Orbital frontal cortex updates state-induced value change for decision-making.
ABSTRACT: 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:Adaptive decision making in dynamic environments requires multiple reinforcement-learning steps that may be implemented by dissociable neural circuits. Here, we used a novel directionally specific viral ablation approach to investigate the function of several anatomically defined orbitofrontal cortex (OFC) circuits during adaptive, flexible decision making in rats trained on a probabilistic reversal learning task. Ablation of OFC neurons projecting to the nucleus accumbens selectively disrupted performance following a reversal, by disrupting the use of negative outcomes to guide subsequent choices. Ablation of amygdala neurons projecting to the OFC also impaired reversal performance, but due to disruptions in the use of positive outcomes to guide subsequent choices. Ablation of OFC neurons projecting to the amygdala, by contrast, enhanced reversal performance by destabilizing action values. Our data are inconsistent with a unitary function of the OFC in decision making. Rather, distinct OFC-amygdala-striatal circuits mediate distinct components of the action-value updating and maintenance necessary for decision making.
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: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:Two ideas have dominated neuropsychology concerning the orbitofrontal cortex (OFC). One holds that OFC regulates emotion and enhances behavioral flexibility through inhibitory control. The other ascribes to OFC a role in updating valuations on the basis of current motivational states. Neuroimaging, neurophysiological and clinical observations are consistent with either or both hypotheses. Although these hypotheses are compatible in principle, we present results supporting the latter view of OFC function and arguing against the former. We found that excitotoxic, fiber-sparing lesions confined to OFC in monkeys did not alter either behavioral flexibility, as measured by object reversal learning, or emotion regulation, as assessed by fear of snakes. A follow-up experiment indicated that a previously reported loss of inhibitory control resulted from damage to nearby fiber tracts and not from OFC dysfunction. Thus, OFC has a more specialized role in reward-guided behavior and emotion than has been thought, a function that includes value updating.
Project description:Understanding how the human brain translates sensory impressions into conscious percepts is a key challenge of neuroscience research. Work in this area has overwhelmingly centered on the conscious experience of vision at the exclusion of the other senses--in particular, smell. We hypothesized that the orbitofrontal cortex (OFC) is a central substrate for olfactory conscious experience because of its privileged physiological role in odor processing. Combining functional magnetic resonance imaging, peripheral autonomic recordings, and olfactory psychophysics, we studied a case of complete anosmia (smell loss) in a patient with circumscribed traumatic brain injury to the right OFC. Despite a complete absence of conscious olfaction, the patient exhibited robust "blind smell," as indexed by reliable odor-evoked neural activity in the left OFC and normal autonomic responses to odor hedonics during presentation of stimuli to the left nostril. These data highlight the right OFC's critical role in subserving human olfactory consciousness.
Project description:We investigated how different subregions of rodent prefrontal cortex contribute to value-based decision making, by comparing neural signals related to animal's choice, its outcome, and action value in orbitofrontal cortex (OFC) and medial prefrontal cortex (mPFC) of rats performing a dynamic two-armed bandit task. Neural signals for upcoming action selection arose in the mPFC, including the anterior cingulate cortex, only immediately before the behavioral manifestation of animal's choice, suggesting that rodent prefrontal cortex is not involved in advanced action planning. Both OFC and mPFC conveyed signals related to the animal's past choices and their outcomes over multiple trials, but neural signals for chosen value and reward prediction error were more prevalent in the OFC. Our results suggest that rodent OFC and mPFC serve distinct roles in value-based decision making and that the OFC plays a prominent role in updating the values of outcomes expected from chosen actions.
Project description:Both basal ganglia (BG) and orbitofrontal cortex (OFC) have been widely implicated in social and non-social decision-making. However, unlike OFC damage, BG pathology is not typically associated with disturbances in social functioning. Here we studied the behavior of patients with focal lesions to either BG or OFC in a multi-strategy competitive game known to engage these regions. We find that whereas OFC patients are significantly impaired, BG patients show intact learning in the economic game. By contrast, when information about the strategic context is absent, both cohorts are significantly impaired. Computational modeling further shows a preserved ability in BG patients to learn by anticipating and responding to the behavior of others using the strategic context. These results suggest that apparently divergent findings on BG contribution to social decision-making may instead reflect a model where higher-order learning processes are dissociable from trial-and-error learning, and can be preserved despite BG damage.
Project description:Animals face the dilemma between exploiting known opportunities and exploring new ones, a decision-making process supported by cortical circuits. While different types of learning may bias exploration, the circumstances and the degree to which bias occurs is unclear. We used an instrumental lever press task in mice to examine whether learned rules generalize to exploratory situations and the cortical circuits involved. We first trained mice to press one lever for food and subsequently assessed how that learning influenced pressing of a second novel lever. Using outcome devaluation procedures we found that novel lever exploration was not dependent on the food value associated with the trained lever. Further, changes in the temporal uncertainty of when a lever press would produce food did not affect exploration. Instead, accrued experience with the instrumental contingency was strongly predictive of test lever pressing with a positive correlation between experience and trained lever exploitation, but not novel lever exploration. Chemogenetic attenuation of orbital frontal cortex (OFC) projection into secondary motor cortex (M2) biased novel lever exploration, suggesting that experience increases OFC-M2 dependent exploitation of learned associations but leaves exploration constant. Our data suggests exploitation and exploration are parallel decision-making systems that do not necessarily compete.
Project description:Behavioral inflexibility is a common symptom of neuropsychiatric disorders which can have a major detrimental impact on quality of life. While the orbitofrontal cortex (OFC) has been strongly implicated in behavioral flexibility in rodents across paradigms, our understanding of how the OFC mediates these behaviors is rapidly adapting. Here we examined neuronal activity during reversal learning by coupling in vivo electrophysiological recording with a mouse touch-screen learning paradigm to further elucidate the role of the OFC in updating reward value. Single unit and oscillatory activity was recorded during well-learned discrimination and 3 distinct phases of reversal (early, chance and well-learned). During touch-screen performance, OFC neuronal firing tracked rewarded responses following a previous rewarded choice when behavior was well learned, but shifted to primarily track repeated errors following a previous error in early reversal. Spike activity tracked rewarded choices independent of previous trial outcome during chance reversal, and returned to the initial pattern of reward response at criterion. Analysis of spike coupling to oscillatory local field potentials showed that less frequently occurring behaviors had significantly fewer neurons locked to any oscillatory frequency. Together, these data support the role of the OFC in tracking the value of individual choices to inform future responses and suggests that oscillatory signaling may be involved in propagating responses to increase or decrease the likelihood that action is taken in the future. They further support the use of touch-screen paradigms in preclinical studies to more closely model clinical approaches to measuring behavioral flexibility.