Matthew A. J. Apps

The Anterior Cingulate Gyrus and Social Cognition: Tracking the Motivation of Others

The anterior cingulate cortex (ACC) is implicated in a broad range of behaviors and cognitive processes, but it has been unclear what contribution, if any, the ACC makes to social behavior. We argue that anatomical and functional evidence suggests that a specific sub-region of ACC—in the gyrus (ACCg)—plays a crucial role in processing social information. We propose that the computational properties of the ACCg support a contribution to social cognition by estimating how motivated other individuals are and dynamically updating those estimates when further evidence suggests they have been erroneous. Notably this model, based on vicarious motivation and error processing, provides a unified account of neurophysiological and neuroimaging evidence that the ACCg is sensitive to costs, benefits, and errors during social interactions. Furthermore, it makes specific, testable predictions about a key mechanism that may underpin variability in socio-cognitive abilities in health and disease.

Reward Pays the Cost of Noise Reduction in Motor and Cognitive Control.

Summary Speed-accuracy trade-off is an intensively studied law governing almost all behavioral tasks across species. Here we show that motivation by reward breaks this law, by simultaneously invigorating movement and improving response precision. We devised a model to explain this paradoxical effect of reward by considering a new factor: the cost of control. Exerting control to improve response precision might itself come at a cost—a cost to attenuate a proportion of intrinsic neural noise. Applying a noise-reduction cost to optimal motor control predicted that reward can increase both velocity and accuracy. Similarly, application to decision-making predicted that reward reduces reaction times and errors in cognitive control. We used a novel saccadic distraction task to quantify the speed and accuracy of both movements and decisions under varying reward. Both faster speeds and smaller errors were observed with higher incentives, with the results best fitted by a model including a precision cost. Recent theories consider dopamine to be a key neuromodulator in mediating motivational effects of reward. We therefore examined how Parkinson’s disease (PD), a condition associated with dopamine depletion, alters the effects of reward. Individuals with PD showed reduced reward sensitivity in their speed and accuracy, consistent in our model with higher noise-control costs. Including a cost of control over noise explains how reward may allow apparent performance limits to be surpassed. On this view, the pattern of reduced reward sensitivity in PD patients can specifically be accounted for by a higher cost for controlling noise.

The role of the midcingulate cortex in monitoring others' decisions

A plethora of research has implicated the cingulate cortex in the processing of social information (i.e., processing elicited by, about, and directed toward others) and reward-related information that guides decision-making. However, it is often overlooked that there is variability in the cytoarchitectonic properties and anatomical connections across the cingulate cortex, which is indicative of functional variability. Here we review evidence from lesion, single-unit recording and functional imaging studies. Taken together, these support the claim that the processing of information that has the greatest influence on social behavior can be localized to the gyral surface of the midcingulate cortex (MCCg). We propose that the MCCg is engaged when predicting and monitoring the outcomes of decisions during social interactions. In particular, the MCCg processes statistical information that tracks the extent to which the outcomes of decisions meet goals when interacting with others. We provide a novel framework for the computational mechanisms that underpin such social information processing in the MCCg. This framework provides testable hypotheses for the social deficits displayed in autism spectrum disorders and psychopathy.

Neurocomputational mechanisms underlying subjective valuation of effort costs.

In everyday life, we have to decide whether it is worth exerting effort to obtain rewards. Effort can be experienced in different domains, with some tasks requiring significant cognitive demand and others being more physically effortful. The motivation to exert effort for reward is highly subjective and varies considerably across the different domains of behaviour. However, very little is known about the computational or neural basis of how different effort costs are subjectively weighed against rewards. Is there a common, domain-general system of brain areas that evaluates all costs and benefits? Here, we used computational modelling and functional magnetic resonance imaging (fMRI) to examine the mechanisms underlying value processing in both the cognitive and physical domains. Participants were trained on two novel tasks that parametrically varied either cognitive or physical effort. During fMRI, participants indicated their preferences between a fixed low-effort/low-reward option and a variable higher-effort/higher-reward offer for each effort domain. Critically, reward devaluation by both cognitive and physical effort was subserved by a common network of areas, including the dorsomedial and dorsolateral prefrontal cortex, the intraparietal sulcus, and the anterior insula. Activity within these domain-general areas also covaried negatively with reward and positively with effort, suggesting an integration of these parameters within these areas. Additionally, the amygdala appeared to play a unique, domain-specific role in processing the value of rewards associated with cognitive effort. These results are the first to reveal the neurocomputational mechanisms underlying subjective cost–benefit valuation across different domains of effort and provide insight into the multidimensional nature of motivation.

Plasticity in Unimodal and Multimodal Brain Areas Reflects Multisensory Changes in Self-Face Identification

Nothing provides as strong a sense of self as seeing ones face. Nevertheless, it remains unknown how the brain processes the sense of self during the multisensory experience of looking at ones face in a mirror. Synchronized visuo-tactile stimulation on ones own and anothers face, an experience that is akin to looking in the mirror but seeing anothers face, causes the illusory experience of ownership over the other persons face and changes in self-recognition. Here, we investigate the neural correlates of this enfacement illusion using fMRI. We examine activity in the human brain as participants experience tactile stimulation delivered to their face, while observing either temporally synchronous or asynchronous tactile stimulation delivered to anothers face on either a specularly congruent or incongruent location. Activity in the multisensory right temporo-parietal junction, intraparietal sulcus, and the unimodal inferior occipital gyrus showed an interaction between the synchronicity and the congruency of the stimulation and varied with the self-reported strength of the illusory experience, which was recorded after each stimulation block. Our results highlight the important interplay between unimodal and multimodal information processing for self-face recognition, and elucidate the neurobiological basis for the plasticity required for identifying with our continuously changing visual appearance.

The anterior cingulate cortex: monitoring the outcomes of others' decisions.

The ability to attribute mental states to others and understand the basis of their decisions is essential for human social interaction. A controversial theory states that this is achieved by simulating anothers information processing in ones own neural circuits. The anterior cingulate cortex (ACC) is known to play an important role in the registration of discrepancies between the predicted and actual outcomes of decisions (prediction errors).When positive and negative feedback fails altogether, the failure may also signal errors in the prediction that the outcome of that decision would be informative and guide future decisions. Does the ACC signal that an outcome is unexpectedly uninformative? When an outcome directed to others is uninformative, do we understand their mental states by simulating them in the circuits of the ACC in our own brain? The aim of our study was to test for these two possibilities in the human brain with event-related fMRI. We tested whether the ACC processes errors in the prediction of informative feedback and whether the ACC is also activated when scanned subjects process the same outcomes of anothers decisions. We show that each is processed by a separate subregion of the ACC.

‘Bodily precision’: a predictive coding account of individual differences in interoceptive accuracy

Individuals differ in their awareness of afferent information from within their bodies, which is typically assessed by a heartbeat perception measure of ‘interoceptive accuracy’ (IAcc). Neural and behavioural correlates of this trait have been investigated, but a theoretical explanation has yet to be presented. Building on recent models that describe interoception within the free energy/predictive coding framework, this paper applies similar principles to IAcc, proposing that individual differences in IAcc depend on ‘precision’ in interoceptive systems, i.e. the relative weight accorded to ‘prior’ representations and ‘prediction errors’ (that part of incoming interoceptive sensation not accounted for by priors), at various levels within the cortical hierarchy and between modalities. Attention has the effect of optimizing precision both within and between sensory modalities. Our central assumption is that people with high IAcc are able, with attention, to prioritize interoception over other sensory modalities and can thus adjust the relative precision of their interoceptive priors and prediction errors, where appropriate, given their personal history. This characterization explains key findings within the interoception literature; links results previously seen as unrelated or contradictory; and may have important implications for understanding cognitive, behavioural and psychopathological consequences of both high and low interoceptive awareness. This article is part of the themed issue ‘Interoception beyond homeostasis: affect, cognition and mental health’.

The role of cognitive effort in subjective reward devaluation and risky decision-making

Motivation is underpinned by cost-benefit valuations where costs—such as physical effort or outcome risk—are subjectively weighed against available rewards. However, in many environments risks pertain not to the variance of outcomes, but to variance in the possible levels of effort required to obtain rewards (effort risks). Moreover, motivation is often guided by the extent to which cognitive—not physical—effort devalues rewards (effort discounting). Yet, very little is known about the mechanisms that underpin the influence of cognitive effort risks or discounting on motivation. We used two cost-benefit decision-making tasks to probe subjective sensitivity to cognitive effort (number of shifts of spatial attention) and to effort risks. Our results show that shifts of spatial attention when monitoring rapidly presented visual stimuli are perceived as effortful and devalue rewards. Additionally, most people are risk-averse, preferring safe, known amounts of effort over risky offers. However, there was no correlation between their effort and risk sensitivity. We show for the first time that people are averse to variance in the possible amount of cognitive effort to be exerted. These results suggest that cognitive effort sensitivity and risk sensitivity are underpinned by distinct psychological and neurobiological mechanisms.

Distinct Subtypes of Apathy Revealed by the Apathy Motivation Index

Apathy is a debilitating but poorly understood disorder characterized by a reduction in motivation. As well as being associated with several brain disorders, apathy is also prevalent in varying degrees in healthy people. Whilst many tools have been developed to assess levels of apathy in clinical disorders, surprisingly there are no measures of apathy suitable for healthy people. Moreover, although apathy is commonly comorbid with symptoms of depression, anhedonia and fatigue, how and why these symptoms are associated is unclear. Here we developed the Apathy-Motivation Index (AMI), a brief self-report index of apathy and motivation. Using exploratory factor analysis (in a sample of 505 people), and then confirmatory analysis (in a different set of 479 individuals), we identified subtypes of apathy in behavioural, social and emotional domains. Latent profile analyses showed four different profiles of apathy that were associated with varying levels of depression, anhedonia and fatigue. The AMI is a novel and reliable measure of individual differences in apathy and might provide a useful means of probing different mechanisms underlying sub-clinical lack of motivation in otherwise healthy individuals. Moreover, associations between apathy and comorbid states may be reflective of problems in different emotional, social and behavioural domains.

The different faces of one's self: An fMRI study into the recognition of current and past self-facial appearances

Mirror self-recognition is often considered as an index of self-awareness. Neuroimaging studies have identified a neural circuit specialised for the recognition of ones own current facial appearance. However, faces change considerably over a lifespan, highlighting the necessity for representations of ones face to continually be updated. We used fMRI to investigate the different neural circuits involved in the recognition of the childhood and current, adult, faces of ones self. Participants viewed images of either their own face as it currently looks morphed with the face of a familiar other or their childhood face morphed with the childhood face of the familiar other. Activity in areas which have a generalised selectivity for faces, including the inferior occipital gyrus, the superior parietal lobule and the inferior temporal gyrus, varied with the amount of current self in an image. Activity in areas involved in memory encoding and retrieval, including the hippocampus and the posterior cingulate gyrus, and areas involved in creating a sense of body ownership, including the temporo-parietal junction and the inferior parietal lobule, varied with the amount of childhood self in an image. We suggest that the recognition of ones own past or present face is underpinned by different cognitive processes in distinct neural circuits. Current self-recognition engages areas involved in perceptual face processing, whereas childhood self-recognition recruits networks involved in body ownership and memory processing.