamus, and regions with the striatum (caudate and putamen) of the basal ganglia. These findings are consistent with our viewpoint that subcortical circuits play an important role in the control of visual attention, and will be presented at the upcoming Society for Neuroscience meeting. We are also planning additional tests of our working framework, including collecting fMRI data during reversible inactivation of the superior colliculus. 1c) Testing how the striatum contributes to attention As a direct test of our idea that subcortical pathways through the basal ganglia are important for visual attention, we have been studying the role of the caudate nucleus (one of the input nuclei for the basal ganglia) during our visual attention ask. The caudate nucleus is onee of the subcortical structure that we have identified in our fMRI results, as well as a structure we identified as a potential target based on neuroanatomy and physiology. Dr. Arcizet has been conducting these difficult recordings over the past year, and has found that caudate neurons are modulated by several factors during the attention task. For many caudate neurons, activity depends on the spatial location of attention and also the choice made by the monkey. Future experiments will confirm these results in additional animals, and test whether pharmacological manipulation of activity in the caudate causes changes in behavioral performance. These results will be presented at the upcoming Society for Neuroscience meeting, and a preliminary report was made at the 2014 Vision Sciences Society meeting. 1d) Investigating the role of subcortical circuits in attention to other visual features Studies of attention have often used visual motion stimuli, which is both salient and ethologically relevant. However, for primates, color is also an important and relevant stimulus feature, but the mechanisms that accomplish attention to color have not been studied. Moreover, studies of the Superior Colliculus and attention have used visual motion stimuli almost exclusively, leaving open the question of whether the role of the SC in attention generalizes across stimulus features, or might be specialized for moving stimuli. To address these issues, Dr. Herman as been examining the responses of neurons in the SC during a color-change detection task. Surprisingly, even though the SC has often been viewed as color-blind, neurons in the SC exhibit vigorous increases in activity triggered by color changes, and this activity is also predictive of the animals behavioral response. These results support the view that the SC contributes to the processing of any behaviorally relevant visual event, regardless of feature dimension. This work presented as a poster at the 2014 Vision Sciences Society meeting, and will be part of a nanosymposium at the upcoming Society for Neuroscience meeting. 2) Role of subcortical neuronal circuits in visual detection and attention in mice Because the circuits we hypothesize to be important for visual attention are highly conserved across vertebrate species, we think it is sensible to explore these circuits in other animal models. Indeed, given the availability of genetic and molecular tools in mice, other animal models provide opportunities to work out the details of neuronal circuits in ways that are not yet possible in nonhuman primates. 2a) Visual detection and attention behavior in mice Although mice can perform many visually guided tasks, there is a major concern in the field that mice may not be able to perform the same types of challenging tasks that have been used to characterize the properties of the primate visual system, including visual attention. To address this issue, Dr. Wang and I have studied the performance of mice trained to detect the presence of an oriented Gabor patch embedded in masking noise. Our data illustrate that mice can be trained to perform challenging visual tasks similar to those that have been used to study visual-motor function in primates. These results will be presented at the upcoming Society for Neuroscience meeting, and a manuscript is currently in preparation. In the upcoming year, we will move our mouse experiments into a larger space that will accommodate a larger number of experimental setups so that we can train and test a larger number of mice. This expanded capacity will allow us to test performance on tasks that are more nearly identical to those that we use in our nonhuman primate studies, and also begin to train lines of cre-expressing mice that will allow us to target specific populations of neurons, specifically in the striatum of the basal ganglia.
| 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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