脑岛自发神经活动强度可预测个体错误后反应调整速度
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摘要
错误后行为调整是指错误反应发生后,个体为了避免错误再次发生和优化未来行为执行而进行的行为调整.本研究旨在采用静息态fMRI技术考察大脑自发神经活动对个体错误后行为调整的预测作用.研究发现, ACC自发神经活动低频振幅(ALFF)值与个体错误后行为调整效应量相关不显著,但是双侧脑岛自发神经活动ALFF值与个体错误后行为调整效应量呈显著正相关.双侧脑岛ALFF值越大的个体,错误后试次反应时越长,错误后调整反应速度越慢.该结果说明,双侧脑岛参与错误后行为调整,并对个体错误后反应速度调整有预测作用.
After committing an error, humans often adopt strategies to change error behaviors, this phenomenon is termed post-error adjustment. The post-error adjustment ability is fundamental to flexible behavior and survival in a complex, varying environment. Resting-state neural activity has been associated with a variety of cognitive abilities, yet its relevance to posterror adjustment has been unclear.Resting-state fMRI is a powerful tool for investigating this spontaneous brain activity, since it can reveal the correlation of the intrinsic functional architecture of the brain and the extrinsic behavior performance. The amplitude of low-frequency fluctuation(ALFF, 0.01–0.08 Hz) is widely used as an indicator of spontaneous fluctuations in brain activity. It has been suggested to reflect individual differences in cognitive control and personality traits. Therefore, the investigation of the spontaneous brain activity related to the post-error adjustment will provide novel insight into the understanding of the generation mechanism of post-error adjustment.The current study employed a modified Go/NoGo task to investigate the intrinsic neural correlates of post-error adjustment by analyzing the ALFF. To yield a sufficient number of error trials, we instructed subjects to withhold their responses in two circumstances.(1) When word meaning and the font color of word were inconsistent, this trial was termed as incongruent Nogo;(2) when a word was presented on two consecutive trials(same meaning and same font color).Considering previous studies have demonstrated that anterior cingulate cortex(ACC) and bilateral insula play an important role in the error monitoring and error adaptation, thus the anterior cingulate cortex and bilateral insula were selected as the regions of interest(ROIs) in the present study. Additionally, the small volume correction was performed for multiple comparison. Moreover, since low-frequency fluctuations in the gray matter were higher than those in the white matter, the ALFF was calculated only in the gray matter.As a result, the ALFF-behavior analysis revealed that the magnitude of post-error adjustment in reaction time was not correlated with the ALFF in ACC. However, the magnitude of post-error adjustment in reaction time was positively associated with the ALFF in bilateral insula. Specifically, stronger spontaneous neuronal activity in bilateral insula corresponded to slower post-error adjustments. Together, the findings suggest that spontaneous activity in the bilateral insula may be the neural indicator of the individual difference in post-error adjustment, which may predict the adjustive time of post-error behavior.
After committing an error, humans often adopt strategies to change error behaviors, this phenomenon is termed post-error adjustment. The post-error adjustment ability is fundamental to flexible behavior and survival in a complex, varying environment. Resting-state neural activity has been associated with a variety of cognitive abilities, yet its relevance to posterror adjustment has been unclear.Resting-state fMRI is a powerful tool for investigating this spontaneous brain activity, since it can reveal the correlation of the intrinsic functional architecture of the brain and the extrinsic behavior performance. The amplitude of low-frequency fluctuation(ALFF, 0.01–0.08 Hz) is widely used as an indicator of spontaneous fluctuations in brain activity. It has been suggested to reflect individual differences in cognitive control and personality traits. Therefore, the investigation of the spontaneous brain activity related to the post-error adjustment will provide novel insight into the understanding of the generation mechanism of post-error adjustment.The current study employed a modified Go/NoGo task to investigate the intrinsic neural correlates of post-error adjustment by analyzing the ALFF. To yield a sufficient number of error trials, we instructed subjects to withhold their responses in two circumstances.(1) When word meaning and the font color of word were inconsistent, this trial was termed as incongruent Nogo;(2) when a word was presented on two consecutive trials(same meaning and same font color).Considering previous studies have demonstrated that anterior cingulate cortex(ACC) and bilateral insula play an important role in the error monitoring and error adaptation, thus the anterior cingulate cortex and bilateral insula were selected as the regions of interest(ROIs) in the present study. Additionally, the small volume correction was performed for multiple comparison. Moreover, since low-frequency fluctuations in the gray matter were higher than those in the white matter, the ALFF was calculated only in the gray matter.As a result, the ALFF-behavior analysis revealed that the magnitude of post-error adjustment in reaction time was not correlated with the ALFF in ACC. However, the magnitude of post-error adjustment in reaction time was positively associated with the ALFF in bilateral insula. Specifically, stronger spontaneous neuronal activity in bilateral insula corresponded to slower post-error adjustments. Together, the findings suggest that spontaneous activity in the bilateral insula may be the neural indicator of the individual difference in post-error adjustment, which may predict the adjustive time of post-error behavior.
引文
1 Danielmeier C,Ullsperger M.Post-error adjustments.Front Psychol,2011,2:233
2 Rabbitt P M.Errors and error correction in choice-response tasks.J Exp Psychol,1966,71:264-272
3 Ullsperger M,Danielmeier C,Jocham G.Neurophysiology of performance monitoring and adaptive behavior.Physiol Rev,2014,94:35-79
4 Wang L J,Liu C P,Hu X P,et al.The alertness level influences post-error adjustments(in Chinese).Chin Sci Bull,2016,61:3708-3717[王丽君,刘长平,胡学平,等.警觉水平影响错误后行为适应.科学通报,2016,61:3708-3717]
5 Botvinick M M,Braver T S,Barch D M,et al.Conflict monitoring and cognitive control.Psychol Rev,2001,108:624-652
6 Hyman J M,Holroyd C B,Seamans J K.A novel neural prediction error found in anterior cingulate cortex ensembles.Neuron,2017,95:447-456
7 Kerns J G,Cohen J D,MacDonald A W,et al.Anterior cingulate conflict monitoring and adjustments in control.Science,2004,303:1023-1026
8 Iannaccone R,Hauser T U,Staempfli P,et al.Conflict monitoring and error processing:New insights from simultaneous EEG-fMRI.NeuroImage,2015,105:395-407
9 Wang L,Tang D,Zhao Y,et al.Disentangling the impacts of outcome valence and outcome frequency on the post-error slowing.Sci Rep,2015,5:8708
10 Stemmer B,Segalowitz S J,Witzke W,et al.Error detection in patients with lesions to the medial prefrontal cortex:An ERP study.Neuropsychologia,2004,42:118-130
11 Maltby N,Tolin D F,Worhunsky P,et al.Dysfunctional action monitoring hyperactivates frontal-striatal circuits in obsessive-compulsive disorder:An event-related fMRI study.NeuroImage,2005,24:495-503
12 Fitzgerald K D,Welsh R C,Gehring W J,et al.Error-related hyperactivity of the anterior cingulate cortex in obsessive-compulsive disorder.Biol Psychiatry,2005,57:287-294
13 Klein T A,Endrass T,Kathmann N,et al.Neural correlates of error awareness.NeuroImage,2007,34:1774-1781
14 Spunt R P,Lieberman M D,Cohen J R,et al.The phenomenology of error processing:The dorsal ACC response to stop-signal errors tracks reports of negative affect.J Cogn Neurosci,2012,24:1753-1765
15 Ham T,Leff A,de Boissezon X,et al.Cognitive control and the salience network:An investigation of error processing and effective connectivity.JNeurosci,2013,33:7091-7098
16 Polli F E,Barton J J S,Vangel M,et al.Schizophrenia patients show intact immediate error-related performance adjustments on an antisaccade task.Schizoph Res,2006,82:191-201
17 Bastin J,Deman P,David O,et al.Direct recordings from human anterior insula reveal its leading role within the error-monitoring network.Cereb Cortex,2017,27:1545-1557
18 Cai W,Chen T,Ryali S,et al.Causal interactions within a frontal-cingulate-parietal network during cognitive control:Convergent evidence from a multisite-multitask investigation.Cereb Cortex,2016,26:2140-2153
19 Jilka S R,Scott G,Ham T,et al.Damage to the salience network and interactions with the default mode network.J Neurosci,2014,34:10798-10807
20 Menon V,Uddin L Q.Saliency,switching,attention and control:A network model of insula function.Brain Struct Funct,2010,214:655-667
21 Godefroid E,Pourtois G,Wiersema J.An aware error is a salient event:The anterior insula assigns salience to aware errors through interoceptive mechanisms.Front Hum Neurosci,2015,9:197
22 Harsay H A,Spaan M,Wijnen J G,et al.Error awareness and salience processing in the oddball task:Shared neural mechanisms.Front Hum Neurosci,2012,6:246
23 Klein T A,Markus U,Claudia D.Error awareness and the insula:Links to neurological and psychiatric diseases.Front Hum Neurosci,2013,7:14
24 Mezer A,Yovel Y,Pasternak O,et al.Cluster analysis of resting-state fMRI time series.NeuroImage,2009,45:1117-1125
25 Pan W,Liu C,Yang Q,et al.The neural basis of trait self-esteem revealed by the amplitude of low-frequency fluctuations and resting state functional connectivity.Soc Cogn Affect Neurosci,2016,11:367-376
26 Wang L,Chen J,Yang Z,et al.Individual differences in the attentional blink:Evidence from the amplitude of low-frequency fluctuations in nonblinkers and blinkers.Biol Psychol,2016,114:33-38
27 Xie B,Qiu M G,Zhang Y,et al.Alterations in the cortical thickness and the amplitude of low-frequency fluctuation in patients with post-traumatic stress disorder.Brain Res,2013,1490:225-232
28 Fox M D,Raichle M E.Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging.Nat Rev Neurosci,2007,8:700-711
29 Zang Y F,He Y,Zhu C Z,et al.Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI.Brain Dev,2007,29:83-91
30 Kunisato Y,Okamoto Y,Okada G,et al.Personality traits and the amplitude of spontaneous low-frequency oscillations during resting state.Neurosci Lett,2011,492:109-113
31 Mennes M,Zuo X N,Kelly C,et al.Linking inter-individual differences in neural activation and behavior to intrinsic brain dynamics.NeuroImage,2011,54:2950-2959
32 Ashburner J.A fast diffeomorphic image registration algorithm.NeuroImage,2007,38:95-113
33 Yan C G,Zang Y F.DPARSF:A MATLAB toolbox for“pipeline”data analysis of resting-state fMRI.Front Syst Neurosci,2010,4:13
34 Biswal B,Zerrin Y F,Haughton V M,et al.Functional connectivity in the motor cortex of resting human brain using echo-planar MRI.Magn Reson Med,1995,34:537-541
35 Song X W,Dong Z Y,Long X Y,et al.REST:A toolkit for resting-state functional magnetic resonance imaging data processing.PLoS One,2011,6:e25031
36 Wang X,Han Z,He Y,et al.Where color rests:Spontaneous brain activity of bilateral fusiform and lingual regions predicts object color knowledge performance.NeuroImage,2013,76:252-263
37 Wiersema J R,van der Meere J J,Roeyers H.Developmental changes in error monitoring:An event-related potential study.Neuropsychologia,2007,45:1649-1657
38 Larson M J,South M,Clayson P E.Sex differences in error-related performance monitoring.Neuroreport,2011,22:44-48
39 Li C R,Zhang S,Duann J R,et al.Gender differences in cognitive control:An extended investigation of the stop signal task.Brain Imag Behav,2009,3:262-276
40 Fischer A G,Danielmeier C,Villringer A,et al.Gender influences on brain responses to errors and post-error adjustments.Sci Rep,2016,6:24435
41 Wang L,Tan J,Chen J,et al.The influence of observers’sex on attention-demanding performance depends on performers’sex.Front Psychol,2015,6:1217
42 Hester R,Foxe J J,Molholm S,et al.Neural mechanisms involved in error processing:A comparison of errors made with and without awareness.NeuroImage,2005,27:602-608
43 Tops M,Boksem M A S.A potential role of the inferior frontal gyrus and anterior insula in cognitive control,brain rhythms,and event-related potentials.Front Psychol,2011,2:330
44 Notebaert W,Houtman F,Opstal F V,et al.Post-error slowing:An orienting account.Cognition,2009,111:275-279
2 Rabbitt P M.Errors and error correction in choice-response tasks.J Exp Psychol,1966,71:264-272
3 Ullsperger M,Danielmeier C,Jocham G.Neurophysiology of performance monitoring and adaptive behavior.Physiol Rev,2014,94:35-79
4 Wang L J,Liu C P,Hu X P,et al.The alertness level influences post-error adjustments(in Chinese).Chin Sci Bull,2016,61:3708-3717[王丽君,刘长平,胡学平,等.警觉水平影响错误后行为适应.科学通报,2016,61:3708-3717]
5 Botvinick M M,Braver T S,Barch D M,et al.Conflict monitoring and cognitive control.Psychol Rev,2001,108:624-652
6 Hyman J M,Holroyd C B,Seamans J K.A novel neural prediction error found in anterior cingulate cortex ensembles.Neuron,2017,95:447-456
7 Kerns J G,Cohen J D,MacDonald A W,et al.Anterior cingulate conflict monitoring and adjustments in control.Science,2004,303:1023-1026
8 Iannaccone R,Hauser T U,Staempfli P,et al.Conflict monitoring and error processing:New insights from simultaneous EEG-fMRI.NeuroImage,2015,105:395-407
9 Wang L,Tang D,Zhao Y,et al.Disentangling the impacts of outcome valence and outcome frequency on the post-error slowing.Sci Rep,2015,5:8708
10 Stemmer B,Segalowitz S J,Witzke W,et al.Error detection in patients with lesions to the medial prefrontal cortex:An ERP study.Neuropsychologia,2004,42:118-130
11 Maltby N,Tolin D F,Worhunsky P,et al.Dysfunctional action monitoring hyperactivates frontal-striatal circuits in obsessive-compulsive disorder:An event-related fMRI study.NeuroImage,2005,24:495-503
12 Fitzgerald K D,Welsh R C,Gehring W J,et al.Error-related hyperactivity of the anterior cingulate cortex in obsessive-compulsive disorder.Biol Psychiatry,2005,57:287-294
13 Klein T A,Endrass T,Kathmann N,et al.Neural correlates of error awareness.NeuroImage,2007,34:1774-1781
14 Spunt R P,Lieberman M D,Cohen J R,et al.The phenomenology of error processing:The dorsal ACC response to stop-signal errors tracks reports of negative affect.J Cogn Neurosci,2012,24:1753-1765
15 Ham T,Leff A,de Boissezon X,et al.Cognitive control and the salience network:An investigation of error processing and effective connectivity.JNeurosci,2013,33:7091-7098
16 Polli F E,Barton J J S,Vangel M,et al.Schizophrenia patients show intact immediate error-related performance adjustments on an antisaccade task.Schizoph Res,2006,82:191-201
17 Bastin J,Deman P,David O,et al.Direct recordings from human anterior insula reveal its leading role within the error-monitoring network.Cereb Cortex,2017,27:1545-1557
18 Cai W,Chen T,Ryali S,et al.Causal interactions within a frontal-cingulate-parietal network during cognitive control:Convergent evidence from a multisite-multitask investigation.Cereb Cortex,2016,26:2140-2153
19 Jilka S R,Scott G,Ham T,et al.Damage to the salience network and interactions with the default mode network.J Neurosci,2014,34:10798-10807
20 Menon V,Uddin L Q.Saliency,switching,attention and control:A network model of insula function.Brain Struct Funct,2010,214:655-667
21 Godefroid E,Pourtois G,Wiersema J.An aware error is a salient event:The anterior insula assigns salience to aware errors through interoceptive mechanisms.Front Hum Neurosci,2015,9:197
22 Harsay H A,Spaan M,Wijnen J G,et al.Error awareness and salience processing in the oddball task:Shared neural mechanisms.Front Hum Neurosci,2012,6:246
23 Klein T A,Markus U,Claudia D.Error awareness and the insula:Links to neurological and psychiatric diseases.Front Hum Neurosci,2013,7:14
24 Mezer A,Yovel Y,Pasternak O,et al.Cluster analysis of resting-state fMRI time series.NeuroImage,2009,45:1117-1125
25 Pan W,Liu C,Yang Q,et al.The neural basis of trait self-esteem revealed by the amplitude of low-frequency fluctuations and resting state functional connectivity.Soc Cogn Affect Neurosci,2016,11:367-376
26 Wang L,Chen J,Yang Z,et al.Individual differences in the attentional blink:Evidence from the amplitude of low-frequency fluctuations in nonblinkers and blinkers.Biol Psychol,2016,114:33-38
27 Xie B,Qiu M G,Zhang Y,et al.Alterations in the cortical thickness and the amplitude of low-frequency fluctuation in patients with post-traumatic stress disorder.Brain Res,2013,1490:225-232
28 Fox M D,Raichle M E.Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging.Nat Rev Neurosci,2007,8:700-711
29 Zang Y F,He Y,Zhu C Z,et al.Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI.Brain Dev,2007,29:83-91
30 Kunisato Y,Okamoto Y,Okada G,et al.Personality traits and the amplitude of spontaneous low-frequency oscillations during resting state.Neurosci Lett,2011,492:109-113
31 Mennes M,Zuo X N,Kelly C,et al.Linking inter-individual differences in neural activation and behavior to intrinsic brain dynamics.NeuroImage,2011,54:2950-2959
32 Ashburner J.A fast diffeomorphic image registration algorithm.NeuroImage,2007,38:95-113
33 Yan C G,Zang Y F.DPARSF:A MATLAB toolbox for“pipeline”data analysis of resting-state fMRI.Front Syst Neurosci,2010,4:13
34 Biswal B,Zerrin Y F,Haughton V M,et al.Functional connectivity in the motor cortex of resting human brain using echo-planar MRI.Magn Reson Med,1995,34:537-541
35 Song X W,Dong Z Y,Long X Y,et al.REST:A toolkit for resting-state functional magnetic resonance imaging data processing.PLoS One,2011,6:e25031
36 Wang X,Han Z,He Y,et al.Where color rests:Spontaneous brain activity of bilateral fusiform and lingual regions predicts object color knowledge performance.NeuroImage,2013,76:252-263
37 Wiersema J R,van der Meere J J,Roeyers H.Developmental changes in error monitoring:An event-related potential study.Neuropsychologia,2007,45:1649-1657
38 Larson M J,South M,Clayson P E.Sex differences in error-related performance monitoring.Neuroreport,2011,22:44-48
39 Li C R,Zhang S,Duann J R,et al.Gender differences in cognitive control:An extended investigation of the stop signal task.Brain Imag Behav,2009,3:262-276
40 Fischer A G,Danielmeier C,Villringer A,et al.Gender influences on brain responses to errors and post-error adjustments.Sci Rep,2016,6:24435
41 Wang L,Tan J,Chen J,et al.The influence of observers’sex on attention-demanding performance depends on performers’sex.Front Psychol,2015,6:1217
42 Hester R,Foxe J J,Molholm S,et al.Neural mechanisms involved in error processing:A comparison of errors made with and without awareness.NeuroImage,2005,27:602-608
43 Tops M,Boksem M A S.A potential role of the inferior frontal gyrus and anterior insula in cognitive control,brain rhythms,and event-related potentials.Front Psychol,2011,2:330
44 Notebaert W,Houtman F,Opstal F V,et al.Post-error slowing:An orienting account.Cognition,2009,111:275-279
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