[Show abstract][Hide abstract] ABSTRACT: Attention is commonly thought to be important for managing the limited resources available in sensory areas of the neocortex. Here we present an alternative view that attention arises as a byproduct of circuits centered on the basal ganglia involved in value-based decision making. The central idea is that decision making depends on properly estimating the current state of the animal and its environment and that the weighted inputs to the currently prevailing estimate give rise to the filter-like properties of attention. After outlining this new framework, we describe findings from physiological, anatomical, computational, and clinical work that support this point of view. We conclude that the brain mechanisms responsible for attention employ a conserved circuit motif that predates the emergence of the neocortex.
Trends in Cognitive Sciences 06/2014; · 16.01 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: 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.
Journal of Vision 01/2014; 14(1). · 2.48 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: 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.
Proceedings of the National Academy of Sciences 06/2013; · 9.81 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: 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. Expected final online publication date for the Annual Review of Neuroscience Volume 36 is July 08, 2013. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.
Annual Review of Neuroscience 05/2013; · 20.61 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: 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.
European Journal of Neuroscience 01/2013; · 3.75 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Visual attention is commonly studied by using visuo-spatial cues indicating probable locations of a target and assessing the effect of the validity of the cue on perceptual performance and its neural correlates. Here, we adapt a cueing task to measure spatial cueing effects on the decisions of honeybees and compare their behavior to that of humans and monkeys in a similarly structured two-alternative forced-choice perceptual task. Unlike the typical cueing paradigm in which the stimulus strength remains unchanged within a block of trials, for the monkey and human studies we randomized the contrast of the signal to simulate more real world conditions in which the organism is uncertain about the strength of the signal. A Bayesian ideal observer that weights sensory evidence from cued and uncued locations based on the cue validity to maximize overall performance is used as a benchmark of comparison against the three animals and other suboptimal models: probability matching, ignore the cue, always follow the cue, and an additive bias/single decision threshold model. We find that the cueing effect is pervasive across all three species but is smaller in size than that shown by the Bayesian ideal observer. Humans show a larger cueing effect than monkeys and bees show the smallest effect. The cueing effect and overall performance of the honeybees allows rejection of the models in which the bees are ignoring the cue, following the cue and disregarding stimuli to be discriminated, or adopting a probability matching strategy. Stimulus strength uncertainty also reduces the theoretically predicted variation in cueing effect with stimulus strength of an optimal Bayesian observer and diminishes the size of the cueing effect when stimulus strength is low. A more biologically plausible model that includes an additive bias to the sensory response from the cued location, although not mathematically equivalent to the optimal observer for the case stimulus strength uncertainty, can approximate the benefits of the more computationally complex optimal Bayesian model. We discuss the implications of our findings on the field's common conceptualization of covert visual attention in the cueing task and what aspects, if any, might be unique to humans.
[Show abstract][Hide abstract] ABSTRACT: Pursuit and saccades almost always select the same target. Is this the results of a common selection process or does smooth pursuit obligatorily follow the stimulus targeted by saccades? To address this question, we used microstimulation of the primate superior colliculus (SC) to redirect the eyes from a selected pursuit target to a distracter moving in the opposite direction. During each trial, monkeys pursued a horizontally moving array of colored target stimuli. In half of the trials, this target array was accompanied by a distracter array moving horizontally in the opposite direction, offset by the vertical amplitude of the stimulation-evoked saccade. We stimulated the SC during maintained pursuit on half of the trials, and measured pursuit eye velocity during the 50-ms interval immediately following the stimulation-evoked saccade to the distracter array. Saccades evoked by SC stimulation did not alter pursuit target selection. Pursuit velocity on average changed by less than 10% of that expected if the monkey had completely switched targets. Moreover, the same changes in velocity occurred when there was no distracter, indicating that even these small changes in pursuit velocity were a direct effect of the evoked saccade, not partial selection of the distracter. These results show that motor execution of saccades is not sufficient to select a pursuit target, and support the idea that the coordination of pursuit and saccades is accomplished by a shared target selection process.
[Show abstract][Hide abstract] ABSTRACT: 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.
[Show abstract][Hide abstract] ABSTRACT: 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.
Journal of Neuroscience 08/2012; 32(31):10627-36. · 6.91 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The characteristics of microsaccades, or small fixational saccades, and their influence on visual function have been studied extensively. However, the detailed mechanisms for generating these movements are less understood. We recently found that the superior colliculus (SC), a midbrain structure involved in saccade generation, also plays a role in microsaccade generation. Here we compared the dynamics of neuronal activity in the SC associated with microsaccades to those observed in this structure in association with larger voluntary saccades. We found that microsaccade-related activity in the SC is characterized by a gradual increase in firing rate starting ∼100 ms prior to microsaccade onset, a peak of neuronal discharge just after movement onset, and a subsequent gradual decrease in firing rate until ∼100 ms after movement onset. These properties were shared with saccade-related SC neurons, recorded from the same monkeys but preferring larger eye movements, suggesting that at the level of the SC the neuronal control of microsaccades is similar to that for larger voluntary saccades. We also found that neurons exhibiting microsaccade-related activity often also exhibited saccade-related activity for slightly larger movements of similar direction, suggesting a continuity of the spatial representation in the SC, in both amplitude and direction, down to the smallest movements. Our results indicate that the mechanisms controlling microsaccades may be fundamentally the same as those for larger saccades, and thus shed new light on the functional role of these eye movements and their possible influence on sensory and sensory-motor processes.
Journal of Neurophysiology 01/2012; 107(7):1904-16. · 3.30 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Viral vectors are promising tools for the dissection of neural circuits. In principle, they can manipulate neurons at a level of specificity not otherwise achievable. While many studies have used viral vector-based approaches in the rodent brain, only a few have employed this technique in the non-human primate, despite the importance of this animal model for neuroscience research. Here, we report evidence that a viral vector-based approach can be used to manipulate a monkey's behavior in a task. For this purpose, we used the allatostatin receptor/allatostatin (AlstR/AL) system, which has previously been shown to allow inactivation of neurons in vivo. The AlstR was expressed in neurons in monkey V1 by injection of an adeno-associated virus 1 (AAV1) vector. Two monkeys were trained in a detection task, in which they had to make a saccade to a faint peripheral target. Injection of AL caused a retinotopic deficit in the detection task in one monkey. Specifically, the monkey showed marked impairment for detection targets placed at the visual field location represented at the virus injection site, but not for targets shown elsewhere. We confirmed that these deficits indeed were due to the interaction of AlstR and AL by injecting saline, or AL at a V1 location without AlstR expression. Post-mortem histology confirmed AlstR expression in this monkey. We failed to replicate the behavioral results in a second monkey, as AL injection did not impair the second monkey's performance in the detection task. However, post-mortem histology revealed a very low level of AlstR expression in this monkey. Our results demonstrate that viral vector-based approaches can produce effects strong enough to influence a monkey's performance in a behavioral task, supporting the further development of this approach for studying how neuronal circuits control complex behaviors in non-human primates.
[Show abstract][Hide abstract] ABSTRACT: 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.
Journal of Neuroscience 10/2011; 31(43):15219-30. · 6.91 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: 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.
Journal of Neuroscience 06/2011; 31(22):8059-66. · 6.91 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The frontal pursuit area (FPA) lies posterior to the frontal eye fields in the frontal cortex and contains neurons that are directionally selective for pursuit eye movements. Lesions of the FPA (alternately called "FEFsem") cause deficits in pursuit acceleration and velocity, which are largest for movements directed toward the lesioned side. Conversely, stimulation of the FPA evokes pursuit from fixation and increases the gain of the pursuit response. On the basis of these properties, it has been hypothesized that the FPA could underlie the selection of pursuit direction. To test this possibility, we manipulated FPA activity and measured the effect on target selection behavior in rhesus monkeys. First, we unilaterally inactivated the FPA with the GABA agonist muscimol. We then measured the monkeys' performance on a pursuit-choice task. Second, we applied microstimulation unilaterally to the FPA during pursuit initiation while monkeys performed the same pursuit-choice task. Both of these manipulations produced significant effects on pursuit metrics; the inactivation decreased pursuit velocity and acceleration, and microstimulation evoked pursuit directly. Despite these changes, both manipulations failed to significantly alter choice behavior. These results show that FPA activity is not necessary for pursuit target selection.
Journal of Neurophysiology 04/2011; 106(1):347-60. · 3.30 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The frontal pursuit area (FPA) contains neurons that are directionally selective for pursuit eye-movements. We found that FPA neurons discriminate target from distracter too late to account for pursuit directional selection. Rather, the timing of neuronal discrimination is linked to pursuit onset, suggesting a role in motor execution. We also found buildup of activity of FPA neurons prior to pursuit onset that correlated with eye acceleration. These results show that the FPA is unlikely to be involved in selection of initial pursuit direction, but could be involved in motor preparation by increasing pursuit gain prior to pursuit onset.
Vision research 10/2010; 51(8):853-66. · 2.29 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: In addition to its well-known role in the control of saccades, the primate superior colliculus (SC) has been implicated in the processes of target choice for overt orienting movements and for covert spatial attention. We focally inactivated the SC, by muscimol injection, while monkeys selected the target of a smooth pursuit, saccade, or button press response from two competing stimuli. The choice stimuli were placed so that one appeared within and the other appeared outside the affected visual field. SC inactivation biased the subject to choose stimuli out of the affected visual field for all three types of responses, although the effects on target choice were significantly smaller for button presses. Inactivation caused no changes in the selection of single stimuli within or out of the affected visual field, indicating the choice bias was not caused by deficits in response execution. The inactivation-induced bias for smooth pursuit and button press responses indicates SC activity is important for selecting the target, independent of any role in saccade preparation.
Journal of Neurophysiology 09/2010; 104(3):1538-48. · 3.30 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Saccadic suppression, a behavioral phenomenon in which perceptual thresholds are elevated before, during, and after saccadic eye movements, is an important mechanism for maintaining perceptual stability. However, even during fixation, the eyes never remain still, but undergo movements including microsaccades, drift, and tremor. The neural mechanisms for mediating perceptual stability in the face of these "fixational" movements are not fully understood. Here, we investigated one component of such mechanisms: a neural correlate of microsaccadic suppression. We measured the size of short-latency, stimulus-induced visual bursts in superior colliculus neurons of adult, male rhesus macaques. We found that microsaccades caused approximately 30% suppression of the bursts. Suppression started approximately 70 ms before microsaccade onset and ended approximately 70 ms after microsaccade end, a time course similar to behavioral measures of this phenomenon in humans. We also identified a new behavioral effect of microsaccadic suppression on saccadic reaction times, even for continuously presented, suprathreshold visual stimuli. These results provide evidence that the superior colliculus is part of the mechanism for suppressing self-generated visual signals during microsaccades that might otherwise disrupt perceptual stability.
Journal of Neuroscience 07/2010; 30(28):9542-7. · 6.91 Impact Factor