TY - JOUR
T1 - Genetic influences on functional connectivity associated with feedback processing and prediction error
T2 - Phase coupling of theta-band oscillations in twins
AU - Demiral, Şükrü Barış
AU - Golosheykin, Simon
AU - Anokhin, Andrey P.
N1 - Funding Information:
This work was supported by grants DA018899, DA027096, DA00421, and AA016812 to A.A. from the National Institutes of Health (NIH). The authors acknowledge organizational and technical assistance by Tara Tinnin, MSW, Olga Novak, and other project staff. The authors also acknowledge the generous giving of time and effort by the study participants.
Publisher Copyright:
© 2016 Elsevier B.V.
PY - 2017/5/1
Y1 - 2017/5/1
N2 - Detection and evaluation of the mismatch between the intended and actually obtained result of an action (reward prediction error) is an integral component of adaptive self-regulation of behavior. Extensive human and animal research has shown that evaluation of action outcome is supported by a distributed network of brain regions in which the anterior cingulate cortex (ACC) plays a central role, and the integration of distant brain regions into a unified feedback-processing network is enabled by long-range phase synchronization of cortical oscillations in the theta band. Neural correlates of feedback processing are associated with individual differences in normal and abnormal behavior, however, little is known about the role of genetic factors in the cerebral mechanisms of feedback processing. Here we examined genetic influences on functional cortical connectivity related to prediction error in young adult twins (age 18, n = 399) using event-related EEG phase coherence analysis in a monetary gambling task. To identify prediction error-specific connectivity pattern, we compared responses to loss and gain feedback. Monetary loss produced a significant increase of theta-band synchronization between the frontal midline region and widespread areas of the scalp, particularly parietal areas, whereas gain resulted in increased synchrony primarily within the posterior regions. Genetic analyses showed significant heritability of frontoparietal theta phase synchronization (24 to 46%), suggesting that individual differences in large-scale network dynamics are under substantial genetic control. We conclude that theta-band synchronization of brain oscillations related to negative feedback reflects genetically transmitted differences in the neural mechanisms of feedback processing. To our knowledge, this is the first evidence for genetic influences on task-related functional brain connectivity assessed using direct real-time measures of neuronal synchronization.
AB - Detection and evaluation of the mismatch between the intended and actually obtained result of an action (reward prediction error) is an integral component of adaptive self-regulation of behavior. Extensive human and animal research has shown that evaluation of action outcome is supported by a distributed network of brain regions in which the anterior cingulate cortex (ACC) plays a central role, and the integration of distant brain regions into a unified feedback-processing network is enabled by long-range phase synchronization of cortical oscillations in the theta band. Neural correlates of feedback processing are associated with individual differences in normal and abnormal behavior, however, little is known about the role of genetic factors in the cerebral mechanisms of feedback processing. Here we examined genetic influences on functional cortical connectivity related to prediction error in young adult twins (age 18, n = 399) using event-related EEG phase coherence analysis in a monetary gambling task. To identify prediction error-specific connectivity pattern, we compared responses to loss and gain feedback. Monetary loss produced a significant increase of theta-band synchronization between the frontal midline region and widespread areas of the scalp, particularly parietal areas, whereas gain resulted in increased synchrony primarily within the posterior regions. Genetic analyses showed significant heritability of frontoparietal theta phase synchronization (24 to 46%), suggesting that individual differences in large-scale network dynamics are under substantial genetic control. We conclude that theta-band synchronization of brain oscillations related to negative feedback reflects genetically transmitted differences in the neural mechanisms of feedback processing. To our knowledge, this is the first evidence for genetic influences on task-related functional brain connectivity assessed using direct real-time measures of neuronal synchronization.
KW - Brain oscillations
KW - Connectivity
KW - EEG
KW - Feedback
KW - Genetics
KW - Neural synchrony
KW - Phase coherence
KW - Prediction error
UR - http://www.scopus.com/inward/record.url?scp=85009209146&partnerID=8YFLogxK
U2 - 10.1016/j.ijpsycho.2016.12.013
DO - 10.1016/j.ijpsycho.2016.12.013
M3 - Article
C2 - 28043892
AN - SCOPUS:85009209146
VL - 115
SP - 133
EP - 141
JO - International Journal of Psychophysiology
JF - International Journal of Psychophysiology
SN - 0167-8760
ER -