Ventromedial prefrontal-subcortical systems and the generation of affective meaning - PubMed (original) (raw)

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Ventromedial prefrontal-subcortical systems and the generation of affective meaning

Mathieu Roy et al. Trends Cogn Sci. 2012 Mar.

Abstract

The ventromedial prefrontal cortex (vmPFC) comprises a set of interconnected regions that integrate information from affective sensory and social cues, long-term memory, and representations of the 'self'. Alhough the vmPFC is implicated in a variety of seemingly disparate processes, these processes are organized around a common theme. The vmPFC is not necessary for affective responses per se, but is critical when affective responses are shaped by conceptual information about specific outcomes. The vmPFC thus functions as a hub that links concepts with brainstem systems capable of coordinating organism-wide emotional behavior, a process we describe in terms of the generation of affective meaning, and which could explain the common role played by the vmPFC in a range of experimental paradigms.

Copyright © 2012 Elsevier Ltd. All rights reserved.

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Figures

Figure 1

Figure 1

Convergence across fields: VMPFC across social, cognitive, affective, and clinical domains. (a) Dorsal anterior/mid cingulate activations re sympathetic activity during emotional/cognitive tasks and exercise [1]. (b) pgACC, sgACC and rostral MPFC activity correlations with parasympathetic/anti-sympathetic activity; top-left: negative correlation with increases in heart rate during a working memory task [90]; bottom-left: decreases in skin conductance during relaxation [91]; right: results from a meta analysis on brain activations associated with high-frequency heart rate variability during emotional and cognitive tasks (red: emotional>cognitive; yellow: emotional = cognitive) [92] (c) left: Stress-related correlates of natural killer (NK) cells increase [93]; right: grief-evoking words correlates with IL-6 [94]. (d) vmPFC and rdACC activity negatively and positively correlates with conditioned SCR during fear conditioning and revearsal [4]; (e) vmPFC activation in meta-analyses of fear extinction (red), placebo (green) and reappraisal (blue). (f) left: vmPFC/sgACC activity during extinction recall [74]; right: vmPFC/sgACC activity (blue) during reappraisal of conditioned fear [52]. (g) rdACC activity in instructed fear paradigms [50]. (h) Positive (left: sgACC/Nacc) and negative (right: rdACC/amygdala) mediators of successful reappraisal of negative emotions [54] (i) left: opioids activate MPFC [95]; right: placebo activates a common sub-region in rACC [95]. (j) Positive (rdACC, thalamus, PAG) and negative (vmPFC) mediators of heart rate increases during social evaluative threat [65]. (k) vmPFC/mOFC activation for valued vs devalued food [46]. (l) Common coding of value of money, trinkets and snacks [67]. (m) left: integration of conceptual knowledge and value representations during decision-making; right: more rostral activity specific to explicit conceptual knowledge [78]. (n) Relative coding of value in the vmPFC [49]. (o) Goal value: healthiness of food for successful dieters or taste of food for unsuccessful dieters [73]. (p) temporal discounting of subjective value [72]. (q) left: same odor labeled as “cheddar cheese” vs “sweat” [68]; right: same wine labeled as “cheap” vs “pricey” [70]. (r) Convergence (red) of activations related to autobiographical memory (light blue), theory of mind (dark blue) and default-mode network (green) [96]. (s) Activity related to imagining past or future events or remembering past events [97]. (t) Activity related to self-reflection [98]. (u) Reduced activation during recall of extinction in PTSD patients vs controls [38]. (v) Hypo- (blue) and hyper- (red) activations in response to aversive stimuli in PTSD patients vs controls [10]. (w) Reduced cerebral blood flow (CBF) in depressed patients vs controls [79]. sgACC: subgenual anterior cingulate cortex, pgACC: perigenual anterior cingulate cortex, rACC: rostral ACC, rdACC: rostro-dorsal anterior cingulate cortex, MPFC: medial prefrontal cortex, vmPFC: ventromedial prefrontal cortex, mOFC: medial orbitofrontal cortex, Nacc: nucleus accumbens, PAG: periaqueductal gray matter SCR: skin conductance response, IL-6: interleukin -6.

Figure 2

Figure 2

A meta-analytic view: Convergence of meaning-related processes in vmPFC. (a) Results of an automated reverse inference meta-analysis using Neurosynth (

neurosynth.org

). Color maps display the probability terms related to vmPFC’s functions given observed activation (P term|activation), (b) Results of a factor analysis with two factors on the meta-analytic reverse inference patterns of activation for the terms “default mode”, “memory”, “self”, “social cognition/mentalizing”, “reward”, “autonomic/endocrine”, “emotion” and “pain”. Top panel: Factor loadings associated with each term. “Emotion”, “autonomic/endocrine” and “reward” strongly loaded on factor 1, “memory” and “default mode” strongly loaded on factor 2, “self” and “social cognition/mentalizing” loaded on both factors, “pain” did not substantially load on any factor. Bottom panel: Spatial extent of the regions associated with the two factors (including voxels with loadings in the top 1% of values across the brain). Factor 1 comprised a large ventro-caudal portion of the vmPFC, subcortical structures (amygdala, striatum and midbrain), right insula and left lateral prefrontal cortex. Factor 2 comprised a more rostral and dorsal portion of the vmPFC, the posterior cingulate cortex (PCC) and bilateral intraparietal sulcii (IPS). The specific searches that defined each category were as follows. In the list below, |, &, and ~ indicate logical OR, AND, and NOT, respectively. * indicates a wildcard including all words beginning with the stem preceding the star. Default mode: “default | resting state | dmn | default mode”. Memory: Average of “episod*” “autobiograph*” “retriev* | recollect*”. Self: “(self | subjective)”. Social cognition/mentalizing: “empath* | theory.of.mind | tom | mentaliz* | trait | (inference & others)”. Emotion: “emotion* | mood | valence | arousal | affective”. Reward: “(reward* | monet* | gain | cocaine | eating | reinforc* | incent* | love | joy | (positive & hedonic) | (positive & emotion) | (positive & affect)) &~ (negative & emotion) ”. Autonomic/endocrine: “autonomic* | scr | hr | cortisol | conductance | heart”. Pain: “pain* | noxious | nocicept*”. Additional details can be found in the Online Supplementary Materials.

Figure I

Figure I

Subdivisions and connectivity of the medial prefrontal cortex. (a) Four functionally distinct zones include ventromedial prefrontal cortex (vmPFC), rostral dorsal anterior cingulate (rdACC), dorsal anterior cingulate (dACC), and dorsomedial prefrontal cortex (dmPFC). We envision meaning construction as occurring principally in vmPFC and rdACC, with substantial contributions from dmPFC. To illustrate the differential connectivity of the vmPFC and dACC zones, ‘seed’ regions were selected based on the peak activation frequencies across the 1,669 studies and 8 domain areas summarized in this review. Areas significantly co-activated with each seed region are shown at the right (see Supplementary Online Materials for details). The dACC (red) and vmPFC (blue) regions co-activated with distinct brain networks. Additional subcortical connectivity with vmPFC was apparent below the stringent thresholds used here (P < .05 corrected). rdACC (purple) showed co-activation with both networks, and particularly strong co-activation with periaqueductal gray (PAG) and other subcortical areas. (b) Further exploration of medial prefrontal co-activation with subcortical regions. For each of the six areas shown, small ‘seed’ regions were placed in the subcortical area, and co-activated areas in the medial prefrontal cortex are shown (P < .0001). rdACC is co-activated with each area, with particularly strong co-activation with dorsal PAG and raphe nuclei associated with active responses to threat, suggesting a possible homology with prelimbic cortex in rats. (c) Location of prelimbic and infralimbic cortices in rats, adapted from [99]. (d) A meta-analytic summary of 138 PET and fMRI studies of positive and negative emotional experience (374 experimental contrasts, selected from a database of 234 studies of emotion described in [88]). Colored regions indicate areas with significantly greater density of activations related to positive (yellow) and negative (blue) emotional experience. Positive emotions more consistently activate the vmPFC, posterior cingulate cortex, ventral striatum and supplementary motor areas, and pre-supplementary motor area. Negative emotions more consistently activate the PAG, rdACC, dmPFC and deep cerebellar areas.

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