Integration of emotion and cognition in the lateral prefrontal cortex

doi:10.1073/pnas.062381899

Integration of emotion and cognition in the lateral prefrontal cortex

Departments of ^*Psychology and ^‡Radiology, Neurology, Neurobiology, and Psychology, Washington University, One Brookings Drive, St. Louis, MO 63130

Edited by Michael I. Posner, Weill Medical College of Cornell University, New York, NY, and approved January 14, 2002 (received for review July 23, 2001)

Abstract

We used functional MRI to test the hypothesis that emotional states can selectively influence cognition-related neural activity in lateral prefrontal cortex (PFC), as evidence for an integration of emotion and cognition. Participants (n = 14) watched short videos intended to induce emotional states (pleasant/approach related, unpleasant/withdrawal related, or neutral). After each video, the participants were scanned while performing a 3-back working memory task having either words or faces as stimuli. Task-related neural activity in bilateral PFC showed a predicted pattern: an Emotion × Stimulus crossover interaction, with no main effects, with activity predicting task performance. This highly specific result indicates that emotion and higher cognition can be truly integrated, i.e., at some point of processing, functional specialization is lost, and emotion and cognition conjointly and equally contribute to the control of thought and behavior. Other regions in lateral PFC showed hemispheric specialization for emotion and for stimuli separately, consistent with a hierarchical and hemisphere-based mechanism of integration.

Footnotes

↵ † To whom reprint requests should be addressed. E-mail: tbraver{at}artsci.wustl.edu.
This paper was submitted directly (Track II) to the PNAS office.
↵ § Recent work suggests that an approach–withdrawal distinction best explains the prefrontal emotion-related hemispheric asymmetries (10–12, 34). Perhaps the strongest evidence is that induced anger—a subjectively unpleasant but approach-motivated emotion—is associated with greater left frontal activity, arguing strongly for an approach–withdrawal account of the prefrontal asymmetry (12). This account might also explain some apparent exceptions (36, 37).
↵ ‖ This procedure is obviously appropriate for identifying task-specific activations but is not clearly so for identifying the direction of emotion-specific activity within a task-related network; see Discussion. The identification of emotion–cognition interactions and hemispheric differences is uninfluenced by this consideration.
↵ ¶ The model is a generalization from diverse data. It might be argued that emotion-related activation should interfere with cognitive activity in the same brain area (for discussion, see ref. 9; J.R.G., unpublished work). However, the opposite behavioral effect is observed (8). If emotion-related activity was due to an independent source of activation within a region (i.e., competing with on-going cognitive activity), it should produce crosstalk or dual-task interference. If emotion modulated ongoing activity, it could produce enhancement.
Abbreviations:

PFC,

prefrontal cortex;

fMRI,

functional MRI;

ROI,

region of interest