Micah Allen

Cognitive-affective neural plasticity following active-controlled mindfulness intervention.

Mindfulness meditation is a set of attention-based, regulatory, and self-inquiry training regimes. Although the impact of mindfulness training (MT) on self-regulation is well established, the neural mechanisms supporting such plasticity are poorly understood. MT is thought to act through interoceptive salience and attentional control mechanisms, but until now conflicting evidence from behavioral and neural measures renders difficult distinguishing their respective roles. To resolve this question we conducted a fully randomized 6 week longitudinal trial of MT, explicitly controlling for cognitive and treatment effects with an active-control group. We measured behavioral metacognition and whole-brain blood oxygenation level-dependent (BOLD) signals using functional MRI during an affective Stroop task before and after intervention in healthy human subjects. Although both groups improved significantly on a response-inhibition task, only the MT group showed reduced affective Stroop conflict. Moreover, the MT group displayed greater dorsolateral prefrontal cortex responses during executive processing, consistent with increased recruitment of top-down mechanisms to resolve conflict. In contrast, we did not observe overall group-by-time interactions on negative affect-related reaction times or BOLD responses. However, only participants with the greatest amount of MT practice showed improvements in response inhibition and increased recruitment of dorsal anterior cingulate cortex, medial prefrontal cortex, and right anterior insula during negative valence processing. Our findings highlight the importance of active control in MT research, indicate unique neural mechanisms for progressive stages of mindfulness training, and suggest that optimal application of MT may differ depending on context, contrary to a one-size-fits-all approach.

Sociocultural patterning of neural activity during self-reflection

Western cultures encourage self-construals independent of social contexts, whereas East Asian cultures foster interdependent self-construals that rely on how others perceive the self. How are culturally specific self-construals mediated by the human brain? Using functional magnetic resonance imaging, we monitored neural responses from adults in East Asian (Chinese) and Western (Danish) cultural contexts during judgments of social, mental and physical attributes of themselves and public figures to assess cultural influences on self-referential processing of personal attributes in different dimensions. We found that judgments of self vs a public figure elicited greater activation in the medial prefrontal cortex (mPFC) in Danish than in Chinese participants regardless of attribute dimensions for judgments. However, self-judgments of social attributes induced greater activity in the temporoparietal junction (TPJ) in Chinese than in Danish participants. Moreover, the group difference in TPJ activity was mediated by a measure of a cultural value (i.e. interdependence of self-construal). Our findings suggest that individuals in different sociocultural contexts may learn and/or adopt distinct strategies for self-reflection by changing the weight of the mPFC and TPJ in the social brain network.

The balanced mind: the variability of task-unrelated thoughts predicts error-monitoring

Self-generated thoughts unrelated to ongoing activities, also known as “mind-wandering,” make up a substantial portion of our daily lives. Reports of such task-unrelated thoughts (TUTs) predict both poor performance on demanding cognitive tasks and blood-oxygen-level-dependent (BOLD) activity in the default mode network (DMN). However, recent findings suggest that TUTs and the DMN can also facilitate metacognitive abilities and related behaviors. To further understand these relationships, we examined the influence of subjective intensity, ruminative quality, and variability of mind-wandering on response inhibition and monitoring, using the Error Awareness Task (EAT). We expected to replicate links between TUT and reduced inhibition, and explored whether variance in TUT would predict improved error monitoring, reflecting a capacity to balance between internal and external cognition. By analyzing BOLD responses to subjective probes and the EAT, we dissociated contributions of the DMN, executive, and salience networks to task performance. While both response inhibition and online TUT ratings modulated BOLD activity in the medial prefrontal cortex (mPFC) of the DMN, the former recruited a more dorsal area implying functional segregation. We further found that individual differences in mean TUTs strongly predicted EAT stop accuracy, while TUT variability specifically predicted levels of error awareness. Interestingly, we also observed co-activation of salience and default mode regions during error awareness, supporting a link between monitoring and TUTs. Altogether our results suggest that although TUT is detrimental to task performance, fluctuations in attention between self-generated and external task-related thought is a characteristic of individuals with greater metacognitive monitoring capacity. Achieving a balance between internally and externally oriented thought may thus aid individuals in optimizing their task performance.

Anterior insula coordinates hierarchical processing of tactile mismatch responses

The body underlies our sense of self, emotion, and agency. Signals arising from the skin convey warmth, social touch, and the physical characteristics of external stimuli. Surprising or unexpected tactile sensations can herald events of motivational salience, including imminent threats (e.g., an insect bite) and hedonic rewards (e.g., a caressing touch). Awareness of such events is thought to depend upon the hierarchical integration of body-related mismatch responses by the anterior insula. To investigate this possibility, we measured brain activity using functional magnetic resonance imaging, while healthy participants performed a roving tactile oddball task. Mass-univariate analysis demonstrated robust activations in limbic, somatosensory, and prefrontal cortical areas previously implicated in tactile deviancy, body awareness, and cognitive control. Dynamic Causal Modelling revealed that unexpected stimuli increased the strength of forward connections along a caudal to rostral hierarchy—projecting from thalamic and somatosensory regions towards insula, cingulate and prefrontal cortices. Within this ascending flow of sensory information, the AIC was the only region to show increased backwards connectivity to the somatosensory cortex, augmenting a reciprocal exchange of neuronal signals. Further, participants who rated stimulus changes as easier to detect showed stronger modulation of descending PFC to AIC connections by deviance. These results suggest that the AIC coordinates hierarchical processing of tactile prediction error. They are interpreted in support of an embodied predictive coding model where AIC mediated body awareness is involved in anchoring a global neuronal workspace.

From cognitivism to autopoiesis: towards a computational framework for the embodied mind

Predictive processing (PP) approaches to the mind are increasingly popular in the cognitive sciences. This surge of interest is accompanied by a proliferation of philosophical arguments, which seek to either extend or oppose various aspects of the emerging framework. In particular, the question of how to position predictive processing with respect to enactive and embodied cognition has become a topic of intense debate. While these arguments are certainly of valuable scientific and philosophical merit, they risk underestimating the variety of approaches gathered under the predictive label. Here, we first present a basic review of neuroscientific, cognitive, and philosophical approaches to PP, to illustrate how these range from solidly cognitivist applications—with a firm commitment to modular, internalistic mental representation—to more moderate views emphasizing the importance of ‘body-representations’, and finally to those which fit comfortably with radically enactive, embodied, and dynamic theories of mind. Any nascent predictive processing theory (e.g., of attention or consciousness) must take into account this continuum of views, and associated theoretical commitments. As a final point, we illustrate how the Free Energy Principle (FEP) attempts to dissolve tension between internalist and externalist accounts of cognition, by providing a formal synthetic account of how internal ‘representations’ arise from autopoietic self-organization. The FEP thus furnishes empirically productive process theories (e.g., predictive processing) by which to guide discovery through the formal modelling of the embodied mind.

Unexpected arousal modulates the influence of sensory noise on confidence

Human perception is invariably accompanied by a graded feeling of confidence that guides metacognitive awareness and decision-making. It is often assumed that this arises solely from the feed-forward encoding of the strength or precision of sensory inputs. In contrast, interoceptive inference models suggest that confidence reflects a weighted integration of sensory precision and expectations about internal states, such as arousal. Here we test this hypothesis using a novel psychophysical paradigm, in which unseen disgust-cues induced unexpected, unconscious arousal just before participants discriminated motion signals of variable precision. Across measures of perceptual bias, uncertainty, and physiological arousal we found that arousing disgust cues modulated the encoding of sensory noise. Furthermore, the degree to which trial-by-trial pupil fluctuations encoded this nonlinear interaction correlated with trial level confidence. Our results suggest that unexpected arousal regulates perceptual precision, such that subjective confidence reflects the integration of both external sensory and internal, embodied states. DOI: http://dx.doi.org/10.7554/eLife.18103.001

The Brain Basis for Misophonia

Summary Misophonia is an affective sound-processing disorder characterized by the experience of strong negative emotions (anger and anxiety) in response to everyday sounds, such as those generated by other people eating, drinking, chewing, and breathing [1, 2, 3, 4, 5, 6, 7, 8]. The commonplace nature of these sounds (often referred to as “trigger sounds”) makes misophonia a devastating disorder for sufferers and their families, and yet nothing is known about the underlying mechanism. Using functional and structural MRI coupled with physiological measurements, we demonstrate that misophonic subjects show specific trigger-sound-related responses in brain and body. Specifically, fMRI showed that in misophonic subjects, trigger sounds elicit greatly exaggerated blood-oxygen-level-dependent (BOLD) responses in the anterior insular cortex (AIC), a core hub of the “salience network” that is critical for perception of interoceptive signals and emotion processing. Trigger sounds in misophonics were associated with abnormal functional connectivity between AIC and a network of regions responsible for the processing and regulation of emotions, including ventromedial prefrontal cortex (vmPFC), posteromedial cortex (PMC), hippocampus, and amygdala. Trigger sounds elicited heightened heart rate (HR) and galvanic skin response (GSR) in misophonic subjects, which were mediated by AIC activity. Questionnaire analysis showed that misophonic subjects perceived their bodies differently: they scored higher on interoceptive sensibility than controls, consistent with abnormal functioning of AIC. Finally, brain structural measurements implied greater myelination within vmPFC in misophonic individuals. Overall, our results show that misophonia is a disorder in which abnormal salience is attributed to particular sounds based on the abnormal activation and functional connectivity of AIC.

Active inference, enactivism and the hermeneutics of social cognition

We distinguish between three philosophical views on the neuroscience of predictive models: predictive coding (associated with internal Bayesian models and prediction error minimization), predictive processing (associated with radical connectionism and ‘simple’ embodiment) and predictive engagement (associated with enactivist approaches to cognition). We examine the concept of active inference under each model and then ask how this concept informs discussions of social cognition. In this context we consider Frith and Friston’s proposal for a neural hermeneutics, and we explore the alternative model of enactivist hermeneutics.

Neurocognitive evidence for mental imagery-driven hypoalgesic and hyperalgesic pain regulation

Mental imagery has the potential to influence perception by directly altering sensory, cognitive, and affective brain activity associated with imagined content. While it is well established that mental imagery can both exacerbate and alleviate acute and chronic pain, it is currently unknown how imagery mechanisms regulate pain perception. For example, studies to date have been unable to determine whether imagery effects depend upon a general redirection of attention away from pain or focused attentional mechanisms. To address these issues, we recorded subjective, behavioral and ERP responses using 64-channel EEG while healthy human participants applied a mental imagery strategy to decrease or increase pain sensations. When imagining a glove covering the forearm, participants reported decreased perceived intensity and unpleasantness, classified fewer high-intensity stimuli as painful, and showed a more conservative response bias. In contrast, when imagining a lesion on the forearm, participants reported increased pain intensity and unpleasantness, classified more low-intensity stimuli as painful, and displayed a more liberal response bias. Using a mass-univariate approach, we further showed differential modulation of the N2 potentials across conditions, with inhibition and facilitation respectively increasing and decreasing N2 amplitudes between 122 and 180 ms. Within this time window, source localization associated inhibiting vs. facilitating pain with neural activity in cortical regions involved in cognitive inhibitory control and in the retrieval of semantic information (i.e., right inferior frontal and temporal regions). In contrast, the main sources of neural activity associated with facilitating vs. inhibiting pain were identified in cortical regions typically implicated in salience processing and emotion regulation (i.e., left insular, inferior-middle frontal, supplementary motor and precentral regions). Overall, these findings suggest that the content of a mental image directly alters pain-related decision and evaluative processing to flexibly produce hypoalgesic and hyperalgesic outcomes.

Noradrenaline blockade specifically enhances metacognitive performance

Impairments in metacognition, the ability to accurately report one’s performance, are common in patients with psychiatric disorders, where a putative neuromodulatory dysregulation provides the rationale for pharmacological interventions. Previously, we have shown how unexpected arousal modulates metacognition (Allen et al., 2016). Here, we report a double-blind, placebo-controlled, study that examined specific effects of noradrenaline and dopamine on both metacognition and perceptual decision making. Signal theoretic analysis of a global motion discrimination task with adaptive performance staircasing revealed that noradrenergic blockade (40 mg propranolol) significantly increased metacognitive performance (type-II area under the curve, AUROC2), but had no impact on perceptual decision making performance. Blockade of dopamine D2/3 receptors (400 mg amisulpride) had no effect on either metacognition or perceptual decision making. Our study is the first to show a pharmacological enhancement of metacognitive performance, in the absence of any effect on perceptual decision making. This enhancement points to a regulatory role for noradrenergic neurotransmission in perceptual metacognition. DOI: http://dx.doi.org/10.7554/eLife.24901.001