Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Differential Activation Patterns in the Same Brain Region Led to Opposite Emotional States

 

PloS Biology, Published: September 8, 2016

https://doi.org/10.1371/journal.pbio.1002546

Differential Activation Patterns in the Same Brain Region Led to Opposite Emotional States

Kazuhisa Shibata, et.al.

Brain Information Communication Research Laboratory Group, Advanced Telecommunications Research Institute International, 2-2-2 Hikaridai, Keihanna Science City, Kyoto, Japan,

Department of Cognitive, Linguistics, & Psychological Sciences, Brown University, Providence, Rhode Island, United States of America

[paraphrase]

In human studies, how averaged activation in a brain region relates to human behavior has been extensively investigated. This approach has led to the finding that positive and negative facial preferences are represented by different brain regions. However, using a functional magnetic resonance imaging (fMRI) decoded neurofeedback (DecNef) method, we found that different patterns of neural activations within the cingulate cortex (CC) play roles in representing opposite directions of facial preference. In the present study, while neutrally preferred faces were presented, multi-voxel activation patterns in the CC that corresponded to higher (or lower) preference were repeatedly induced by fMRI DecNef. As a result, previously neutrally preferred faces became more (or less) preferred. We conclude that a different activation pattern in the CC, rather than averaged activation in a different area, represents and suffices to determine positive or negative facial preference. This new approach may reveal the importance of an activation pattern within a brain region in many cognitive functions.

In recent years, several methods have been developed for manipulating brain activity in humans. Real-time functional magnetic resonance imaging decoded neurofeedback (fMRI DecNef) is a method that allows the induction of specific patterns of brain activity by measuring the current pattern, comparing this to the pattern to be induced, and giving the subjects feedback on how close the two patterns of neuronal activity are. Using fMRI DecNef, we manipulated the pattern of activation in the cingulate cortex—a part of the cerebral cortex that plays a role in preference to different categories including faces and daily items—and tested whether we could change these preferences. In the experiment, a specific activation pattern in the cingulate cortex corresponding to higher (or lower) preference was induced by fMRI DecNef while subjects were seeing a neutrally preferred face. As a result, these neutrally preferred faces became more (or less) preferred. Our finding suggests that different patterns of activation in the cingulate cortex represent, and are sufficient to determine, different emotional states. Our new approach using fMRI DecNef may reveal the importance of activation patterns within a brain region, rather than activation in a whole region, in many cognitive functions.

Facial preferences influence a wide range of social outcomes from face perception to social behavior [313] and, therefore, has been a subject of great interest. Theories of facial preferences have also been developed, with the general consensus that positive and negative facial preferences are represented by different brain regions including the amygdala, basal ganglia, insular cortex, occipitotemporal cortex, orbit frontal cortex, lateral prefrontal cortex, and cingulate cortex (CC). The CC has also been reported to play roles in preference to different categories including faces and daily items.

A recently developed online functional magnetic resonance imaging (fMRI) decoded neurofeedback (DecNef) has allowed us to induce a different multi-voxel pattern of activation within the same brain region. In the present study, using fMRI DecNef, we tested whether a different pattern of activations within a single brain region can sufficiently change facial preferences in a positive or negative direction.

In the experiment, we chose the CC as the target brain region for fMRI DecNef because the CC was found to be the best region whose multi-voxel activation patterns represent both positive and negative facial preferences in the current study among the regions previously implicated in facial preference. We tested whether subjects’ preferences to neutrally preferred faces could be changed toward a positive (or negative) direction by fMRI DecNef, which induced multi-voxel activation patterns in the CC that correspond to higher (or lower) preference with presentations of the neutrally rated faces to generate a new association between the faces and manipulated preferences. As a result, the previously neutrally rated faces became significantly more (or less) preferred. Although subjects’ facial preferences were successfully changed, subjects remained unaware of the aim to change their facial preferences. On the contrary to the previous belief that a different brain region plays a role in positive or negative facial preference, our results are in accord with the hypothesis that it is a different activation pattern in the CC that represents and suffices to determine positive or negative facial preference.

The results of the present study indicate that highly selective activity patterns for higher or lower preference within the CC that were repeatedly paired with facial stimuli lead to changes in subjects’ facial preferences. Although these results do not deny important roles of other regions in facial preference, our study clearly demonstrates that inductions of different patterns of activation within the CC suffice to determine changes of facial preference in opposite directions beyond subjects’ will.

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