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Face processing is fundamental to primates and has been extensively studied in higher-order visual cortex. Here, we report that visual neurons in the midbrain superior colliculus (SC) of macaque monkeys display a preference for images of faces. This preference emerges within 40 ms of stimulus onset-well before "face patches" in visual cortex-and, at the population level, can be used to distinguish faces from other visual objects with accuracies of ∼80%. This short-latency face preference in SC depends on signals routed through early visual cortex because inactivating the lateral geniculate nucleus, the key relay from retina to cortex, virtually eliminates visual responses in SC, including face-related activity. These results reveal an unexpected circuit in the primate visual system for rapidly detecting faces in the periphery, complementing the higher-order areas needed for recognizing individual faces.

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Introduction: If neuroscientists were asked which brain area is responsible for object recognition in primates, most would probably answer infero-temporal (IT) cortex. While IT is likely responsible for fine discriminations, and it is accordingly dominated by foveal visual inputs, there is more to object recognition than fine discrimination. Importantly, foveation of an object of interest usually requires recognizing, with reasonable confidence, its presence in the periphery. Arguably, IT plays a secondary role in such peripheral recognition, and other visual areas might instead be more critical. Methods: To investigate how signals carried by early visual processing areas (such as LGN and V1) could be used for object recognition in the periphery, we focused here on the task of distinguishing faces from non-faces. We tested how sensitive various models were to nuisance parameters, such as changes in scale and orientation of the image, and the type of image background. Results: We found that a model of V1 simple or complex cells could provide quite reliable information, resulting in performance better than 80% in realistic scenarios. An LGN model performed considerably worse. Discussion: Because peripheral recognition is both crucial to enable fine recognition (by bringing an object of interest on the fovea), and probably sufficient to account for a considerable fraction of our daily recognition-guided behavior, we think that the current focus on area IT and foveal processing is too narrow. We propose that rather than a hierarchical system with IT-like properties as its primary aim, object recognition should be seen as a parallel process, with high-accuracy foveal modules operating in parallel with lower-accuracy and faster modules that can operate across the visual field.

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The locus coeruleus is the seat of a brain-wide neuromodulatory circuit. Using optogenetic and electrophysiological tools to selectively interrogate noradrenergic neurons in non-human primates, Ghosh and Maunsell show how locus coeruleus neurons contribute to a specific aspect of visual attention.

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Face processing is fundamental to primates and has been extensively studied in higher-order visual cortex. Here we report that visual neurons in the midbrain superior colliculus (SC) display a preference for faces, that the preference emerges within 50ms of stimulus onset - well before "face patches" in visual cortex - and that this activity can distinguish faces from other visual objects with accuracies of ~80%. This short-latency preference in SC depends on signals routed through early visual cortex, because inactivating the lateral geniculate nucleus, the key relay from retina to cortex, virtually eliminates visual responses in SC, including face-related activity. These results reveal an unexpected circuit in the primate visual system for rapidly detecting faces in the periphery, complementing the higher-order areas needed for recognizing individual faces.

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Correlated variability in neuronal activity (spike count correlations, rSC) can constrain how information is read out from populations of neurons. Traditionally, rSC is reported as a single value summarizing a brain area. However, single values, like summary statistics, stand to obscure underlying features of the constituent elements. We predict that in brain areas containing distinct neuronal subpopulations, different subpopulations will exhibit distinct levels of rSC that are not captured by the population rSC. We tested this idea in macaque superior colliculus (SC), a structure containing several functional classes (i.e., subpopulations) of neurons. We found that during saccade tasks, different functional classes exhibited differing degrees of rSC. "Delay class" neurons displayed the highest rSC, especially during saccades that relied on working memory. Such dependence of rSC on functional class and cognitive demand underscores the importance of taking functional subpopulations into account when attempting to model or infer population coding principles.

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We define attention as "the set of evolved brain processes that leads to adaptive and effective behavioral selection." Our emphasis is on understanding the biological and neural mechanisms that make the behavioral properties of attention possible. Although much has been learned about the functional operation of attention by postulating and testing different aspects of attention, our view is that the distinctions most frequently relied upon are much less useful for identifying the detailed biological mechanisms and brain circuits. Instead, we adopt an evolutionary perspective that, while speculative, generates a different set of guiding principles for understanding the form and function of attention. We then provide a thought experiment, introducing a device that we intend to serve as an intuition pump for thinking about how the brain processes for attention might be organized, and that illustrates the features of the biological processes that might ultimately answer the question. This article is categorized under: Cognitive Biology > Evolutionary Roots of Cognition Psychology > Attention Philosophy > Psychological Capacities.

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Recent evidence suggests that microsaccades are causally linked to the attention-related modulation of neurons-specifically, that microsaccades toward the attended location are required for the subsequent changes in firing rate. These findings have raised questions about whether attention-related modulation is due to different states of attention as traditionally assumed or might instead be a secondary effect of microsaccades. Here, in two rhesus macaques, we tested the relationship between microsaccades and attention-related modulation in the superior colliculus (SC), a brain structure crucial for allocating attention. We found that attention-related modulation emerged even in the absence of microsaccades, was already present prior to microsaccades toward the cued stimulus, and persisted through the suppression of activity that accompanied all microsaccades. Nonetheless, consistent with previous findings, we also found significant attention-related modulation when microsaccades were directed toward, rather than away from, the cued location. Thus, despite the clear links between microsaccades and attention, microsaccades are not necessary for attention-related modulation, at least not in the SC. They do, however, provide an additional marker for the state of attention, especially at times when attention is shifting from one location to another.

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Covert visual attention is accomplished by a cascade of mechanisms distributed across multiple brain regions. Visual cortex is associated with enhanced representations of relevant stimulus features, whereas the contributions of subcortical circuits are less well understood but have been associated with selection of relevant spatial locations and suppression of distracting stimuli. As a step toward understanding these subcortical circuits, here we identified how neuronal activity in the intermediate layers of the superior colliculus (SC) of head-fixed mice is modulated during covert visual attention. We found that spatial cues modulated both firing rate and spike-count correlations. Crucially, the cue-related modulation in firing rate was due to enhancement of activity at the cued spatial location rather than suppression at the uncued location, indicating that SC neurons in our task were modulated by an excitatory or disinhibitory circuit mechanism focused on the relevant location, rather than broad inhibition of irrelevant locations. This modulation improved the neuronal discriminability of visual-change-evoked activity, but only when assessed for neuronal activity between the contralateral and ipsilateral SC. Together, our findings indicate that neurons in the mouse SC can contribute to covert visual selective attention by biasing processing in favor of locations expected to contain task-relevant information.

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In primates, stimulus-driven changes in visual attention can facilitate or hinder perceptual performance, depending on the location and timing of the stimulus event. Mice have emerged as a powerful model for studying visual circuits and behavior; however, it is unclear whether mice show similar interactions between stimulus events and visual attention during perceptual decisions. To investigate this, we trained head-fixed mice to detect a near-threshold change in visual orientation and tested how performance was altered by task-irrelevant stimuli that occurred at different times and locations with respect to the orientation change. We found that task-irrelevant stimuli strongly affected mouse performance. Specifically, stimulus-driven attention in mice followed a similar time course as that in other species: The decreases in reaction times fully emerged between 250 and 400 ms after the stimulus event, and detection accuracy was not affected. However, the effects of stimulus-driven attention on behavior in mice were insensitive to stimulus-event location, an aspect different from what is known in primates. In contrast, reaction times in mice were reduced at longer delays after the task-irrelevant stimulus event regardless of its spatial congruence to the target. These results highlight the strengths and limitations of using mice as a model for studying higher-order visual functions.

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Brain perturbation studies allow detailed causal inferences of behavioral and neural processes. Because the combination of brain perturbation methods and neural measurement techniques is inherently challenging, research in humans has predominantly focused on non-invasive, indirect brain perturbations, or neurological lesion studies. Non-human primates have been indispensable as a neurobiological system that is highly similar to humans while simultaneously being more experimentally tractable, allowing visualization of the functional and structural impact of systematic brain perturbation. This review considers the state of the art in non-human primate brain perturbation with a focus on approaches that can be combined with neuroimaging. We consider both non-reversible (lesions) and reversible or temporary perturbations such as electrical, pharmacological, optical, optogenetic, chemogenetic, pathway-selective, and ultrasound based interference methods. Method-specific considerations from the research and development community are offered to facilitate research in this field and support further innovations. We conclude by identifying novel avenues for further research and innovation and by highlighting the clinical translational potential of the methods.

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Recent fMRI experiments identified an attention-related region in the macaque temporal cortex, here called the floor of the superior temporal sulcus (fSTS), as the primary cortical target of superior colliculus (SC) activity. However, it remains unclear which aspects of attention are processed by fSTS neurons and how or why these might depend on SC activity. Here, we show that SC inactivation decreases attentional modulations in fSTS neurons by increasing their activity for ignored stimuli in addition to decreasing their activity for attended stimuli. Neurons in the fSTS also exhibit event-related activity during attention tasks linked to detection performance, and this link is eliminated during SC inactivation. Finally, fSTS neurons respond selectively to particular visual objects, and this selectivity is reduced markedly during SC inactivation. These diverse, high-level properties of fSTS neurons all involve visual signals that carry behavioral relevance. Their dependence on SC activity could reflect a circuit that prioritizes cortical processing of events detected subcortically.

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Visual information is represented across multiple areas in the mouse visual cortex. A new study has revealed that some higher visual areas are important for seeing even simple visual features, whereas other areas have more complex effects on visual decisions.

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Recent work has implicated the primate basal ganglia in visual perception and attention, in addition to their traditional role in motor control. The basal ganglia, especially the caudate nucleus 'head' (CDh) of the striatum, receive indirect anatomical connections from the superior colliculus (SC), a midbrain structure that is known to play a crucial role in the control of visual attention. To test the possible functional relationship between these subcortical structures, we recorded CDh neuronal activity of macaque monkeys before and during unilateral SC inactivation in a spatial attention task. SC inactivation significantly altered the attention-related modulation of CDh neurons and strongly impaired the classification of task-epochs based on CDh activity. Only inactivation of SC on the same side of the brain as recorded CDh neurons, not the opposite side, had these effects. These results demonstrate a novel interaction between SC activity and attention-related visual processing in the basal ganglia.

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The basal ganglia are implicated in a range of perceptual functions [1], in addition to their well-known role in the regulation of movement [2]. One unifying explanation for these diverse roles is that the basal ganglia control the level of commitment to particular motor or cognitive outcomes based on the behavioral context [3, 4]. If this explanation is applicable to the allocation of visual spatial attention, then the involvement of basal ganglia circuits should incorporate the subject's expectations about the spatial location of upcoming events as well as the routing of visual signals that guide the response. From the viewpoint of signal detection theory, these changes in the level of commitment might correspond to shifts in the subject's decision criterion, one of two distinct components recently ascribed to visual selective attention [5]. We tested this idea using unilateral optogenetic activation of neurons in the dorsal striatum of mice during a visual spatial attention task [6], taking advantage of the ability to specifically target medium spiny neurons in the "direct" pathway associated with promoting responses [7, 8]. By comparing results across attention task conditions, we found that direct-pathway activation caused changes in performance determined by the spatial probability and location of the visual event. Moreover, across conditions with identical visual stimulation, activation shifted the decision criterion selectively when attention was directed to the contralateral visual field. These results demonstrate that activity through the basal ganglia may play an important and distinct role among the multifarious mechanisms that accomplish visual spatial attention.

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The superior colliculus (SC) is arguably the most important visual structure in the mouse brain and is well known for its involvement in innate responses to visual threats and prey items. In other species, the SC plays a central role in voluntary as well as innate visual functions, including crucial contributions to selective attention and perceptual decision-making. In the mouse, the possible role of the SC in voluntary visual choice behaviors has not been established. Here, we demonstrate that the mouse SC of both sexes plays a causal role in visual perceptual decision-making by transiently inhibiting SC activity during an orientation change detection task. First, unilateral SC inhibition-induced spatially specific deficits in detection. Hit rates were reduced, and reaction times increased for orientation changes in the contralateral but not ipsilateral visual field. Second, the deficits caused by SC inhibition were specific to a temporal epoch coincident with early visual burst responses in the SC. Inhibiting SC during this 100-ms period caused a contralateral detection deficit, whereas inhibition immediately before or after did not. Third, SC inhibition reduced visual detection sensitivity. Psychometric analysis revealed that inhibiting SC visual activity significantly increased detection thresholds for contralateral orientation changes. In addition, effects on detection thresholds and lapse rates caused by SC inhibition were larger in the presence of a competing visual stimulus, indicating a role for the mouse SC in visual target selection. Together, our results demonstrate that the mouse SC is necessary for the normal performance of voluntary visual choice behaviors.SIGNIFICANCE STATEMENT The mouse superior colliculus (SC) has become a popular model for studying the circuit organization and development of the visual system. Although the SC is a fundamental component of the visual pathways in mice, its role in visual perceptual decision-making is not clear. By investigating how temporally precise SC inhibition influenced behavioral performance during a visually guided orientation change detection task, we identified a 100-ms temporal epoch of SC visual activity that is crucial for the ability of mice to detect behaviorally relevant visual changes. In addition, we found that SC inhibition also caused deficits in visual target selection. Thus, our findings highlight the importance of the SC for visual perceptual choice behavior in the mouse.

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We describe a set of protocols for doing visual psychophysical experiments in head-fixed mice. The goal of this approach was to conduct in mice the same type of precise and well-controlled tests of visual perception and decision making as is commonly done in primates. For example, these experimental protocols were the basis for our demonstration that mice are capable of visual selective attention in paradigms adapted from classic attention cueing paradigms in primates. Basic Protocol 1 describes how to construct the experimental apparatus, including the removable wheel assembly on which the mice run during the visual tasks, the lick spout used to deliver rewards and detect licks, and the behavioral box that places these components together with the visual displays. We also describe the functions of the computerized control system and the design of the customized head fixture. Basic Protocol 2 describes the preparation of mice for the experiments, including the detailed surgical steps. Basic Protocol 3 describes the transition to a food schedule for the mice and how to operate the experimental apparatus. Basic Protocol 4 outlines the logic of the task design and the steps necessary for training the mice. Finally, Basic Protocol 5 describes how to obtain and analyze the psychometric data. Our methods include several distinctive features, including a custom quick-release method for holding the head and specific strategies for training mice over multiple weeks. Published 2020. U.S. Government. Basic Protocol 1: Experimental apparatus Basic Protocol 2: Head fixture surgery Basic Protocol 3: General operation of the experimental apparatus Basic Protocol 4: Behavioral task design and training Basic Protocol 5: Psychometric data collection and analysis.

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How sensory signals are processed by the visual cortex is not fixed but changes depending on our spatial goals and whether or not we are moving. New research helps explain why these two effects do not always work well together.

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Spatial neglect is a common clinical syndrome involving disruption of the brain's attention-related circuitry, including the dorsocaudal temporal cortex. In macaques, the attention deficits associated with neglect can be readily modeled, but the absence of evidence for temporal cortex involvement has suggested a fundamental difference from humans. To map the neurological expression of neglect-like attention deficits in macaques, we measured attention-related fMRI activity across the cerebral cortex during experimental induction of neglect through reversible inactivation of the superior colliculus and frontal eye fields. During inactivation, monkeys exhibited hallmark attentional deficits of neglect in tasks using either motion or non-motion stimuli. The behavioral deficits were accompanied by marked reductions in fMRI attentional modulation that were strongest in a small region on the floor of the superior temporal sulcus; smaller reductions were also found in frontal eye fields and dorsal parietal cortex. Notably, direct inactivation of the mid-superior temporal sulcus (STS) cortical region identified by fMRI caused similar neglect-like spatial attention deficits. These results identify a putative macaque homolog to temporal cortex structures known to play a central role in human neglect.

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The original and corrected figures are shown in the accompanying Publisher Correction.