Whether driving a car, shopping for food, or paying attention in a classroom of boisterous teenagers, it’s often hard to maintain focus on goals in the face of distraction. Brain imaging studies in ...humans implicate the dorsal anterior cingulate cortex (dACC) in regulating the conflict between goals and distractors. Here we show that single dACC neurons signal conflict between task goals and distractors in the rhesus macaque, particularly for biologically relevant social stimuli. For some neurons, task conflict signals predicted subsequent changes in pupil size—a peripheral index of arousal linked to noradrenergic tone—associated with reduced distractor interference. dACC neurons also responded to errors, and these signals predicted adjustments in pupil size. These findings provide the first neurophysiological endorsement of the hypothesis that dACC regulates conflict, in part, via modulation of pupil-linked processes such as arousal.
•Conflict is signaled in rhesus macaque dorsal anterior cingulate cortex (dACC)•Conflict signals in macaque dACC are linked to task, rather than action conflict•dACC neurons also track pupil size and predict adjustments in pupil size•dACC responses to both conflict and errors are linked to pupil size within neurons
Cingulate conflict signals have been thought of as uniquely human, but Ebitz et al. report conflict signals in macaque neurons. These neurons predicted task-facilitating adjustments in arousal in response to both conflict and errors, suggesting a unified function for dACC.
The prefrontal cortex (PFC) is thought to flexibly regulate sensorimotor responses, perhaps through modulating activity in other circuits. However, the scope of that control remains unknown: it ...remains unclear whether the PFC can modulate basic reflexes. One canonical example of a central reflex is the pupil light reflex (PLR): the automatic constriction of the pupil in response to luminance increments. Unlike pupil size, which depends on the interaction of multiple physiological and neuromodulatory influences, the PLR reflects the action of a simple brainstem circuit. However, emerging behavioral evidence suggests that the PLR may be modulated by cognitive processes. Although the neural basis of these modulations remains unknown, one possible source is the PFC, particularly the frontal eye field (FEF), an area of the PFC implicated in the control of attention. We show that microstimulation of the rhesus macaque FEF alters the magnitude of the PLR in a spatially specific manner. FEF microstimulation enhanced the PLR to probes presented within the stimulated visual field, but suppressed the PLR to probes at nonoverlapping locations. The spatial specificity of this effect parallels the effect of FEF stimulation on attention and suggests that FEF is capable of modulating visuomotor transformations performed at a lower level than was previously known. These results provide evidence of the selective regulation of a basic brainstem reflex by the PFC.
The pupil light reflex (PLR) is our brain's first and most fundamental mechanism for light adaptation. Although it is often described in textbooks as being an immutable reflex, converging evidence suggests that the magnitude of the PLR is modulated by cognitive factors. The neural bases of these modulations are unknown. Here, we report that microstimulation in the prefrontal cortex (PFC) modulates the gain of the PLR, changing how a simple reflex circuit responds to physically identical stimuli. These results suggest that control structures such as the PFC can add complexity and flexibility to even a basic brainstem circuit.
A major shift is happening within neurophysiology: a population doctrine is drawing level with the single-neuron doctrine that has long dominated the field. Population-level ideas have so far had ...their greatest impact in motor neuroscience, but they hold great promise for resolving open questions in cognition as well. Here, we codify the population doctrine and survey recent work that leverages this view to specifically probe cognition. Our discussion is organized around five core concepts that provide a foundation for population-level thinking: (1) state spaces, (2) manifolds, (3) coding dimensions, (4) subspaces, and (5) dynamics. The work we review illustrates the progress and promise that population-level thinking holds for cognitive neuroscience—for delivering new insight into attention, working memory, decision-making, executive function, learning, and reward processing.
The population doctrine holds that the fundamental computational unit of the brain is the population. This view holds great promise for resolving open questions in cognition. Ebitz and Hayden discuss five core concepts of population analysis and review relevant papers.
In uncertain environments, decision-makers must balance two goals: they must “exploit” rewarding options but also “explore” in order to discover rewarding alternatives. Exploring and exploiting ...necessarily change how the brain responds to identical stimuli, but little is known about how these states, and transitions between them, change how the brain transforms sensory information into action. To address this question, we recorded neural activity in a prefrontal sensorimotor area while monkeys naturally switched between exploring and exploiting rewarding options. We found that exploration profoundly reduced spatially selective, choice-predictive activity in single neurons and delayed choice-predictive population dynamics. At the same time, reward learning was increased in brain and behavior. These results indicate that exploration is related to sudden disruptions in prefrontal sensorimotor control and rapid, reward-dependent reorganization of control dynamics. This may facilitate discovery through trial and error.
•Monkeys transition between exploratory and exploitative goal states•During exploration, prefrontal choice-predictive activity is virtually absent•Prefrontal dynamics are disrupted during exploration both within and across trials•Exploration enhances reward-dependent learning in brain and behavior
Exploratory choices permit the discovery of new rewarding options. Ebitz et al. report that spatially selective, choice-predictive neurons in the prefrontal cortex do not predict choice before exploratory decisions. Reduced prefrontal control may underlie flexible decision-making and trial-and-error discovery.
We have the capacity to follow arbitrary stimulus-response rules, meaning simple policies that guide our behavior. Rule identity is broadly encoded across decision-making circuits, but there are less ...data on how rules shape the computations that lead to choices. One idea is that rules could simplify these computations. When we follow a rule, there is no need to encode or compute information that is irrelevant to the current rule, which could reduce the metabolic or energetic demands of decision-making. However, it is not clear if the brain can actually take advantage of this computational simplicity. To test this idea, we recorded from neurons in 3 regions linked to decision-making, the orbitofrontal cortex (OFC), ventral striatum (VS), and dorsal striatum (DS), while macaques performed a rule-based decision-making task. Rule-based decisions were identified via modeling rules as the latent causes of decisions. This left us with a set of physically identical choices that maximized reward and information, but could not be explained by simple stimulus-response rules. Contrasting rule-based choices with these residual choices revealed that following rules (1) decreased the energetic cost of decision-making; and (2) expanded rule-relevant coding dimensions and compressed rule-irrelevant ones. Together, these results suggest that we use rules, in part, because they reduce the costs of decision-making through a distributed representational warping in decision-making circuits.
Over 50 years of research have established that cognitive processes influence pupil size. This has led to the widespread use of pupil size as a peripheral measure of cortical processing in psychology ...and neuroscience. However, the function of cortical control over the pupil remains poorly understood. Why does visual attention change the pupil light reflex? Why do mental effort and surprise cause pupil dilation? Here, we consider these functional questions as we review and synthesize two literatures on cognitive effects on the pupil: how cognition affects pupil light response and how cognition affects pupil size under constant luminance. We propose that cognition may have co-opted control of the pupil in order to filter incoming visual information to optimize it for particular goals. This could complement other cortical mechanisms through which cognition shapes visual perception.
Exogenous application of the neuromodulatory hormone oxytocin (OT) promotes prosocial behavior and can improve social function. It is unclear, however, whether OT promotes prosocial behavior per se, ...or whether it facilitates social interaction by reducing a state of vigilance toward potential social threats. To disambiguate these two possibilities, we exogenously delivered OT to male rhesus macaques, which have a characteristic pattern of species-typical social vigilance, and examined their performance in three social attention tasks. We first determined that, in the absence of competing task demands or goals, OT increased attention to faces and eyes, as in humans. By contrast, OT reduced species typical social vigilance for unfamiliar, dominant, and emotional faces in two additional tasks. OT eliminated the emergence of a typical state of vigilance when dominant face images were available during a social image choice task. Moreover, OT improved performance on a reward-guided saccade task, despite salient social distractors: OT reduced the interference of unfamiliar faces, particularly emotional ones, when these faces were task irrelevant. Together, these results demonstrate that OT suppresses vigilance toward potential social threats in the rhesus macaque. We hypothesize that a basic role for OT in regulating social vigilance may have facilitated the evolution of prosocial behaviors in humans.
Abstract We make decisions by comparing values, but it is not yet clear how value is represented in the brain. Many models assume, if only implicitly, that the representational geometry of value is ...linear. However, in part due to a historical focus on noisy single neurons, rather than neuronal populations, this hypothesis has not been rigorously tested. Here, we examine the representational geometry of value in the ventromedial prefrontal cortex (vmPFC), a part of the brain linked to economic decision-making, in two male rhesus macaques. We find that values are encoded along a curved manifold in vmPFC. This curvilinear geometry predicts a specific pattern of irrational decision-making: that decision-makers will make worse choices when an irrelevant, decoy option is worse in value, compared to when it is better. We observe this type of irrational choices in behavior. Together, these results not only suggest that the representational geometry of value is nonlinear, but that this nonlinearity could impose bounds on rational decision-making.
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