Affective value and associative processing share a cortical substrate - PubMed (original) (raw)
Affective value and associative processing share a cortical substrate
Amitai Shenhav et al. Cogn Affect Behav Neurosci. 2013 Mar.
Abstract
The brain stores information in an associative manner so that contextually related entities are connected in memory. Such associative representations mediate the brain's ability to generate predictions about which other objects and events to expect in a given context. Likewise, the brain encodes and is able to rapidly retrieve the affective value of stimuli in our environment. That both contextual associations and affect serve as building blocks of numerous mental functions often makes interpretation of brain activation ambiguous. A critical brain region where such activation has often resulted in equivocal interpretation is the medial orbitofrontal cortex (mOFC), which has been implicated separately in both affective and associative processing. To characterize its role more unequivocally, we tested whether activity in the mOFC was most directly attributable to affective processing, associative processing, or a combination of both. Subjects performed an object recognition task while undergoing fMRI scans. Objects varied independently in their affective valence and in their degree of association with other objects (associativity). Analyses revealed an overlapping sensitivity whereby the left mOFC responded both to increasingly positive affective value and to stronger associativity. These two properties individually accounted for mOFC response, even after controlling for their interrelationship. The role of the mOFC is either general enough to encompass associations that link stimuli both with reinforcing outcomes and with other stimuli or abstract enough to use both valence and associativity in conjunction to inform downstream processes related to perception and action. These results may further point to a fundamental relationship between associativity and positive affect.
Figures
Figure 1
Task timeline. Subjects viewed objects presented briefly and in isolation (150ms), followed by a colorful backward mask (100ms) and then rated how common the object was (1.5s response period). In between trials subjects viewed a black fixation cross for variable durations.
Figure 2
Analysis of mOFC reactivity to affectively valenced categories relative to neutral objects of varying associativity. a) Examples of stimuli from each of the four object categories. b) Individually-defined left mOFC anatomical ROI shown on a single subject’s inflated surface. c) Group ROI analyses show average BOLD response to each of these four categories in left mOFC. Error bars reflect between-subject standard errors of the mean.
Figure 3
a) Whole-brain analysis projected onto the inflated cortical surface display main effect of condition (left; significance values based on _F_-test for group repeated-measures ANOVA) and simple effect contrast (_t_-test) for the average of all conditions relative to baseline (right). b–d) Whole-brain contrasts (_t_-tests) display relative BOLD activation when viewing Strongly versus Weakly associative objects (neutrally valenced) and objects containing Positive affective value (relative to Neutral and Negative) (left: surface-based shown at uncorrected voxelwise threshold of p<0.001; right: same activations shown on the brain volume in Talairach space, all shown at voxelwise p<0.01, extent-thresholded to achieve a whole-brain cluster-corrected threshold of p<0.05). e) A conjunction of these three (corrected) contrasts reveals a role for the left mOFC at the intersection of affective and associative processing. Whole-brain maps provided for completeness, but analyses of interest were performed in a priori ROI’s.
Figure 4
Analysis of mOFC reactivity to fully crossed set of objects of increasing valence (Negative, Neutral, Positive) and different associativity levels (Weak vs. Strong). a) Examples of stimuli from each of six object categories. b) Group ROI analyses in left mOFC reveal main effects for both valence and associativity. Error bars reflect between-subject standard errors of the mean.
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References
- Baddeley A. Selective attention and performance in dangerous environments. British Journal of Psychology. 1972;63:537–546. - PubMed
- Bar M. Visual objects in context. Nature Reviews Neuroscience. 2004;5(8):617–629. - PubMed
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