Emotional processing in anterior cingulate and medial prefrontal cortex

Abstract

Negative emotional stimuli activate a broad network of brain regions, including the medial prefrontal (mPFC) and anterior cingulate (ACC) cortices. An early influential view dichotomized these regions into dorsal-caudal cognitive and ventral-rostral affective subdivisions. In this review, we examine a wealth of recent research on negative emotions in animals and humans, using the example of fear or anxiety, and conclude that, contrary to the traditional dichotomy, both subdivisions make key contributions to emotional processing. Specifically, dorsal-caudal regions of the ACC and mPFC are involved in appraisal and expression of negative emotion, whereas ventral-rostral portions of the ACC and mPFC have a regulatory role with respect to limbic regions involved in generating emotional responses. Moreover, this new framework is broadly consistent with emerging data on other negative and positive emotions.

Figure I

Parcellation of anterior cingulate cortex (ACC) and medial prefrontal cortex (mPFC) subregions. Abbreviations: sg=subgenual, pg=pregenual, vm=ventromedial, rm=rostromedial, dm=dorsomedial, ad=anterior dorsal, pd=posterior dorsal, SMA=supplementary motor area.

Figure 1

Activation foci associated with fear and its regulation. Predominantly dorsal ACC/mPFC activations are seen during classical (Pavlovian) fear conditioning (A), as well as during instructed fear paradigms, which circumvent fear learning (B). Likewise, sympathetic nervous system activity correlates positively primarily with dorsal ACC/mPFC regions and negatively primarily with ventral ACC/mPFC regions, supporting a role for the dorsal ACC/mPFC in fear expression (C). During within-session extinction, activation is seen in both the dorsal and ventral ACC/mPFC (D), while during subsequent delayed recall and expression of the extinction memory, when the imaging data is less confounded by residual expression of fear responses, activation is primarily in the ventral ACC/mPFC (E). Information of the studies selected for this and all following peak voxel plots can be found in the online supplemental materials.

Figure 2

(A) Emotional conflict across a variety of experimental paradigms is associated with activation in the dorsal ACC/mPFC. (B) Decreasing negative emotion through reappraisal is associated with preferential activation of the dorsal ACC/mPFC. Targets of amygdalar connectivity during tasks involving appraisal/expression (C) or regulation (D) of negative emotion. Positive connectivity is seen primarily during appraisal/expression tasks, and most heavily in the dorsal ACC/mPFC. By contrast, negative connectivity is seen most heavily in the ventral ACC/mPFC across both appraisal/expression and regulation tasks. These connectivity findings are therefore consistent with the dorsoventral functional-anatomical parcellation of the ACC/mPFC derived from activation analyses.

Figure 3

A graphical depiction of the ACC/mPFC functional model aligned across an appraisal/expression versus regulation dimension for negative emotion. The imperfect separation of these functions across the dorsal and ventral ACC/mPFC noted in the reviewed studies is represented schematically as an intermixing of red (appraisal/expression) and blue (regulation) circles.