Covert shift of attention modulates the value encoding in the orbitofrontal cortex.
ABSTRACT: During value-based decision making, we often evaluate the value of each option sequentially by shifting our attention, even when the options are presented simultaneously. The orbitofrontal cortex (OFC) has been suggested to encode value during value-based decision making. Yet it is not known how its activity is modulated by attention shifts. We investigated this question by employing a passive viewing task that allowed us to disentangle effects of attention, value, choice and eye movement. We found that the attention modulated OFC activity through a winner-take-all mechanism. When we attracted the monkeys' attention covertly, the OFC neuronal activity reflected the reward value of the newly attended cue. The shift of attention could be explained by a normalization model. Our results strongly argue for the hypothesis that the OFC neuronal activity represents the value of the attended item. They provide important insights toward understanding the OFC's role in value-based decision making.
Project description:Recent hypotheses have posited that orbital frontal cortex (OFC) is important for using inferred consequences to guide behavior. Less clear is OFC's contribution to goal-directed or model-based behavior, where the decision to act is controlled by previous experience with the consequence or outcome. Investigating OFC's role in learning about changed outcomes separate from decision-making is not trivial and often the two are confounded. Here we adapted an incentive learning task to mice, where we investigated processes controlling experience-based outcome updating independent from inferred action control. We found chemogenetic OFC attenuation did not alter the ability to perceive motivational state-induced changes in outcome value but did prevent the experience-based updating of this change. Optogenetic inhibition of OFC excitatory neuron activity selectively when experiencing an outcome change disrupted the ability to update, leaving mice unable to infer the appropriate behavior. Our findings support a role for OFC in learning that controls decision-making.
Project description:Orbitofrontal cortex (OFC) is widely held to be critical for flexibility in decision-making when established choice values change. OFC's role in such decision making was investigated in macaques performing dynamically changing three-armed bandit tasks. After selective OFC lesions, animals were impaired at discovering the identity of the highest value stimulus following reversals. However, this was not caused either by diminished behavioral flexibility or by insensitivity to reinforcement changes, but instead by paradoxical increases in switching between all stimuli. This pattern of choice behavior could be explained by a causal role for OFC in appropriate contingent learning, the process by which causal responsibility for a particular reward is assigned to a particular choice. After OFC lesions, animals' choice behavior no longer reflected the history of precise conjoint relationships between particular choices and particular rewards. Nonetheless, OFC-lesioned animals could still approximate choice-outcome associations using a recency-weighted history of choices and rewards.
Project description:Orbitofrontal cortex (OFC) function is often characterized in terms of stimulus-reward mapping; however, more recent evidence suggests that the OFC may play a role in selecting and representing extended actions. First, previously encoded reward associations in the OFC could be used to inform responding in novel but similar situations. Second, when evaluated in tasks requiring the animal to perform extended actions, response selective activity can be recorded in the OFC. Finally, the interaction between the OFC and hippocampus illustrates OFC's role in response selection. The OFC may facilitate reward-guided memory retrieval by selecting the memories most relevant to achieve a goal. This model for OFC function places it within the hierarchy of increasingly complex action representations that support decision making.
Project description:We examined whether the preparation of saccadic eye movements, when behaviorally dissociated from covert attention, modulates activity within visual cortex. We measured single-neuron and local field potential (LFP) responses to visual stimuli in area V4 while monkeys covertly attended a stimulus at one location and prepared saccades to a potential target at another. In spite of the irrelevance of visual information at the saccade target, visual activity at that location was modulated at least as much as, and often more than, activity at the covertly attended location. Modulations of activity at the attended and saccade target locations were qualitatively similar and included increased response magnitude, stimulus selectivity, and spiking reliability, as well as increased gamma and decreased low-frequency power of LFPs. These results demonstrate that saccade preparation is sufficient to modulate visual cortical representations and suggest that the interrelationship of oculomotor and attention-related mechanisms extends to posterior visual cortex.
Project description:Anterior insular and orbitofrontal cortex (AIC and OFC, respectively) are known to play important roles in decision making under risk. However, risk-related AIC neural activity has not been investigated and it is controversial whether the rodent OFC conveys genuine risk signals. To address these issues, we examined AIC and OFC neuronal activity in rats responding to five distinct auditory cues predicting water reward with different probabilities. Both structures conveyed significant neural signals for reward, value and risk, with value and risk signals conjunctively coded. However, value signals were stronger and appeared earlier in the OFC, and many risk-coding OFC neurons responded only to the cue predicting certain (100%) reward. Also, AIC neurons tended to increase their activity for a prolonged time following a negative outcome and according to previously expected value. These results show that both the AIC and OFC convey neural signals related to reward uncertainty, but in different ways. The OFC might play an important role in encoding certain reward-biased, risk-modulated subjective value, whereas the AIC might convey prolonged negative outcome and disappointment signals.
Project description:Naturalistic decision-making typically involves sequential deployment of attention to choice alternatives to gather information before a decision is made. Attention filters how information enters decision circuits, thus implying that attentional control may shape how decision computations unfold. We recorded neuronal activity from three subregions of the prefrontal cortex (PFC) while monkeys performed an attention-guided decision-making task. From the first saccade to decision-relevant information, a triple dissociation of decision- and attention-related computations emerged in parallel across PFC subregions. During subsequent saccades, orbitofrontal cortex activity reflected the value comparison between currently and previously attended information. In contrast, the anterior cingulate cortex carried several signals reflecting belief updating in light of newly attended information, the integration of evidence to a decision bound and an emerging plan for what action to choose. Our findings show how anatomically dissociable PFC representations evolve during attention-guided information search, supporting computations critical for value-guided choice.
Project description:We examined the contribution of the amygdala to value signals within orbital prefrontal cortex (OFC) and medial prefrontal cortex (MFC). On each trial, monkeys chose between two stimuli that were associated with different quantities of reward. In intact monkeys, as expected, neurons in both OFC and MFC signaled the reward quantity associated with stimuli. Contrasted with MFC, OFC contained a larger proportion of neurons encoding reward quantity and did so with faster response latencies. Removing the amygdala eliminated these differences, mainly by decreasing value coding in OFC. Similar decreases occurred in OFC immediately before and after reward delivery. Although the amygdala projects to both OFC and MFC, we found that it has its greatest influence over reward-value coding in OFC. Notably, amygdala lesions did not abolish value coding in OFC, which shows that OFC's representations of the value of objects, choices, and outcomes depends, in large part, on other sources.
Project description:Decision makers are curious and consequently value advance information about future events. We made use of this fact to test competing theories of value representation in area 13 of orbitofrontal cortex (OFC). In a new task, we found that monkeys reliably sacrificed primary reward (water) to view advance information about gamble outcomes. While monkeys integrated information value with primary reward value to make their decisions, OFC neurons had no systematic tendency to integrate these variables, instead encoding them in orthogonal manners. These results suggest that the predominant role of the OFC is to encode variables relevant for learning, attention, and decision making, rather than integrating them into a single scale of value. They also suggest that OFC may be placed at a relatively early stage in the hierarchy of information-seeking decisions, before evaluation is complete. Thus, our results delineate a circuit for information-seeking decisions and suggest a neural basis for curiosity.
Project description:When making a subjective choice, the brain must compute a value for each option and compare those values to make a decision. The orbitofrontal cortex (OFC) is critically involved in this process, but the neural mechanisms remain obscure, in part due to limitations in our ability to measure and control the internal deliberations that can alter the dynamics of the decision process. Here we tracked these dynamics by recovering temporally precise neural states from multidimensional data in OFC. During individual choices, OFC alternated between states associated with the value of two available options, with dynamics that predicted whether a subject would decide quickly or vacillate between the two alternatives. Ensembles of value-encoding neurons contributed to these states, with individual neurons shifting activity patterns as the network evaluated each option. Thus, the mechanism of subjective decision-making involves the dynamic activation of OFC states associated with each choice alternative.
Project description:Although perceptual decision making activates a network of brain areas involved in sensory, integrative, and motor functions, circuit activity can clearly be modulated by factors beyond the stimulus. Of particular interest is to understand how the network is modulated by top-down factors such as attention. Here, we demonstrate in a motion coherence task that selective attention produces marked changes in the blood oxygen level-dependent (BOLD) response in a subset of regions within a human perceptual decision-making circuit. Specifically, when motion is attended, the BOLD response decreases with increasing motion coherence in many regions, including the motion-sensitive area MT+, the intraparietal sulcus, and the inferior frontal sulcus. However, when motion is ignored, the negative parametric response in a subset of this circuit becomes positive. Through both modeling and connectivity analyses, we demonstrate that this inversion both reflects a top-down influence and segregates attentional from accumulation regions, thereby permitting us to further delineate the contributions of different regions to the perceptual decision.