The Neural Correlates of Aversive Feelings: Anterior...
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The Neural Correlates of Aversive Feelings: Anterior Insula Responses to Route Obstructions during Virtual Navigation Henrietta Afari 2 , Fenna M. Krienen 2 , Randy L. Buckner 1,2,3,4 HHMI 1 , Psychology & Ctr for Brain Science, Harvard 2 , Radiology & Martinos Ctr, MGH/HMS 3 , Psychiatry, MGH/HMS 4 Introduction Supported by NIH Grants AG03456, AG021910, the Howard Hughes Medical Institute and fellowships to F.M.K. from N.D.S.E.G., the Ashford Fellows Fund and the Sackler Scholars Program for Psychobiology. Special thanks also go to Daniel Schacter and Angela Castellanos for their immense help with the project. Contact: [email protected] Methods Previous literature has established a robust theoretical and empirical foundation for the role of emotion in affective learning. Although emerging evidence highlights a critical role of the insular cortex in mediating feelings, uncertainty and risk in the context of decision making, neuroscientific studies of affective learning have largely focused on structures such as the amygdala and the ventral striatum. The present study therefore examined the effects of the insular cortex associated with different feeling states during error-based learning. In classical decision-making conundrums, predictions about future outcomes based on past experiences arbitrate future actions (Singer, Critchley, & Preuschoff, 2009). Aversive behavioral responses such as frustration arise when there are discrepancies between predicted and actual risks, often sustaining significant errors and costs that help make future predictions more accurate (Singer et al., 2009). Moreover, emerging evidence suggest that agency, a feeling that the self is the cause of action, has a strong relationship to the processing of prediction error during risk assessment (Yomogida, et al., 2010). Using a first-person virtual navigation maze, we investigated behavioral and neuroanatomical responses to unexpected stimuli during memory retrieval of learned routes. We constructed route obstructions which differed in degree of predictability, agency and cost and analyzed the distribution of self-reported negative affect to these events. We hypothesized that the resulting affective responses would co-vary with barrier type and would be associated with differential anterior insula activity. Experiment 1: Behavioral Study Experiment 2: fMRI Study Participants Training Session • 2-4 days prior to scan session (mean session duration: 1.5 hrs) • Participants are trained to criterion performance on optimal routes between 4 rooms, and are required to learn the location of hidden fixed barriers. cue hidden fixed barriers goal Testing Session • Repeat criterion training (mean duration: 45 min) • Introduce new rule: on each trial, one additional barrier may be encountered in an unexpected location. Rebuild (REB) barriers: requires forming a novel route NoRebuild (NoREB) barriers: irrelevant to planned route Fixed barriers: pre-learned barriers Barrier Types and Associated Costs Results Conclusions 1) Subjective feeling states of frustration were higher for barrier events with high prediction error, agency error and rebuild costs, and lower for those with low scores on these three metrics. 2) Frustration levels as modulated by barrier type were associated with increased activity in the anterior insular cortex. Barrier type also modulated basolateral amygdala activity, but the response profile did not match that of the negative affect reports. 3) Our findings not only highlight the common role of the anterior insula in mediating feelings, uncertainty and costs, but also draws our attention to the capacity of subjective feeling state signals to provide adaptive information during classical error- based and affective learning. 4) Further studies should examine the effects of feelings of frustration on subsequent performance during error-based learning. Future studies should also more carefully isolate the individual contributions of prediction, agency and rebuild errors and costs to the development of frustration. The reduced engagement of the amygdala and ventral striatum are interesting and further studies should empirically examine the differential contributions of these structures. References Singer, T., Critchley, H. D., & Preuschoff, K. (2009). A common role of insula in feelings, empathy and uncertainty. Trends in Cognitive Sciences, 13(8), 334-340. Yomogida, Y., Sugiura, M., Sassa, Y., Wakusawa, K., Sekiguchi, A., Fukushima, A., et al. (2010). The neural basis of agency: An fMRI study. NeuroImage, 50, 198-207. Frustration at barrier events are strongly mediated by the Anterior Insula Cortex Affect Responses during Active Navigation Contrasts show anterior insular activations are robust across all four inter-barrier comparisons. Minimal t-values were set at 3.43 for FIXED barrier comparisons and 3.37 for other barrier comparisons (p < 0.001). A) Negative affect response of frustration is highest for FIXED, lowest for NoREB, and intermediate for REB. B) Positive affect responses are fairly equal across barrier conditions C) Positive affect is mostly associated with goal events in the maze. Avg, Average. *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001. 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 FIXED REB NoREB Avg. Proportion of Button Presses Barrier Type ** *** **** -0.2 0 0.2 0.4 0.6 0.8 1 1.2 1.4 1.6 FIXED REB NoREB Beta value Barrier Type **** **** *** FIXED vs. GOAL Anterior insula FIXED vs. REB FIXED vs. NoREB REB vs. NoREB A C B D -0.5 -0.45 -0.4 -0.35 -0.3 -0.25 -0.2 -0.15 -0.1 -0.05 0 FIXED REB NoREB Beta value Barrier Type * * Significant differences in barrier comparisons for Left Basolateral Amygdala, though they do not follow the self-report negative affect distribution. N = 31 0 0.1 0.2 0.3 0.4 0.5 p(Button Press) Distance Traveled FIXED Events 0 0.01 0.02 0.03 0.04 0.05 0.06 p(Button Press) Distance Traveled Rebuild Events 0 0.02 0.04 0.06 p(Button Press) Distance Traveled No Rebuild Events FIXED Barrier REB Barrier NoREB Barrier Prediction Error Cost High High Low Agency Error Cost High Low Low Rebuild Cost Low High None Basolateral Amygdala Activity Does Not Follow Negative Affect Distribution A) Stronger Left Anterior Insula Cortex activation for FIXED than for REB which have greater insula activity than NoREB barrier events. B) Activation is modulated by magnitude of turns. N = 33 Neural Responses to Barrier Events 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 FIXED REB NoREB Barrier Type ** Negative Frustration Affect Levels Co-vary with Barrier Type A. Negative Affect B. Positive Affect 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 GOAL CUE OTHER Positive Negative C. X bu&on presses temporary barriers fixed barriers Single sample run (Positive Affect) Single sample run (Negative Affect) X bu&on presses 0 0.02 0.04 0.06 0.08 0.1 0.12 p(Button Press) Pause Events 0 0.05 0.1 0.15 0.2 0.25 p(Button Press) Goal Events A B A) Real-time plot of the navigation runs for a sample subject in the negative affect group. B) Probabilities of button presses in response to negative and positive affect during active navigation. event onset Negative affect group Positive affect group -12000 -12000 0 -12000 -12000 0 -12000 -12000 0 -12000 -12000 0 -12000 -12000 0 • N=24 (mean age = 22.8 yr, 14 male; all RH) 12 in positive affect group, 12 in negative • 1 participant excluded for failure to reach criterion performance level • N=33 (mean age = 21.3 yr, 30 male; all RH) • 6 participants excluded for low FIXED barrier encounters (error rates) during navigation Imaging Parameters • 3T Siemens Tim Trio MRI scanner (12 channel coil) • T1-weighted ME-MPRAGE (1.20 mm iso, TR = 2.2s, TI = 1.1s, TE = 1.54ms • Gradient echo T2*-weighted BOLD acquisition (3.00 mm iso, transverse orientation, 31 slices, TR = 2.0s, TE = 30ms) Affect Self-Report Measures • Feeling states were indicated by pressing a pre-specified button on the keyboard. • Participants were assigned to either Positive or Negative affect group. Distance Traveled Distance Traveled A. -0.5 0 0.5 1 1.5 2 2.5 TURNS TURNS MAGNITUDE Beta value Turns analysis B. The Maze FIXED Barrier REB/ NoREB .. Barrier -36, 16, -8 ROI ROI
Transcript of The Neural Correlates of Aversive Feelings: Anterior...
The Neural Correlates of Aversive Feelings: Anterior Insula Responses to Route Obstructions during Virtual Navigation
Henrietta Afari2, Fenna M. Krienen2, Randy L. Buckner1,2,3,4 HHMI1, Psychology & Ctr for Brain Science, Harvard2, Radiology & Martinos Ctr, MGH/HMS3, Psychiatry, MGH/HMS4
Introduction
Supported by NIH Grants AG03456, AG021910, the Howard Hughes Medical Institute and fellowships to F.M.K. from N.D.S.E.G., the Ashford Fellows Fund and the Sackler Scholars Program for Psychobiology. Special thanks also go to Daniel Schacter and Angela Castellanos for their immense help with the project. Contact: [email protected]
Methods
Previous literature has established a robust theoretical and empirical foundation for the role of emotion in affective learning. Although emerging evidence highlights a critical role of the insular cortex in mediating feelings, uncertainty and risk in the context of decision making, neuroscientific studies of affective learning have largely focused on structures such as the amygdala and the ventral striatum.
The present study therefore examined the effects of the insular cortex associated with different feeling states during error-based learning. In classical decision-making conundrums, predictions about future outcomes based on past experiences arbitrate future actions (Singer, Critchley, & Preuschoff, 2009). Aversive behavioral responses such as frustration arise when there are discrepancies between predicted and actual risks, often sustaining significant errors and costs that help make future predictions more accurate (Singer et al., 2009). Moreover, emerging evidence suggest that agency, a feeling that the self is the cause of action, has a strong relationship to the processing of prediction error during risk assessment (Yomogida, et al., 2010).
Using a first-person virtual navigation maze, we investigated behavioral and neuroanatomical responses to unexpected stimuli during memory retrieval of learned routes. We constructed route obstructions which differed in degree of predictability, agency and cost and analyzed the distribution of self-reported negative affect to these events. We hypothesized that the resulting affective responses would co-vary with barrier type and would be associated with differential anterior insula activity.
Experiment 1: Behavioral Study Experiment 2: fMRI Study
Participants
Training Session • 2-4 days prior to scan session (mean session duration: 1.5 hrs) • Participants are trained to criterion performance on optimal routes between 4 rooms,
and are required to learn the location of hidden fixed barriers.
cue hidden fixed barriers goal
Testing Session • Repeat criterion training (mean duration: 45 min) • Introduce new rule: on each trial, one additional barrier may be encountered in an unexpected location.
Rebuild (REB) barriers: requires forming a novel route NoRebuild (NoREB) barriers: irrelevant to planned route Fixed barriers: pre-learned barriers Barrier Types and Associated Costs
Results
Conclusions 1) Subjective feeling states of frustration were higher for barrier events with high prediction error, agency error and rebuild costs, and lower for those with low scores on these three metrics.
2) Frustration levels as modulated by barrier type were associated with increased activity in the anterior insular cortex. Barrier type also modulated basolateral amygdala activity, but the response profile did not match that of the negative affect reports.
3) Our findings not only highlight the common role of the anterior insula in mediating feelings, uncertainty and costs, but also draws our attention to the capacity of subjective feeling state signals to provide adaptive information during classical error-based and affective learning.
4) Further studies should examine the effects of feelings of frustration on subsequent performance during error-based learning. Future studies should also more carefully isolate the individual contributions of prediction, agency and rebuild errors and costs to the development of frustration. The reduced engagement of the amygdala and ventral striatum are interesting and further studies should empirically examine the differential contributions of these structures.
References Singer, T., Critchley, H. D., & Preuschoff, K. (2009). A common role of insula in feelings, empathy and uncertainty. Trends in Cognitive Sciences, 13(8), 334-340.
Yomogida, Y., Sugiura, M., Sassa, Y., Wakusawa, K., Sekiguchi, A., Fukushima, A., et al. (2010). The neural basis of agency: An fMRI study. NeuroImage, 50, 198-207.
Frustration at barrier events are strongly mediated by the Anterior Insula Cortex
Affect Responses during Active Navigation
Contrasts show anterior insular activations are robust across all four inter-barrier comparisons. Minimal t-values were set at 3.43 for FIXED barrier comparisons and 3.37 for other barrier comparisons (p < 0.001).
A) Negative affect response of frustration is highest for FIXED, lowest for NoREB, and intermediate for REB. B) Positive affect responses are fairly equal across barrier conditions C) Positive affect is mostly associated with goal events in the maze. Avg, Average. *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001.
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Significant differences in barrier comparisons for Left Basolateral Amygdala, though they do not follow the self-report negative affect distribution. N = 31
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Basolateral Amygdala Activity Does Not Follow Negative Affect Distribution
A) Stronger Left Anterior Insula Cortex activation for FIXED than for REB which have greater insula activity than NoREB barrier events. B) Activation is modulated by magnitude of turns. N = 33
Neural Responses to Barrier Events
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A) Real-time plot of the navigation runs for a sample subject in the negative affect group.
B) Probabilities of button presses in response to negative and positive affect during active navigation.
event onset Negative affect group Positive affect group
-12000 -12000 0
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• N=24 (mean age = 22.8 yr, 14 male; all RH) 12 in positive affect group, 12 in negative • 1 participant excluded for failure to reach
criterion performance level
• N=33 (mean age = 21.3 yr, 30 male; all RH) • 6 participants excluded for low FIXED barrier encounters (error rates) during
navigation
Imaging Parameters • 3T Siemens Tim Trio MRI scanner (12 channel coil) • T1-weighted ME-MPRAGE (1.20 mm iso, TR = 2.2s, TI = 1.1s, TE = 1.54ms • Gradient echo T2*-weighted BOLD acquisition (3.00 mm iso, transverse orientation, 31 slices, TR = 2.0s, TE = 30ms)
Affect Self-Report Measures • Feeling states were indicated by pressing a pre-specified button on the keyboard. • Participants were assigned to either Positive or Negative affect group.
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