Journal Article

The integration of negative affect, pain and cognitive control in the cingulate cortex

Salomons, Tim V., Davidson, Richard J., Shackman, Alexander J., Fox, Andrew S., Slagter, Heleen A., Winter, Jameel J.

2011

Overview

Key Points The rostral cingulate cortex occupies a central position in models of emotion, pain and cognitive control. Work in these domains has strongly influenced recent models of social behaviour and psychopathology. The segregationist view: it has been argued that the rostral cingulate cortex is functionally segregated into affective and cognitive divisions. Although this view remains influential, new data suggest that it is no longer tenable. Robust links have been forged between the anterior subdivision of the midcingulate cortex (aMCC) and negative affect (as with the anticipation and delivery of pain), leading some to speculate that aMCC implements a 'domain-general' process that is integral to negative affect, pain and cognitive control. Physiological evidence: a meta-analysis of activation foci from functional imaging studies of negative affect, pain and cognitive control revealed that aMCC is consistently activated by all three domains, refuting claims that cognition and emotion are strictly segregated in the cingulate. Anatomical evidence: aMCC is characterized by substantial connections with subcortical regions involved in negative affect and pain (the spinothalamic system, periaqueductal grey, amygdala, nucleus accumbens and substantia nigra). Unlike other cortical 'hot spots' for emotion, aMCC harbours the rostral cingulate zone (RCZ) — a premotor area that is heavily interconnected with other motor centres (including the facial nucleus). Functional evidence: measures of negative affect, pain and cognitive control exhibit convergent functional properties. These measures covary with one another and are amplified in similar ways by uncertainty about responses and outcomes. The adaptive control hypothesis: the core function common to negative affect, pain and cognitive control is the need to determine an optimal course of action in the face of uncertainty — that is, to exert 'adaptive control'. We suggest that aMCC implements adaptive control by using information about punishment to bias responding in situations where the optimal course of action is uncertain or entails response competition. Further evidence: pain-responsive MCC neurons are activated by the anticipation of pain, activated during instrumental escape from pain and are sensitive to manipulations of certainty and conflict. Lesions of aMCC alter how threat modulates instrumental behaviour. aMCC activity during aversively motivated learning is predicted by computational models of control and reinforcement learning. These data encourage a broader perspective on the functional significance of cingulate activity, one that recognizes that aMCC did not evolve to optimize performance on laboratory measures of 'cold' cognition. The data that we have surveyed are consistent with the possibility that the contribution of aMCC to measures of cognitive control stems from its older role in regulating 'hot' behaviours. The adaptive control hypothesis provides a clear roadmap to the most profitable avenues for understanding the contribution of aMCC to negative affect and pain. In this Review, Shackman and colleagues challenge claims that emotion and cognition are functionally segregated in the cingulate cortex. They show that negative affect, pain and cognitive control activate a common subdivision of the cingulate cortex, and propose that this region uses punishment-related information to optimize goal-directed behaviour. It has been argued that emotion, pain and cognitive control are functionally segregated in distinct subdivisions of the cingulate cortex. However, recent observations encourage a fundamentally different view. Imaging studies demonstrate that negative affect, pain and cognitive control activate an overlapping region of the dorsal cingulate — the anterior midcingulate cortex (aMCC). Anatomical studies reveal that the aMCC constitutes a hub where information about reinforcers can be linked to motor centres responsible for expressing affect and executing goal-directed behaviour. Computational modelling and other kinds of evidence suggest that this intimacy reflects control processes that are common to all three domains. These observations compel a reconsideration of the dorsal cingulate's contribution to negative affect and pain.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 631/378/1457 / 631/378/2649/2150 / 692/698/1688/64 / Adult and adolescent clinical studies / Animal Genetics and Genomics / Animals / Behavioral Sciences / Biological and medical sciences / Biological Techniques / Biomedical and Life Sciences / Biomedicine / Brain research / Cingulate cortex / Cognition / Cognition & reasoning / Cognition - physiology / Emotions - physiology / Fundamental and applied biological sciences. Psychology / Gyrus Cinguli - physiology / Humans / Hypotheses / Medical sciences / Neurobiology / Neurosciences / Pain / Pain - physiopathology / Pain - psychology / Physiological aspects / Physiology / Psychology. Psychoanalysis. Psychiatry / Psychopathology. Psychiatry / Psychoses / Reinforcement, Psychology / review-article / Schizophrenia / Somesthesis and somesthetic pathways (proprioception, exteroception, nociception); interoception; electrolocation. Sensory receptors / Vertebrates: nervous system and sense organs