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Dorsomedial and ventromedial prefrontal cortex lesions differentially impact social influence and temporal discounting.
The medial prefrontal cortex (mPFC) has long been associated with economic and social decision-making in neuroimaging studies. Several debates question whether different ventral mPFC (vmPFC) and dorsal mPFC (dmPFC) regions have specific functions or whether there is a gradient supporting social and nonsocial cognition. Here, we tested an unusually large sample of rare participants with focal damage to the mPFC (N = 33), individuals with lesions elsewhere (N = 17), and healthy controls (N = 71) (total N = 121). Participants completed a temporal discounting task to estimate their baseline discounting preferences before learning the preferences of two other people, one who was more temporally impulsive and one more patient. We used Bayesian computational models to estimate baseline discounting and susceptibility to social influence after learning others' economic preferences. mPFC damage increased susceptibility to impulsive social influence compared to healthy controls and increased overall susceptibility to social influence compared to those with lesions elsewhere. Importantly, voxel-based lesion-symptom mapping (VLSM) of computational parameters showed that this heightened susceptibility to social influence was attributed specifically to damage to the dmPFC (area 9; permutation-based threshold-free cluster enhancement (TFCE) p < 0.025). In contrast, lesions in the vmPFC (areas 13 and 25) and ventral striatum were associated with a preference for seeking more immediate rewards (permutation-based TFCE p < 0.05). We show that the dmPFC is causally implicated in susceptibility to social influence, with distinct ventral portions of mPFC involved in temporal discounting. These findings provide causal evidence for sub-regions of the mPFC underpinning fundamental social and cognitive processes.
Neural dynamics of reselecting visual and motor contents in working memory after external interference.
In everyday tasks, we must often shift our focus away from internal representations held in working memory to engage with perceptual events in the external world. Here, we investigated how our internal focus is reestablished following an interrupting task by tracking the reselection of visual representations and their associated action plans in working memory. Specifically, we ask whether reselection occurs for both visual and motor memory attributes and when this reselection occurs. We developed a visual-motor working-memory task in which participants were retrospectively cued to select one of two memory items before being interrupted by a perceptual discrimination task. To determine what information was reselected, the memory items had distinct visual and motor attributes. To determine when internal representations were reselected, the interrupting task was presented at one of three distinct time points following the retro-cue. We employed electroencephalography time-frequency analyses to track the initial selection and later reselection of visual and motor representations, as operationalized through modulations of posterior alpha (8-12 Hz) activity relative to the memorized item location (visual) and of central beta (13-30 Hz) activity relative to the required response hand (motor). Our results showed that internal visual and motor contents were concurrently reselected immediately after completing the interrupting task, rather than only when internal information was required for memory-guided behavior. Thus, following interruption, we swiftly resume our internal focus in working memory through the simultaneous reselection of memorized visual representations and their associated action plans, thereby restoring internal contents to a ready-to-use state.Significance statement A key challenge for working memory is to maintain past visual representations and their associated actions while engaging with the external environment. Our cognitive system must, therefore, often juggle multiple tasks within a common time frame. Despite the ubiquity of multi-task situations in everyday life, working memory has predominantly been studied devoid of additional perceptual, attentional, and response demands during the retention interval. Here, we investigate the neural dynamics of returning to internal contents following task-relevant interruptions. Particularly, we identify which attributes of internal representations are reselected and when this reselection occurs. Our findings demonstrate that both visual and motor contents are reselected immediately and in tandem after completion of an external, interrupting task.
Evaluation of an adaptation to the Oxford Cognitive Screen for reduced visual acuity: a cohort study.
BACKGROUND: The Oxford Cognitive Screen (OCS) was specifically designed for acute stroke survivors and to be inclusive of aphasia, neglect, motor impairments. However, reduced visual acuity (VA), including lack of access to required reading glasses, can impact completion rates and performance. The aim of the study was to evaluate contrast enhanced OCS-tasks for completion rates and equivalence to the original version. METHODS: Adult stroke survivors were asked to complete two versions (standard and adapted) of two tasks (broken hearts cancellation and trails) in a randomized order, to determine relative completion rates and equivalency. A bedside vision assessment, completed by an orthoptist was collected, including near and distance VA with required refractive correction if available. Two groups were created based on near VA; normal near VA (≥0.2LogMAR) and reduced near VA (<0.2LogMAR). RESULTS: Five hundred participants were recruited, 56.8% male, mean age 70.62 years. Mean near VA was 0.278 (SD0.277) LogMAR. The broken hearts and trails tasks were completed by 2.2% (p=0.041) and 0.4% (p=0.791) more participants respectively with the adapted version. Participants completing both versions with good near VA were used to analyze equivalence. All the lower and upper bounds of the two one-sided test of equivalence fell within the range of 0.5SD for all scores, indicating that the means are equivalent. Analysis of impairment detection revealed fair to good agreement. CONCLUSION: The adapted version is suitable for stroke survivors with reduced near VA to complete the assessment. In the presence of good VA, the tasks were deemed to be equivalent.
A view-based decision mechanism for rewards in the primate amygdala.
Primates make decisions visually by shifting their view from one object to the next, comparing values between objects, and choosing the best reward, even before acting. Here, we show that when monkeys make value-guided choices, amygdala neurons encode their decisions in an abstract, purely internal representation defined by the monkey's current view but not by specific object or reward properties. Across amygdala subdivisions, recorded activity patterns evolved gradually from an object-specific value code to a transient, object-independent code in which currently viewed and last-viewed objects competed to reflect the emerging view-based choice. Using neural-network modeling, we identified a sequence of computations by which amygdala neurons implemented view-based decision making and eventually recovered the chosen object's identity when the monkeys acted on their choice. These findings reveal a neural mechanism in the amygdala that derives object choices from abstract, view-based computations, suggesting an efficient solution for decision problems with many objects.
Mechanisms of adjustments to different types of uncertainty in the reward environment across mice and monkeys.
Despite being unpredictable and uncertain, reward environments often exhibit certain regularities, and animals navigating these environments try to detect and utilize such regularities to adapt their behavior. However, successful learning requires that animals also adjust to uncertainty associated with those regularities. Here, we analyzed choice data from two comparable dynamic foraging tasks in mice and monkeys to investigate mechanisms underlying adjustments to different types of uncertainty. In these tasks, animals selected between two choice options that delivered reward probabilistically, while baseline reward probabilities changed after a variable number (block) of trials without any cues to the animals. To measure adjustments in behavior, we applied multiple metrics based on information theory that quantify consistency in behavior, and fit choice data using reinforcement learning models. We found that in both species, learning and choice were affected by uncertainty about reward outcomes (in terms of determining the better option) and by expectation about when the environment may change. However, these effects were mediated through different mechanisms. First, more uncertainty about the better option resulted in slower learning and forgetting in mice, whereas it had no significant effect in monkeys. Second, expectation of block switches accompanied slower learning, faster forgetting, and increased stochasticity in choice in mice, whereas it only reduced learning rates in monkeys. Overall, while demonstrating the usefulness of metrics based on information theory in examining adaptive behavior, our study provides evidence for multiple types of adjustments in learning and choice behavior according to uncertainty in the reward environment.
Role of the amygdala in decisions under ambiguity and decisions under risk: evidence from patients with Urbach-Wiethe disease.
Various neuropsychological studies have shown that decision-making deficits can occur in a wide range of patients with brain damage or dysfunctions. Decisions under ambiguity, as measured with the Iowa Gambling Task, primarily depend on the integrity of the ventromedial prefrontal cortex and the amygdala, as well as on further brain regions such as the somatosensory cortex. However, little is known about the specific role of these structures in decisions under risk measured with tasks that offer explicit rules for gains and losses and winning probabilities, for example, the Game of Dice Task. We aimed to investigate the potential role of the amygdala for decisions under risk. For this purpose, we examined three patients with Urbach-Wiethe disease--a rare syndrome associated with selective bilateral mineralisation of the amygdalae. Neuropsychological performance was assessed with the Iowa Gambling Task (decisions under ambiguity), the Game of Dice Task (decisions under risk), and an extensive neuropsychological test battery focussing on executive functions. Furthermore, previous studies found relationships between generating skin conductance responses and deciding advantageously in the Iowa Gambling Task. Accordingly, we recorded skin conductance responses during both decision tasks as a measure of emotional reactivity. Results indicate that patients with selective amygdala damage have lower scores in both decisions under ambiguity and decisions under risk. Decisions under risk are especially compromised in patients who also demonstrate deficits in executive functioning. In both gambling tasks, patients showed reduced skin conductance responses compared to healthy comparison subjects. The results suggest that deciding advantageously under risk conditions involves both the use of feedback from previous trials, as required by decisions under ambiguity, and in addition, executive functions.
Decision-making, errors, and confidence in the brain.
To provide a fundamental basis for understanding decision-making and decision confidence, we analyze a neuronal spiking attractor-based model of decision-making. The model predicts probabilistic decision-making with larger neuronal responses and larger functional magnetic resonance imaging (fMRI) blood-oxygen-level-dependent (BOLD) responses on correct than on error trials because the spiking noise-influenced decision attractor state of the network is consistent with the external evidence. Moreover, the model predicts that the neuronal activity and the BOLD response will become larger on correct trials as the discriminability ΔI increases and confidence increases and will become smaller as confidence decreases on error trials as ΔI increases. Confidence is thus an emergent property of the model. In an fMRI study of an olfactory decision-making task, we confirm these predictions for cortical areas including medial prefrontal cortex and the cingulate cortex implicated in choice decision-making, showing a linear increase in the BOLD signal with ΔI on correct trials, and a linear decrease on error trials. These effects were not found in a control area, the orbitofrontal cortex, where reward value useful for the choice is represented on a continuous scale but that is not implicated in the choice itself. This provides a unifying approach to decision-making and decision confidence and to how spiking-related noise affects choice, confidence, synaptic and neuronal activity, and fMRI signals.
From affective value to decision-making in the prefrontal cortex.
Representing the affective value of a reward on a continuous scale may occur separately from making a binary, for example yes vs no, decision about whether to choose the reward. To investigate whether these are separable processes, we used functional magnetic resonance imaging to measure activations produced by pleasant warm, unpleasant cold, and affectively complex combinations of these stimuli applied to the hand. On some trials the affective value was rated on a continuous scale, and on different trials a yes-no decision was made about whether the stimulus should be repeated in future. Decision-making contrasted with just rating the affective stimuli revealed activations in the medial prefrontal cortex area 10, implicating this area in binary decision-making. Activations related to the pleasantness ratings and which were not influenced when a binary decision was made were found in the pregenual cingulate and parts of the orbitofrontal cortex, implicating these regions in the continuous representation of affective value. When a decision was yes vs. no, effects were found in the dorsal cingulate cortex, agranular (anterior) insula and ventral tegmental area, implicating these areas in initiating actions to obtain goals.
The orbitofrontal cortex and beyond: from affect to decision-making.
The orbitofrontal cortex represents the reward or affective value of primary reinforcers including taste, touch, texture, and face expression. It learns to associate other stimuli with these to produce representations of the expected reward value for visual, auditory, and abstract stimuli including monetary reward value. The orbitofrontal cortex thus plays a key role in emotion, by representing the goals for action. The learning process is stimulus-reinforcer association learning. Negative reward prediction error neurons are related to this affective learning. Activations in the orbitofrontal cortex correlate with the subjective emotional experience of affective stimuli, and damage to the orbitofrontal cortex impairs emotion-related learning, emotional behaviour, and subjective affective state. With an origin from beyond the orbitofrontal cortex, top-down attention to affect modulates orbitofrontal cortex representations, and attention to intensity modulates representations in earlier cortical areas of the physical properties of stimuli. Top-down word-level cognitive inputs can bias affective representations in the orbitofrontal cortex, providing a mechanism for cognition to influence emotion. Whereas the orbitofrontal cortex provides a representation of reward or affective value on a continuous scale, areas beyond the orbitofrontal cortex such as the medial prefrontal cortex area 10 are involved in binary decision-making when a choice must be made. For this decision-making, the orbitofrontal cortex provides a representation of each specific reward in a common currency.
Experimentally revealed stochastic preferences for multicomponent choice options.
Realistic, everyday rewards contain multiple components. An apple has taste and size. However, we choose in single dimensions, simply preferring some apples to others. How can such single-dimensional preference relationships refer to multicomponent choice options? Here, we measured how stochastic choices revealed preferences for 2-component milkshakes. The preferences were intuitively graphed as indifference curves that represented the orderly integration of the 2 components as trade-off: parts of 1 component were given up for obtaining 1 additional unit of the other component without a change in preference. The well-ordered, nonoverlapping curves satisfied leave-one-out tests, followed predictions by machine learning decoders and correlated with single-dimensional Becker-DeGroot-Marschak (BDM) auction-like bids for the 2-component rewards. This accuracy suggests a decision process that integrates multiple reward components into single-dimensional estimates in a systematic fashion. In interspecies comparisons, human performance matched that of highly experienced laboratory monkeys, as measured by accuracy of the critical trade-off between bundle components. These data describe the nature of choices of multicomponent choice options and attest to the validity of the rigorous economic concepts and their convenient graphic schemes for explaining choices of human and nonhuman primates. The results encourage formal behavioral and neural investigations of normal, irrational, and pathological economic choices. (PsycInfo Database Record (c) 2020 APA, all rights reserved).
Attention-dependent modulation of cortical taste circuits revealed by Granger causality with signal-dependent noise.
We show, for the first time, that in cortical areas, for example the insular, orbitofrontal, and lateral prefrontal cortex, there is signal-dependent noise in the fMRI blood-oxygen level dependent (BOLD) time series, with the variance of the noise increasing approximately linearly with the square of the signal. Classical Granger causal models are based on autoregressive models with time invariant covariance structure, and thus do not take this signal-dependent noise into account. To address this limitation, here we describe a Granger causal model with signal-dependent noise, and a novel, likelihood ratio test for causal inferences. We apply this approach to the data from an fMRI study to investigate the source of the top-down attentional control of taste intensity and taste pleasantness processing. The Granger causality with signal-dependent noise analysis reveals effects not identified by classical Granger causal analysis. In particular, there is a top-down effect from the posterior lateral prefrontal cortex to the insular taste cortex during attention to intensity but not to pleasantness, and there is a top-down effect from the anterior and posterior lateral prefrontal cortex to the orbitofrontal cortex during attention to pleasantness but not to intensity. In addition, there is stronger forward effective connectivity from the insular taste cortex to the orbitofrontal cortex during attention to pleasantness than during attention to intensity. These findings indicate the importance of explicitly modeling signal-dependent noise in functional neuroimaging, and reveal some of the processes involved in a biased activation theory of selective attention.
Selective attention to affective value alters how the brain processes olfactory stimuli.
How does selective attention to affect influence sensory processing? In a functional magnetic resonance imaging investigation, when subjects were instructed to remember and rate the pleasantness of a jasmine odor, activations were greater in the medial orbito-frontal and pregenual cingulate cortex than when subjects were instructed to remember and rate the intensity of the odor. When the subjects were instructed to remember and rate the intensity, activations were greater in the inferior frontal gyrus. These top-down effects occurred not only during odor delivery but started in a preparation period after the instruction before odor delivery, and continued after termination of the odor in a short-term memory period. Thus, depending on the context in which odors are presented and whether affect is relevant, the brain prepares itself, responds to, and remembers an odor differently. These findings show that when attention is paid to affective value, the brain systems engaged to prepare for, represent, and remember a sensory stimulus are different from those engaged when attention is directed to the physical properties of a stimulus such as its intensity. This differential biasing of brain regions engaged in processing a sensory stimulus depending on whether the cognitive demand is for affect-related versus more sensory-related processing may be an important aspect of cognition and attention. This has many implications for understanding the effects not only of olfactory but also of other sensory stimuli.
Attentional modulation of affective versus sensory processing: functional connectivity and a top-down biased activation theory of selective attention.
Top-down selective attention to the affective properties of taste stimuli increases activation to the taste stimuli in the orbitofrontal cortex (OFC) and pregenual cingulate cortex (PGC), and selective attention to the intensity of the stimuli increases the activation in the insular taste cortex, but the origin of the top-down attentional biases is not known. Using psychophysiological interaction connectivity analyses, we showed that in the anterior lateral prefrontal cortex (LPFC) at Y = 53 mm the correlation with activity in OFC and PGC seed regions was greater when attention was to pleasantness compared with when attention was to intensity. Conversely, we showed that in a more posterior region of the LPFC at Y = 34 the correlation with activity in the anterior insula seed region was greater when attention was to intensity compared with when attention was to pleasantness. We also showed that correlations between areas in these separate processing streams were dependent on selective attention to affective value versus physical intensity of the stimulus. We then propose a biased activation theory of selective attention to account for the findings and contrast this with a biased competition theory of selective attention.
How cognition modulates affective responses to taste and flavor: top-down influences on the orbitofrontal and pregenual cingulate cortices.
How cognition influences the affective brain representations of the taste and flavor of a food is important not only for understanding top-down influences in the brain, but also in relation to the topical issues of appetite control and obesity. We found using functional magnetic resonance imaging that activations related to the affective value of umami taste and flavor (as shown by correlations with pleasantness ratings) in the orbitofrontal cortex were modulated by word-level descriptors. Affect-related activations to taste were modulated in a region that receives from the orbitofrontal cortex, the pregenual cingulate cortex, and to taste and flavor in another region that receives from the orbitofrontal cortex, the ventral striatum. Affect-related cognitive modulations were not found in the insular taste cortex, where the intensity but not the pleasantness of the taste was represented. We conclude that top-down language-level cognitive effects reach far down into the earliest cortical areas that represent the appetitive value of taste and flavor. This is an important way in which cognition influences the neural mechanisms that control appetite.