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

Abstract

PrefaceIt has been argued that emotion, pain, and cognitive control are functionally segregated in distinct subdivisions of the cingulate cortex. But recent observations encourage a fundamentally different view. Imaging studies indicate that negative affect, pain, and cognitive control activate an overlapping region of dorsal cingulate, the anterior midcingulate cortex (aMCC). Anatomical studies reveal that aMCC constitutes a hub where information about reinforcers can be linked to motor centers responsible for expressing affect and executing goal-directed behavior. Computational modeling 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 dorsal cingulate's contribution to negative affect and pain. † Manuscript Correspondence: Alexander J. Shackman (shackman@wisc.edu) or Tim V. Salomons (tvsalomons@gmail.com) Competing Interests StatementThe authors declare no competing financial interests. NIH Public Access Author ManuscriptNat Rev Neurosci. Author manuscript; available in PMC 2011 September 1. IntroductionIn humans and other primates, the cingulate, a thick belt of cortex encircling the corpus callosum, is one of the most prominent features on the mesial surface of the brain ( Figure 1a). Early research suggested that the rostral cingulate gyrus (Brodmann's 'precingulate' 1 ; architectonic areas 24, 25, 32, and 33) plays a key role in affect and motivation (Figure 1b) 2 .More recent research has enlarged the breadth of functions ascribed to this region; in addition to emotion 3 , the rostral cingulate plays a central role in contemporary models of pain 4, 5 and cognitive control 6,7 . Work in these three basic domains has, in turn, strongly influenced prominent models of social behavior 8 , psychopathology [9][10][11] , and neurological disorders 12 .Despite this progress, key questions about the functional organization and significance of activity in the rostral cingulate remain unresolved. Perhaps the most basic question is whether emotion, pain, and cognitive control are segregated into distinct subdivisions of the rostral cingulate or are instead integrated in a common region. In a pair of landmark reviews, Devinsky et al. 13 and Bush et al. 14 marshaled a broad range of functional imaging, electrophysiological, and anatomical data in support of functional segregation, arguing that the anterior cingulate cortex (ACC or 'rostral' ACC) is specialized for affective processes, whereas the midcingulate cortex (MCC or 'dorsal' ACC) is specialized for cognitive processes (Figure 1c, 1d). Subsequent meta-analyses of imaging studies have provided some support for this claim 15 .Although the segregationist model remains highly influential, new data suggests that it is no longer tenable. For instance, recent imaging data implicate MCC in the regulation of autonomic activity 16,17 and the perception and production of emotion 3,18 . Likewise, neuronal recordings demonstrate that MCC is responsive to ...

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