Stimulus-driven visual attention in mice.

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.

A Causal Role for Mouse Superior Colliculus in Visual Perceptual Decision-Making.

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.

Combining brain perturbation and neuroimaging in non-human primates.

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.

Superior colliculus and visual spatial attention.

The superior colliculus (SC) has long been known to be part of the network of brain areas involved in spatial attention, but recent findings have dramatically refined our understanding of its functional role. The SC both implements the motor consequences of attention and plays a crucial role in the process of target selection that precedes movement. Moreover, even in the absence of overt orienting movements, SC activity is related to shifts of covert attention and is necessary for the normal control of spatial attention during perceptual judgments. The neuronal circuits that link the SC to spatial attention may include attention-related areas of the cerebral cortex, but recent results show that the SC's contribution involves mechanisms that operate independently of the established signatures of attention in visual cortex. These findings raise new issues and suggest novel possibilities for understanding the brain mechanisms that enable spatial attention.

Covert spatial selection in primate basal ganglia.

The basal ganglia are important for action selection. They are also implicated in perceptual and cognitive functions that seem far removed from motor control. Here, we tested whether the role of the basal ganglia in selection extends to nonmotor aspects of behavior 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 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.

Changes in perceptual sensitivity related to spatial cues depends on subcortical activity.

Spatial cues allow animals to selectively attend to relevant visual stimuli while ignoring distracters. This process depends on a distributed neuronal network, and an important current challenge is to understand the functional contributions made by individual brain regions within this network and how these contributions interact. Recent findings point to a possible anatomical segregation, with cortical and subcortical brain regions contributing to different functional components of selective attention. Cortical areas, especially visual cortex, may be responsible for implementing changes in perceptual sensitivity by changing the signal-to-noise ratio, whereas other regions, such as the superior colliculus, may be involved in processes that influence selection between competing stimuli without regulating perceptual sensitivity. Such a segregation of function would predict that when activity in the superior colliculus is suppressed by reversible inactivation, animals should still show changes in perceptual sensitivity mediated by the intact cortical circuits. Contrary to this prediction, here we report that inactivation of the primate superior colliculus eliminates the changes in perceptual sensitivity made possible by spatial cues. These findings demonstrate changes in perceptual sensitivity depend not only on neuronal activity in cortex but also require interaction with signals from the superior colliculus.

Attention deficits without cortical neuronal deficits.

The ability to process relevant stimuli selectively is a fundamental function of the primate visual system. The best-understood correlate of this function is the enhanced response of neurons in the visual cortex to attended stimuli. However, recent results show that the superior colliculus (SC), a midbrain structure, also has a crucial role in visual attention. It has been assumed that the SC acts through the same well-known mechanisms in the visual cortex. Here we tested this hypothesis by transiently inactivating the SC during a motion-change-detection task and measuring responses in two visual cortical areas. We found that despite large deficits in visual attention, the enhanced responses of neurons in the visual cortex to attended stimuli were unchanged. These results show that the SC contributes to visual attention through mechanisms that are independent of the classic effects in the visual cortex, demonstrating that other processes must have key roles in visual attention.

Learning where to look for a hidden target.

Survival depends on successfully foraging for food, for which evolution has selected diverse behaviors in different species. Humans forage not only for food, but also for information. We decide where to look over 170,000 times per day, approximately three times per wakeful second. The frequency of these saccadic eye movements belies the complexity underlying each individual choice. Experience factors into the choice of where to look and can be invoked to rapidly redirect gaze in a context and task-appropriate manner. However, remarkably little is known about how individuals learn to direct their gaze given the current context and task. We designed a task in which participants search a novel scene for a target whose location was drawn stochastically on each trial from a fixed prior distribution. The target was invisible on a blank screen, and the participants were rewarded when they fixated the hidden target location. In just a few trials, participants rapidly found the hidden targets by looking near previously rewarded locations and avoiding previously unrewarded locations. Learning trajectories were well characterized by a simple reinforcement-learning (RL) model that maintained and continually updated a reward map of locations. The RL model made further predictions concerning sensitivity to recent experience that were confirmed by the data. The asymptotic performance of both the participants and the RL model approached optimal performance characterized by an ideal-observer theory. These two complementary levels of explanation show how experience in a novel environment drives visual search in humans and may extend to other forms of search such as animal foraging.

Effects of spatial cues on color-change detection in humans.

Studies of covert spatial attention have largely used motion, orientation, and contrast stimuli as these features are fundamental components of vision. The feature dimension of color is also fundamental to visual perception, particularly for catarrhine primates, and yet very little is known about the effects of spatial attention on color perception. Here we present results using novel dynamic color stimuli in both discrimination and color-change detection tasks. We find that our stimuli yield comparable discrimination thresholds to those obtained with static stimuli. Further, we find that an informative spatial cue improves performance and speeds response time in a color-change detection task compared with an uncued condition, similar to what has been demonstrated for motion, orientation, and contrast stimuli. Our results demonstrate the use of dynamic color stimuli for an established psychophysical task and show that color stimuli are well suited to the study of spatial attention.

Simulating component-to-pattern dynamic effects with a computer model of middle temporal pattern neurons.

Some primate motion-sensitive middle temporal (MT) neurons respond best to motion orthogonal to a contour's orientation (component types) whereas another class (pattern type) responds maximally to the overall pattern motion. We have previously developed a model of the pattern-type neurons using integration of the activity generated in speed- and direction-tuned subunits. However, a number of other models have also been able to replicate MT neuron pattern-like behavior using a diverse range of mechanisms. This basic property does not really challenge or help discriminate between the different model types. There exist two sets of findings that we believe provide a better yardstick against which to assess MT pattern models. Some MT neurons have been shown to change from component to pattern behavior over brief time intervals. MT neurons have also been observed to switch from component- to pattern-like behavior when the intensity of the intersections in a plaid pattern stimulus changes. These properties suggest more complex time- and contrast-sensitive internal mechanisms underlying pattern motion extraction, which provide a real challenge for modelers. We have now replicated these two component-to-pattern effects using our MT pattern model. It incorporates two types of V1 neurons (sustained and transient), and these have slightly different time delays; this initially favors the component response, thus mimicking the temporal effects. We also discovered that some plaid stimuli contain a contrast asymmetry that depends on the plaid direction and the intensity of the intersections. This causes the model MT pattern units to act as component units.

Short-latency preference for faces in primate superior colliculus depends on visual cortex.

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.

Attention: The blue spot reveals one of its secrets.

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.

Visual fixation as equilibrium: evidence from superior colliculus inactivation.

During visual fixation, the image of an object is maintained within the fovea. Previous studies have shown that such maintenance involves the deep superior colliculus (dSC). However, the mechanisms by which the dSC supports visual fixation remain controversial. According to one view, activity in the rostral dSC maintains gaze direction by preventing neurons in the caudal dSC from issuing saccade commands. An alternative hypothesis proposes that gaze direction is achieved through equilibrium of target position signals originating from the two dSCs. Here, we show in monkeys that artificially reducing activity in the rostral half of one dSC results in a biased estimate of target position during fixation, consistent with the second hypothesis, rather than an inability to maintain gaze fixation as predicted by the first hypothesis. After injection of muscimol at rostral sites in the dSC, fixation became more stable since microsaccade rate was reduced rather than increased. Moreover, the scatter of eye positions was offset relative to preinactivation baselines. The magnitude and the direction of the offsets depended on both the target size and the injected site in the collicular map. Other oculomotor parameters, such as the accuracy of saccades to peripheral targets and the amplitude and velocity of fixational saccades, were largely unaffected. These results suggest that the rostral half of the dSC supports visual fixation through a distributed representation of behaviorally relevant target position signals. The inactivation-induced fixation offset establishes the foveal visual stimulation that is required to restore the balance of activity between the two dSCs.

Superior colliculus inactivation alters the relationship between covert visual attention and microsaccades.

Microsaccades are tiny saccades that occur during gaze fixation. Whereas these movements have traditionally been viewed as random, it was recently discovered that microsaccade directions can be significantly biased by covertly attended visual stimuli. The detailed mechanisms mediating such a bias are neither known nor immediately obvious, especially because the amplitudes of the movements influenced by attentional cueing could be up to two orders of magnitude smaller than the eccentricity of the attended location. Here, we tested whether activity in the peripheral superior colliculus (SC) is necessary for this correlation between attentional cueing and microsaccades. We reversibly and focally inactivated SC neurons representing peripheral regions of visual space while rhesus monkeys performed a demanding covert visual attention task. The normal bias of microsaccade directions observed in each monkey before SC inactivation was eliminated when a cue was placed in the visual region affected by the inactivation; microsaccades were, instead, biased away from the affected visual space. When the cue was placed at another location unaffected by SC inactivation, the baseline cue-induced bias of microsaccade directions remained mostly intact, because the cue was in unaffected visual space, and any remaining changes were again explained by a repulsion of microsaccades away from the inactivated region. Our results indicate that peripheral SC activity is required for the link between microsaccades and the cueing of covert visual attention, and that it could do so by altering the probability of triggering microsaccades without necessarily affecting the motor generation of these movements.

What is attention?

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.

Correlated variability in primate superior colliculus depends on functional class.

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.

Short-latency preference for faces in the primate superior colliculus.

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.

Superior colliculus inactivation alters the weighted integration of visual stimuli.

The primate superior colliculus (SC) is important for the winner-take-all selection of targets for orienting movements. Such selection takes time, however, and the earliest motor responses typically are guided by a weighted vector average of the visual stimuli, before the winner-take-all selection of a single target. We tested whether SC activity plays a role in this initial stage of orienting by inactivating the SC in two macaques (Macaca mulatta) with local muscimol injections. After SC inactivation, initial orienting responses still followed a vector average, but the contribution of the visual stimulus inside the affected field was decreased, and the contribution of the stimulus outside the affected field was increased. These results demonstrate that the SC plays an important role in the weighted integration of visual signals for orienting, in addition to its role in the winner-take-all selection of the target.

Modulation of microsaccades in monkey during a covert visual attention task.

The use of awake, fixating monkeys in neuroscience has allowed significant advances in understanding numerous brain functions. However, fixation is an active process, with the occurrence of incessant eye movements, including rapid ones called microsaccades. Even though microsaccades have been shown to be modulated by stimulus and cognitive processes in humans, it is not known to what extent these results are similar in monkeys or why they occur. Here, we analyzed the stimulus-, context-, and attention-related changes in microsaccades while monkeys performed a challenging visual attention task. The distributions of microsaccade times were highly stereotypical across thousands of trials in the task. Moreover, in epochs of the task in which animals anticipated the occurrence of brief stimulus probes, microsaccade frequency decreased to a rate of less than one movement per second even on long multisecond trials. These effects were explained by the observation that microsaccades occurring at the times of the brief probes were sometimes associated with reduced perceptual performance. Microsaccade directions also exhibited temporal modulations related to the attentional demands of the task, like earlier studies in humans, and were more likely to be directed toward an attended location on successfully performed trials than on unsuccessfully completed ones. Our results show that microsaccades in nonhuman primates are correlated with the allocation of stimulus-evoked and sustained covert attention. We hypothesize that involvement of the superior colliculus in microsaccade generation and attentional allocation contributes to these observations. More importantly, our results clarify the potential role of these eye movements in modifying behavior and neural activity.