A neural mechanism for terminating decisions.

The brain makes decisions by accumulating evidence until there is enough to stop and choose. Neural mechanisms of evidence accumulation are established in association cortex, but the site and mechanism of termination are unknown. Here, we show that the superior colliculus (SC) plays a causal role in terminating decisions, and we provide evidence for a mechanism by which this occurs. We recorded simultaneously from neurons in the lateral intraparietal area (LIP) and SC while monkeys made perceptual decisions. Despite similar trial-averaged activity, we found distinct single-trial dynamics in the two areas: LIP displayed drift-diffusion dynamics and SC displayed bursting dynamics. We hypothesized that the bursts manifest a threshold mechanism applied to signals represented in LIP to terminate the decision. Consistent with this hypothesis, SC inactivation produced behavioral effects diagnostic of an impaired threshold sensor and prolonged the buildup of activity in LIP. The results reveal the transformation from deliberation to commitment.

Deficits in decision-making induced by parietal cortex inactivation are compensated at two timescales.

Perceptual decisions arise through the transformation of samples of evidence into a commitment to a proposition or plan of action. Such transformation is thought to involve cortical circuits capable of computation over timescales associated with working memory, attention, and planning. Neurons in the lateral intraparietal area (LIP) play a role in these functions, and much of what is known about the neurobiology of decision-making has been influenced by studies of LIP and its network of connections. However, the causal role of LIP remains controversial. In this study, we used pharmacological and chemogenetic methods to inactivate LIP in one brain hemisphere of four rhesus monkeys. This inactivation produced biases in decisions, but the effects dissipated despite persistent neural inactivation, implying compensation by unaffected areas. Compensation occurred rapidly within an experimental session and more gradually across sessions. These findings resolve disparate studies and inform the interpretation of focal perturbations of brain function.

Multiple decisions about one object involve parallel sensory acquisition but time-multiplexed evidence incorporation.

The brain is capable of processing several streams of information that bear on different aspects of the same problem. Here, we address the problem of making two decisions about one object, by studying difficult perceptual decisions about the color and motion of a dynamic random dot display. We find that the accuracy of one decision is unaffected by the difficulty of the other decision. However, the response times reveal that the two decisions do not form simultaneously. We show that both stimulus dimensions are acquired in parallel for the initial ∼0.1 s but are then incorporated serially in time-multiplexed bouts. Thus, there is a bottleneck that precludes updating more than one decision at a time, and a buffer that stores samples of evidence while access to the decision is blocked. We suggest that this bottleneck is responsible for the long timescales of many cognitive operations framed as decisions.

The Segmentation of Proto-Objects in the Monkey Primary Visual Cortex.

During visual perception, the brain enhances the representations of image regions that belong to figures and suppresses those that belong to the background. Natural images contain many regions that initially appear to be part of a figure when analyzed locally (proto-objects) but are actually part of the background if the whole image is considered. These proto-grounds must be correctly assigned to the background to allow correct shape identification and guide behavior. To understand how the brain resolves this conflict between local and global processing, we recorded neuronal activity from the primary visual cortex (V1) of macaque monkeys while they discriminated between n/u shapes that have a central proto-ground region. We studied the fine-grained spatiotemporal profile of neural activity evoked by the n/u shape and found that neural representation of the object proceeded from a coarse-to-fine resolution. Approximately 100 ms after the stimulus onset, the representation of the proto-ground region was enhanced together with the rest of the n/u surface, but after ∼115 ms, the proto-ground was suppressed back to the level of the background. Suppression of the proto-ground was only present in animals that had been trained to perform the shape-discrimination task, and it predicted the choice of the animal on a trial-by-trial basis. Attention enhanced figure-ground modulation, but it had no effect on the strength of proto-ground suppression. The results indicate that the accuracy of scene segmentation is sharpened by a suppressive process that resolves local ambiguities by assigning proto-grounds to the background.

Focal optogenetic suppression in macaque area MT biases direction discrimination and decision confidence, but only transiently.

Insights from causal manipulations of brain activity depend on targeting the spatial and temporal scales most relevant for behavior. Using a sensitive perceptual decision task in monkeys, we examined the effects of rapid, reversible inactivation on a spatial scale previously achieved only with electrical microstimulation. Inactivating groups of similarly tuned neurons in area MT produced systematic effects on choice and confidence. Behavioral effects were attenuated over the course of each session, suggesting compensatory adjustments in the downstream readout of MT over tens of minutes. Compensation also occurred on a sub-second time scale: behavior was largely unaffected when the visual stimulus (and concurrent suppression) lasted longer than 350 ms. These trends were similar for choice and confidence, consistent with the idea of a common mechanism underlying both measures. The findings demonstrate the utility of hyperpolarizing opsins for linking neural population activity at fine spatial and temporal scales to cognitive functions in primates.

The influence of attention and reward on the learning of stimulus-response associations.

We can learn new tasks by listening to a teacher, but we can also learn by trial-and-error. Here, we investigate the factors that determine how participants learn new stimulus-response mappings by trial-and-error. Does learning in human observers comply with reinforcement learning theories, which describe how subjects learn from rewards and punishments? If yes, what is the influence of selective attention in the learning process? We developed a novel redundant-relevant learning paradigm to examine the conjoint influence of attention and reward feedback. We found that subjects only learned stimulus-response mappings for attended shapes, even when unattended shapes were equally informative. Reward magnitude also influenced learning, an effect that was stronger for attended than for non-attended shapes and that carried over to a subsequent visual search task. Our results provide insights into how attention and reward jointly determine how we learn. They support the powerful learning rules that capitalize on the conjoint influence of these two factors on neuronal plasticity.

Working memory accuracy for multiple targets is driven by reward expectation and stimulus contrast with different time-courses.

The richness of sensory input dictates that the brain must prioritize and select information for further processing and storage in working memory. Stimulus salience and reward expectations influence this prioritization but their relative contributions and underlying mechanisms are poorly understood. Here we investigate how the quality of working memory for multiple stimuli is determined by priority during encoding and later memory phases. Selective attention could, for instance, act as the primary gating mechanism when stimuli are still visible. Alternatively, observers might still be able to shift priorities across memories during maintenance or retrieval. To distinguish between these possibilities, we investigated how and when reward cues determine working memory accuracy and found that they were only effective during memory encoding. Previously learned, but currently non-predictive, color-reward associations had a similar influence, which gradually weakened without reinforcement. Finally, we show that bottom-up salience, manipulated through varying stimulus contrast, influences memory accuracy during encoding with a fundamentally different time-course than top-down reward cues. While reward-based effects required long stimulus presentation, the influence of contrast was strongest with brief presentations. Our results demonstrate how memory resources are distributed over memory targets and implicates selective attention as a main gating mechanism between sensory and memory systems.

Serial grouping of 2D-image regions with object-based attention in humans.

After an initial stage of local analysis within the retina and early visual pathways, the human visual system creates a structured representation of the visual scene by co-selecting image elements that are part of behaviorally relevant objects. The mechanisms underlying this perceptual organization process are only partially understood. We here investigate the time-course of perceptual grouping of two-dimensional image-regions by measuring the reaction times of human participants and report that it is associated with the gradual spread of object-based attention. Attention spreads fastest over large and homogeneous areas and is slowed down at locations that require small-scale processing. We find that the time-course of the object-based selection process is well explained by a 'growth-cone' model, which selects surface elements in an incremental, scale-dependent manner. We discuss how the visual cortical hierarchy can implement this scale-dependent spread of object-based attention, leveraging the different receptive field sizes in distinct cortical areas.

The Effects of Context and Attention on Spiking Activity in Human Early Visual Cortex.

Here we report the first quantitative analysis of spiking activity in human early visual cortex. We recorded multi-unit activity from two electrodes in area V2/V3 of a human patient implanted with depth electrodes as part of her treatment for epilepsy. We observed well-localized multi-unit receptive fields with tunings for contrast, orientation, spatial frequency, and size, similar to those reported in the macaque. We also observed pronounced gamma oscillations in the local-field potential that could be used to estimate the underlying spiking response properties. Spiking responses were modulated by visual context and attention. We observed orientation-tuned surround suppression: responses were suppressed by image regions with a uniform orientation and enhanced by orientation contrast. Additionally, responses were enhanced on regions that perceptually segregated from the background, indicating that neurons in the human visual cortex are sensitive to figure-ground structure. Spiking responses were also modulated by object-based attention. When the patient mentally traced a curve through the neurons' receptive fields, the accompanying shift of attention enhanced neuronal activity. These results demonstrate that the tuning properties of cells in the human early visual cortex are similar to those in the macaque and that responses can be modulated by both contextual factors and behavioral relevance. Our results, therefore, imply that the macaque visual system is an excellent model for the human visual cortex.

Noninvasive Brain Stimulation in Pediatric Attention-Deficit Hyperactivity Disorder (ADHD): A Review.

Attention-deficit hyperactivity disorder (ADHD) is one of the most prevalent neurodevelopmental disorders in the pediatric population. The clinical management of ADHD is currently limited by a lack of reliable diagnostic biomarkers and inadequate therapy for a minority of patients who do not respond to standard pharmacotherapy. There is optimism that noninvasive brain stimulation may help to address these limitations. Transcranial magnetic stimulation and transcranial direct current stimulation are 2 methods of noninvasive brain stimulation that modulate cortical excitability and brain network activity. Transcranial magnetic stimulation can be used diagnostically to probe cortical neurophysiology, whereas daily use of repetitive transcranial magnetic stimulation or transcranial direct current stimulation can induce long-lasting and potentially therapeutic changes in targeted networks. In this review, we highlight research showing the potential diagnostic and therapeutic applications of transcranial magnetic stimulation and transcranial direct current stimulation in pediatric ADHD. We also discuss the safety and ethics of using these tools in the pediatric population.

TMS affects moral judgment, showing the role of DLPFC and TPJ in cognitive and emotional processing.

Decision-making involves a complex interplay of emotional responses and reasoning processes. In this study, we use TMS to explore the neurobiological substrates of moral decisions in humans. To examining the effects of TMS on the outcome of a moral-decision, we compare the decision outcome of moral-personal and moral-impersonal dilemmas to each other and examine the differential effects of applying TMS over the right DLPFC or right TPJ. In this comparison, we find that the TMS-induced disruption of the DLPFC during the decision process, affects the outcome of the moral-personal judgment, while TMS-induced disruption of TPJ affects only moral-impersonal conditions. In other words, we find a double-dissociation between DLPFC and TPJ in the outcome of a moral decision. Furthermore, we find that TMS-induced disruption of the DLPFC during non-moral, moral-impersonal, and moral-personal decisions lead to lower ratings of regret about the decision. Our results are in line with the dual-process theory and suggest a role for both the emotional response and cognitive reasoning process in moral judgment. Both the emotional and cognitive processes were shown to be involved in the decision outcome.

Surface reconstruction, figure-ground modulation, and border-ownership.

The Differentiation-Integration for Surface Completion (DISC) model aims to explain the reconstruction of visual surfaces. We find the model a valuable contribution to our understanding of figure-ground organization. We point out that, next to border-ownership, neurons in visual cortex code whether surface elements belong to a figure or the background and that this is influenced by attention. We furthermore suggest that there must be strong links between object recognition and figure-ground assignment in order to resolve the status of interior contours. Incorporation of these factors in neurocomputational models will further improve our understanding of surface reconstruction, figure-ground organization, and border-ownership.

The time course of perceptual grouping in natural scenes.

Visual perception starts with localized filters that subdivide the image into fragments that undergo separate analyses. The visual system has to reconstruct objects by grouping image fragments that belong to the same object. A widely held view is that perceptual grouping occurs in parallel across the visual scene and without attention. To test this idea, we measured the speed of grouping in pictures of animals and vehicles. In a classification task, these pictures were categorized efficiently. In an image-parsing task, participants reported whether two cues fell on the same or different objects, and we measured reaction times. Despite the participants' fast object classification, perceptual grouping required more time if the distance between cues was larger, and we observed an additional delay when the cues fell on different parts of a single object. Parsing was also slower for inverted than for upright objects. These results imply that perception starts with rapid object classification and that rapid classification is followed by a serial perceptual grouping phase, which is more efficient for objects in a familiar orientation than for objects in an unfamiliar orientation.