Dissociation in human prefrontal cortex of affective influences on working memory-related activity - PubMed (original) (raw)

William M Perlstein et al. Proc Natl Acad Sci U S A. 2002.

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Abstract

Although neural activity associated with emotion is becoming better understood, the influence of affective parameters on brain activity reflecting cognitive functioning in humans remains poorly characterized. We examined affective influences on working memory (WM) and tested the hypotheses that (i) dorsolateral prefrontal cortex (DLPFC) activity reflecting WM is influenced by the emotion-evoking qualities of task-relevant stimuli, but only when brought "on-line" by task demands, and (ii) DLPFC and orbitofrontal cortex (OFC) activities are inversely related as a function of emotional valence. Participants performed two tasks while event-related functional MRI measured brain activity; one task required active maintenance of stimulus representations in WM, and the other task required target detection responses with no demand for WM. Stimuli were standardized emotional (pleasant and unpleasant) and neutral pictures. Emotional stimuli differentially influenced DPFC and OFC activity during WM; DLPFC was influenced by emotional valence, enhanced by pleasant and reduced by unpleasant, compared to neutral stimuli, only when task conditions required WM. OFC was valence-sensitive during both tasks, greater to arousing than neutral stimuli when WM demand was low and in inverse relationship to DLPFC with high WM demand. Further, DLPFC and OFC activities are inversely related with respect to emotional valence during the WM task. The results are consistent with the hypothesis that the intrinsic valence of task-relevant stimuli maintained in WM modulates DLPFC activity but only when the DLPFC is required for task demands. Findings suggest a conceptualization of DLPFC and its involvement in WM that takes into account a role for affective parameters.

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Figures

Figure 1

Figure 1

Cognitive tasks, sample stimuli, and fMRI scanning sequence. (a) Stimuli (70% cues, 30% probes) were presented for 2.5 s followed by an 11.5-s delay. Pleasant, neutral, and unpleasant pictures were presented randomly within each trial block. Subjects indicated if an infrequently presented probe matrix contained the immediately preceding cue (WM) or an image in the surround that was identical to the image in the center (DET). (b) fMRI acquisition was synchronized to stimulus onset, and four 3.5-s scans were acquired during the course of each 14-s trial.

Figure 2

Figure 2

Mean normalized magnitude of startle blink (n = 9) evoked during the delay period after the presentation of cues in the DET and WM tasks. (Standard error bars are shown.)

Figure 3

Figure 3

Task- and valence-related effects on prefrontal cortex activity (n = 10). (a) Slice image illustrates regions of the right DPFC (BA 46/9) and medial OFC (BA 10/11) that exhibited significant task-related changes in signal intensity (P < .0025; white, memory > detection; black, detection > memory). Maximum z values for dorsolateral and medial frontal clusters were 4.61 and 4.01, respectively; cluster sizes were 95 and 102 voxels, respectively. Numbers in parentheses show the standard reporting coordinates (ref. ; x, y, z) for voxels exhibiting the most significant P value. R, right; L, left. (b) Task-related signal intensity change as a function of scan-in-trial shown as the percentage change in signal intensity from scan 1 in the DET task. (c) Mean range-corrected (_x_i − minimum/maximum − minimum) signal intensity as a function of task and valence for the right dorsolateral (left) and medial orbitofrontal (right) clusters. Signal intensity was averaged across all significant voxels in each cluster. (Standard error bars are shown.)

Figure 4

Figure 4

Mean range-corrected (_x_i − minimum/maximum − minimum) signal intensity as a function of pleasant and unpleasant valence for the right dorsolateral and orbitofrontal regions in the WM task. Nine of ten subjects showed the inverse DLPFC-OFC valence pattern.

Figure 5

Figure 5

Task- and valence-related effects on behavioral performance in 23 subjects who performed a modified version of the task wherein probe stimuli contained only two rather than nine pictures.

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