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. Standard models of visual attention emphasize the role of the cortex, but our results indicate that 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) Correlated variability in populations of midbrain neurons constrains how perceptual choices are formed Recent work has demonstrated that noise correlations limit what can be read out from neuronal populations during perceptual choices. The midbrain superior colliculus (SC) participates in covert perceptual choices but the role of correlations in SC neurons has not been examined. We considered how varying degrees of correlation would affect read-out in a simple difference model comparing pooled activity between the right and left SC. We found that in this model positive correlations between right and left SC would facilitate read-out, whereas both negative between-SC correlations and positive within-SC correlations would hinder read-out. We identified specific combinations of between- and within-SC correlation values that best predicted the monkeys behavior, and others that would prevent accurate prediction. We next measured the extracellular activity of left and right SC neurons simultaneously with multi-contact probes while the monkey made covert perceptual choices. The monkeys task was to decide whether a relevant (cued) peripheral stimulus had changed color saturation requiring a joystick release, or if the irrelevant (foil) stimulus had changed, requiring him to maintain joystick hold. In 3 sessions, we recorded the activity of 80 visual-movement neurons, slightly more than 1000 between- and within-pool pairs. On average, SC neurons displayed weak but significantly positive pairwise correlations, which were stronger within (0.09) than between pools (0.047). Our measurements of within- and between-SC correlations nicely matched a subset of the values that allowed our pooling model to best predict monkey performance. Our findings demonstrate that covert perceptual choices can be decoded from the pooled activity of midbrain neurons. The match between our theoretical calculations and empirical measurements suggests that the read-out of covert perceptual choices from the SC depends on the relative levels of activity in the right and left SC. These results are now accepted for publication in Nature Neuroscience. 1b) A novel attention-related area in the macaque temporal cortex We have made significant progress in identifying how the midbrain superior colliculus (SC) interacts with cortical attention mechanisms. Using electrophysiological recordings and pharmacological perturbations, we found a novel attention-related area in the primate temporal cortex that is causally linked to SC, as well as to behavior in an attention task. Two monkeys performed a selective spatial attention task in which patches of motion were presented on either side of a central fixation point. In Attend to motion blocks, monkeys were rewarded for attending to the motion patches and releasing a joystick in response to a change in motion direction. In Ignore motion blocks, reward was delivered for ignoring the change in motion direction and instead, responding to a change in fixation point luminance. During performance in the attention task, we recorded from ensembles of neurons in a region previously identified by fMRI in the fundus of the superior temporal sulcus (aFST/IPa) of two macaques before (n = 244) and during (n = 223) SC inactivation. We made three novel findings. First, neurons in aFST/IPa exhibited significantly higher activity for stimuli in their receptive field during the attend to motion condition compared to the ignore, indicating that this region reflects behavioral manipulations of attention. Second, the attention-related modulation of aFST/IPa neurons was substantially reduced during SC inactivation (61% reduction), demonstrating a causal link between SC activity and attention-related modulation in aFST/IPa. Third, reversible inactivation in area aFST/IPa itself during task performance produced deficits in the monkeys ability to detect changes in either one or both of our task stimuli, establishing a causal role for aFST/IPa in the selective attention task. These results demonstrate a novel attention-related area in the temporal cortex (aFST/IPa). The causal contributions of aFST/IPa to attention task performance and its dependence on SC activity indicate that it is a crucial link between the cortical and subcortical networks subserving the process of selective attention. 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) Visual selective attention in mice The discrepancies between the visual and cognitive abilities of primates and mice raise the possibility that mice might not have selective visual attention, at least not in the forms well-known in primates. We recently tested for selective visual attention in mice, using three behavioral paradigms adapted from primate studies of attention. We trained head-fixed mice running on a wheel to detect a threshold-level change in a visual stimulus with distractors, and provided visual spatial cues that indicated the likely location of the relevant visual change. Because our mice reported their detection by licking a central spout, and the visual change occurred in either the right or left visual field, we were able to measure lateralized effects on perceptual choice without confounds from biases in motor responses. We found spatially specific changes in perceptual sensitivity, criterion and reaction times. In a Posner-style cueing task, a spatial cue indicated the probable location of the relevant visual event, and we found that valid cues increased response accuracy and shortened reaction times. In a cue versus no-cue task, an informative spatial cue was provided on half the trials, and we found that the spatial cue again increased response accuracy and shortened reaction times, and lowered detection thresholds measured from psychometric curves. In a filter task, the spatial cue indicated the location of the relevant visual event, and we found that mice could be trained to ignore irrelevant but otherwise identical visual events at uncued locations. Together, these results (recently published in Current Biology) demonstrate that mice exhibit visual selective attention, paving the way to use visual paradigms in mice to study the genetic and neuronal circuit mechanisms of selective attention.
| 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 |
| 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 |
| 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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