Please wait a minute...
Acta Psychologica Sinica    2018, Vol. 50 Issue (6) : 655-666     DOI: 10.3724/SP.J.1041.2018.00655
Reports of Empirical Studies |
The relationship between the caudate nucleus-orbitomedial prefrontal cortex connectivity and reactive aggression: A resting-state fMRI study
Qi JIANG1(),Lulu HOU1,2,Jiang QIU3,Changran LI1,Huanzhen WANG1
1 Mental Health Research Center of Southwest University, Faculty of Psychology, Southwest University, Chongqing 400715, China
2 Department of Psychology, School of Social and Behavior Sciences, Nanjing University, Nanjing 210023, China
3 Key Laboratory of Cognition and Personality of Southwest University, Faculty of Psychology, Southwest University, Chongqing 400715, China
Download: PDF(1453 KB)   HTML Review File (1 KB) 
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks     Supporting Info

Reactive aggression has been widely concerned by researchers because of its serious impact on society, such as violent crimes. Existing neuroimaging studies using patients with high levels of aggression indicated a network of brain regions subserve reactive aggression, including amygdala, caudate nucleus, and orbitofrontal cortex. Furthermore, researchers believed that reduced prefrontal activity along with heightened subcortical activity in the context of provocative stimuli poses an increased risk for reactive aggression. However, evidence for this theory in healthy population is lacking, especially this independently of the experiment task.

In this study, the modified TAP was used and the punishment levels selected for the virtual opponents serve as indicator of reactive aggression. Based on the previous researches, Orbitomedial Prefrontal (OMPFC) was selected as the seed to investigate the relationship of reactive aggression and the connectivity between OMPFC and other brain regions using resting state fMRI. Thirty-night undergraduates (mean age = 20.05 ± 0.92 years old) were enrolled in the experiment. The resting state functional magnetic resonance (rs-fMRI) data was acquired using Echo Planar Imaging (EPI) sequence from a 3-T Siemens Magnetom Trio scanner (Siemens Medical, Erlangen, Germany). This scanning acquired 242 volumes with TR = 2 s (lasting 8 min and 8 sec). rs-fMRI data was processed and analyzed using the REST (Resting-State fMRI Data Analysis Toolkit) toolbox to calculate Functional Connectivity (FC) and Granger Causality Analysis (GCA), which reflects the functional and effective connectivity among different areas, respectively. The results of FC indicated that the functional connectivity between the left OMPFC and right angular gyrus, left OMPFC and bilateral caudate nucleus, right OMPFC and right caudate nucleus were significantly correlated with the reactive aggression. Furthermore, the follow-up GCA indicated that the effective connectivity of right caudate nucleus to the right OMPFC was correlated significantly with reactive aggression, especially in the provocative condition.

The caudate nucleus plays an important role in flexibly responding to the environment. It is activated in response to reward. When the individuals thought the aggression was valuable and seemed to receive reward after the aggression, the caudate nucleus was also activated. Furthermore, a study combined PET and fMRI and revealed a strong relationship between the caudate nucleus and cortical areas associated with executive functioning (i.e., the function of prefrontal cortex). Another study demonstrated that violent offenders behaved more aggressively and showed significantly higher brain reactivity to provocations within the caudate nucleus, as well as reduced caudate nucleus-prefrontal cortex connectivity. To sum up, these results suggest that the connectivity between OMPFC and caudate nucleus is closely related to reactive aggression. It provides some evidence for further revealing the neural mechanism of reactive aggression, and firstly made a systematic analysis of reactive aggression using resting state functional connectivity and effective connectivity.

Keywords reactive aggression      resting-state fMRI      functional connectivity      effective connectivity      Granger causality analysis      OMPFC      caudate nucleus     
ZTFLH:  B845  
Corresponding Authors: Qi JIANG     E-mail:
Issue Date: 28 April 2018
E-mail this article
E-mail Alert
Articles by authors
Lulu HOU
Jiang QIU
Changran LI
Huanzhen WANG
Cite this article:   
Qi JIANG,Lulu HOU,Jiang QIU, et al. The relationship between the caudate nucleus-orbitomedial prefrontal cortex connectivity and reactive aggression: A resting-state fMRI study[J]. Acta Psychologica Sinica, 2018, 50(6): 655-666.
URL:     OR
脑区 半球 MNI坐标 体素数量 t
角回 48, -63, 51 51 5.58
尾状核 -12, 15, 3 30 4.85
18, -15, 21 27 4.37
内侧前额叶 33, 48, -6 74 5.66
51, 30, 33 32 4.95
-42, 48, 3 88 4.55
尾状核 12, 0, 15 54 4.41
内侧前额叶 33, 51, -6 69 5.92
42, 33, 39 48 4.75
-36, 45, 3 45 4.32
功能连接 反应性攻击
-0.43** -0.36* -0.44***
-0.50** -0.46** -0.53***
-0.51** -0.54*** -0.59***
-0.54** -0.55*** -0.61***
效应连接 反应性攻击
-0.05 0.02 -0.01
0.02 -0.09 -0.04
0.21 -0.01 0.11
0.08 0.02 0.05
-0.21 -0.16 -0.20
-0.19 -0.17 -0.20
0.24 0.10 0.19
-0.31 -0.33* -0.36*
[1] Anderson C. A., & Bushman B. J . ( 2002). Human aggression. Annual Review of Psychology, 53(1), 27-51.
[2] Bettencourt B. A., Talley A., Benjamin A. J., & Valentine J . ( 2006). Personality and aggressive behavior under provoking and neutral conditions: A meta-analytic review. Psychological Bulletin, 132(5), 751-777.
pmid: 16910753 url:
[3] Beyer F., Münte T. F., Erdmann C., & Kr?mer U. M . ( 2014). Emotional reactivity to threat modulates activity in mentalizing network during aggression. Social Cognitive and Affective Neuroscience, 9(10), 1552-1560.
pmid: 23986265 url:
[4] Beyer F., Münte T. F., G?ttlich M., & Kr?mer U. M . ( 2015). Orbitofrontal cortex reactivity to angry facial expression in a social interaction correlates with aggressive behavior. Cerebral Cortex, 25(9), 3057-3063.
pmid: 24842782 url:
[5] Bj?rklund A., & Dunnett S. B . ( 2007). Dopamine neuron systems in the brain: An update. Trends in Neurosciences, 30(5), 194-202.
pmid: 17408759 url:
[6] Blair, R. J. R . ( 2012). Considering anger from a cognitive neuroscience perspective. Wiley Interdisciplinary Reviews: Cognitive Science, 3(1), 65-74.
pmid: 22267973 url:
[7] Brett M., Anton J. L., Valabregue R., & Poline J. B . ( 2002). Region of interest analysis using the MarsBar toolbox for SPM 99. NeuroImage, 16(2), S497.
[8] Chen G., Hamilton J. P., Thomason M. E., Gotlib I. H., Saad Z. S., & Cox R. W . ( 2009). Granger causality via vector auto-regression tuned for fMRI data analysis. In Proceedings of the 17th annual scientific meeting and exhibition (Vol. 17, p. 1718). Honolulu, Hawaii.
[9] Coccaro E. F., McCloskey M. S., Fitzgerald D. A., & Phan K. L . ( 2007). Amygdala and orbitofrontal reactivity to social threat in individuals with impulsive aggression. Biological Psychiatry, 62(2), 168-178.
pmid: 17210136 url:
[10] Coccaro E. F., Sripada C. S., Yanowitch R. N., & Phan K. L . ( 2011). Corticolimbic function in impulsive aggressive behavior. Biological Psychiatry, 69(12), 1153-1159.
pmid: 21531387 url:
[11] da Cunha-Bang S., Fisher P. M., Hjordt L. V., Perfalk E., Skibsted A. P., Bock C., .. Knudsen G. M . ( 2017). Violent offenders respond to provocations with high amygdala and striatal reactivity. Social Cognitive and Affective Neuroscience, 12(5), 802-810.
pmid: 28338916 url:
[12] Damasio H., Grabowski T., Frank R., Galaburda A. M., & Damasio A. R . ( 1994). The return of Phineas Gage: Clues about the brain from the skull of a famous patient. Science, 264(5162), 1102-1105.
pmid: 8178168 url:
[13] Davis M., & Whalen P. J . ( 2001). The amygdala: Vigilance and emotion. Molecular Psychiatry, 6(1), 13-34.
pmid: 11244481 url:
[14] D?biec, J. ( 2005). Peptides of love and fear: Vasopressin and oxytocin modulate the integration of information in the amygdala. BioEssays, 27(9), 869-873.
pmid: 16108061 url:
[15] Finger E. C., Marsh A. A., Mitchell D. G., Reid M. E., Sims C., Budhani S., .. Blair J. R . ( 2008). Abnormal ventromedial prefrontal cortex function in children with psychopathic traits during reversal learning. Archives of General Psychiatry, 65(5), 586-594.
[16] Fite P. J., Rubens S. L., Preddy T. M., Raine A., & Pardini D. A . ( 2014). Reactive/proactive aggression and the development of internalizing problems in males: The moderating effect of parent and peer relationships. Aggressive Behavior, 40(1), 69-78.
pmid: 23868672 url:
[17] Fulwiler C. E., King J. A., & Zhang N. Y . ( 2012). Amygdala- orbitofrontal resting state functional connectivity is associated with trait anger. Neuroreport, 23(10), 606-610.
pmid: 22617448 url:
[18] Gatzke-Kopp L. M., & Beauchaine T. P . ( 2007). Central nervous system substrates of impulsivity: Implications for the development of attention-deficit/hyperactivity disorder and conduct disorder. In D. Coch, G. Dawson, & K. W. Fischer (Eds.), Human behavior, Learning, and the developing brain: Atypical development (pp. 239-263). New York: Guilford.
[19] Gatzke-Kopp L. M., Beauchaine T. P., Shannon K. E., Chipman J., Fleming A. P., Crowell S. E., .. Aylward E . ( 2009). Neurological correlates of reward responding in adolescents with and without externalizing behavior disorders. Journal of Abnormal Psychology, 118(1), 203-213.
pmid: 19222326 url:
[20] Giancola P. R., & Parrott D. J . ( 2008). Further evidence for the validity of the Taylor aggression paradigm. Aggressive Behavior, 34(2), 214-229.
pmid: 17894385 url:
[21] Glenn A. L., & Yang Y. L . ( 2012). The potential role of the striatum in antisocial behavior and psychopathy. Biological Psychiatry, 72(10), 817-822.
pmid: 22672927 url:
[22] Gopal A., Clark E., Allgair A., D'Amato C., Furman M., Gansler D. A., & Fulwiler C . ( 2013). Dorsal/ventral parcellation of the amygdala: Relevance to impulsivity and aggression. Psychiatry Research: Neuroimaging, 211(1), 24-30.
pmid: 23352275 url:
[23] Grahn J. A., Parkinson J. A., & Owen A. M . ( 2009). The role of the basal ganglia in learning and memory: Neuropsychological studies. Behavioural Brain Research, 199(1), 53-60.
pmid: 19059285 url:
[24] Greicius M. D., Flores B. H., Menon V., Glover G. H., Solvason H. B., Kenna H., .. Schatzberg A. F . ( 2007). Resting-state functional connectivity in major depression: Abnormally increased contributions from subgenual cingulate cortex and thalamus. Biological Psychiatry, 62(5), 429-437.
pmid: 17210143 url:
[25] Hahn A., Stein P., Windischberger C., Weissenbacher A., Spindelegger C., Moser E., .. Lanzenberger R . ( 2011). Reduced resting-state functional connectivity between amygdala and orbitofrontal cortex in social anxiety disorder. NeuroImage, 56(3), 881-889.
[26] Hamilton J. P., Chen G., Thomason M. E., Schwartz M. E., & Gotlib I. H . ( 2011). Investigating neural primacy in major depressive disorder: Multivariate Granger causality analysis of resting-state fMRI time-series data. Molecular Psychiatry, 16(7), 763-772.
pmid: 2925061 url:
[27] Herpertz S. C., Nagy K., Ueltzh?ffer K., Schmitt R., Mancke F., Schmahl C., & Bertsch K . ( 2017). Brain mechanisms underlying reactive aggression in borderline personality disorder—Sex matters. Biological Psychiatry, 82(4), 257-266.
pmid: 28388995 url:
[28] Hoptman M. J., D'Angelo D., Catalano D., Mauro C. J., Shehzad Z. E., Kelly A. M. C., .. Milham M. P . ( 2010). Amygdalofrontal functional disconnectivity and aggression in schizophrenia. Schizophrenia Bulletin, 36(5), 1020-1028.
pmid: 2930349 url:
[29] Huber D., Veinante P., & Stoop R . ( 2005). Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala. Science, 308(5719), 245-248.
pmid: 15821089 url:
[30] Koenigs M., & Tranel D . ( 2007). Irrational economic decision-making after ventromedial prefrontal damage: Evidence from the ultimatum game. Journal of Neuroscience, 27(4), 951-956.
[31] Kr?mer U. M., Jansma H., Tempelmann C., & Münte T. F . ( 2007). Tit-for-tat: The neural basis of reactive aggression. NeuroImage, 38(1), 203-211.
pmid: 17765572 url:
[32] Kr?mer U. M., Riba J., Richter S., & Münte T. F . ( 2011). An fMRI study on the role of serotonin in reactive aggression. PLoS One, 6(11), e27668.
[33] LeDoux, J. ( 1998). Fear and the brain: Where have we been, and where are we going? Biological Psychiatry, 44(12), 1229-1238.
pmid: 9861466 url:
[34] LeDoux, J. E . ( 2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, 155-184.
[35] Lee G. P., Bechara A., Adolphs R., Arena J., Meador K. J., Loring D. W., & Smith J. R . ( 1998). Clinical and physiological effects of stereotaxic bilateral amygdalotomy for intractable aggression. The Journal of Neuropsychiatry and Clinical Neurosciences, 10(4), 413-420.
pmid: 9813786 url:
[36] Liu Y. L., Teng Z. J., Lan H. Y., Zhang X., & Yao D. Z . ( 2015). Short-term effects of prosocial video games on aggression: An event-related potential study. Frontiers in Behavioral Neuroscience, 9, 193.
pmid: 4513560 url:
[37] Lotze M., Veit R., Anders S., & Birbaumer N . ( 2007). Evidence for a different role of the ventral and dorsal medial prefrontal cortex for social reactive aggression: An interactive fMRI study. NeuroImage, 34(1), 470-478.
pmid: 17071110 url:
[38] Maren, S. ( 2001). Neurobiology of Pavlovian fear conditioning. Annual Review of Neuroscience, 24, 897-931.
pmid: 11520922 url:
[39] Mark V. H., Sweet W., & Ervin F . ( 1975). Deep temporal lobe stimulation and destructive lesions in episodically violent temporal lobe epileptics. In W. Fields & W. Sweet (Eds.), Neural bases of violence and aggression (pp. 379-400). St. Louis: Warren H. Greem, Inc.
[40] McCloskey M. S., Phan K. L., Angstadt M., Fettich K. C., Keedy S., & Coccaro E. F . ( 2016). Amygdala hyperactivation to angry faces in intermittent explosive disorder. Journal of Psychiatric Research, 79, 34-41.
pmid: 27145325 url:
[41] McEwen C. A., & McEwen B. S . ( 2017). Social structure, adversity, toxic stress, and intergenerational poverty: An early childhood model. Annual Review of Sociology, 43, 445-472.
[42] Motzkin J. C., Newman J. P., Kiehl K. A., & Koenigs M . ( 2011). Reduced prefrontal connectivity in psychopathy. Journal of Neuroscience, 31(48), 17348-17357.
pmid: 3311922 url:
[43] Narabayashi H., Nagao T., Saito Y., Yoshida M., & Nagahata M . ( 1963). Stereotaxic amygdalotomy for behavior disorders. Archives of Neurology, 9(1), 1-16.
pmid: 13937583 url:
[44] Nelson R. J., & Trainor B. C . ( 2007). Neural mechanisms of aggression. Nature Reviews Neuroscience, 8(7), 536-546.
[45] New A. S., Hazlett E. A., Buchsbaum M. S., Goodman M., Mitelman S. A., Newmark R., .. Siever L. J . ( 2007). Amygdala-prefrontal disconnection in borderline personality disorder. Neuropsychopharmacology, 32(7), 1629-1640.
[46] Pietrini P., Guazzelli M., Basso G., Jaffe K., & Grafman J . ( 2000). Neural correlates of imaginal aggressive behavior assessed by positron emission tomography in healthy subjects. American Journal of Psychiatry, 157(11), 1772-1781.
[47] Ramirez J. M., & Andreu J. M . ( 2006). Aggression, and some related psychological constructs (anger, hostility, and impulsivity) Some comments from a research project. Neuroscience and Biobehavioral Reviews, 30(3), 276-291.
pmid: 16081158 url:
[48] Riva P., Gabbiadini A., Lauro L. J. R., Andrighetto L., Volpato C., & Bushman B. J . ( 2017). Neuromodulation can reduce aggressive behavior elicited by violent video games. Cognitive, Affective, and Behavioral Neuroscience, 17(2), 452-459.
[49] Rosell D. R., & Siever L. J . ( 2015). The neurobiology of aggression and violence. CNS Spectrums, 20(3), 254-279.
pmid: 25936249 url:
[50] Rudebeck P. H., Bannerman D. M., & Rushworth M. F. S . ( 2008). The contribution of distinct subregions of the ventromedial frontal cortex to emotion, social behavior, and decision making. Cognitive, Affective, and Behavioral Neuroscience, 8(4), 485-497.
pmid: 19033243 url:
[51] Sagvolden T., Johansen E. B., Aase H., & Russell V. A . ( 2005). A dynamic developmental theory of attention- deficit/hyperactivity disorder (ADHD) predominantly hyperactive/impulsive and combined subtypes. Behavioral and Brain Sciences, 28(3), 397-419.
pmid: 16209748 url:
[52] Sah P., Faber E. S. L., Lopez de Lopez M., & Power J. P . ( 2003). The amygdaloid complex: Anatomy and physiology. Physiological Reviews, 83(3), 803-834.
pmid: 12843409 url:
[53] Shannon K. E., Sauder C., Beauchaine T. P., & Gatzke-Kopp L. M . ( 2009). Disrupted effective connectivity between the medial frontal cortex and the caudate in adolescent boys with externalizing behavior disorders. Criminal Justice and Behavior, 36(11), 1141-1157.
[54] Siever, L. J . ( 2008). Neurobiology of aggression and violence. American Journal of Psychiatry, 165(4), 429-442.
pmid: 18346997 url:
[55] Song X. W., Dong Z. Y., Long X. Y., Li S. F., Zuo X. N., Zhu C. Z., .. Zang Y. F . ( 2011). REST: A toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One, 6(9), e25031.
pmid: 3176805 url:
[56] Takeuchi H., Taki Y., Hashizume H., Sassa Y., Nagase T., Nouchi R., & Kawashima R . ( 2012). The association between resting functional connectivity and creativity. Cerebral Cortex, 22(12), 2921-2929.
pmid: 22235031 url:
[57] Taylor, S. P . ( 1967). Aggressive behavior and physiological arousal as a function of provocation and the tendency to inhibit aggression. Journal of Personality, 35(2), 297-310.
pmid: 6059850 url:
[58] Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., .. Joliot M . ( 2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15(1), 273-289.
pmid: 1177199511771995 url:
[59] V?llm B., Richardson P., McKie S., Elliott R., Dolan M., & Deakin B . ( 2007). Neuronal correlates of reward and loss in cluster B personality disorders: A functional magnetic resonance imaging study. Psychiatry Research: Neuroimaging, 156(2), 151-167.
pmid: 17920821 url:
[60] Wu Q. Z., Li D. M., Kuang W. H., Zhang T. J., Lui S., Huang X. Q., .. Gong Q. Y . ( 2011). Abnormal regional spontaneous neural activity in treatment-refractory depression revealed by resting-state fMRI. Human Brain Mapping, 32(8), 1290-1299.
pmid: 20665717 url:
[61] Yan C. G., & Zang Y. F . ( 2010). DPARSF: A MATLAB toolbox for “pipeline” data analysis of resting-state fMRI. Frontiers in Systems Neuroscience, 413.
pmid: 2889691 url:
[62] Zeng L. L., Shen H., Liu L., Wang L. B., Li B. J., Fang P., .. Hu D. W . ( 2012). Identifying major depression using whole-brain functional connectivity: A multivariate pattern analysis. Brain, 135(5), 1498-1507.
pmid: 22418737 url:
[63] Zink C. F., Pagnoni G., Martin M. E., Dhamala M., & Berns G. S . ( 2003). Human striatal response to salient nonrewarding stimuli. Journal of Neuroscience, 23(22), 8092-8097.
pmid: 12954871 url:
[64] Zink C. F., Pagnoni G., Martin-Skurski M. E., Chappelow J. C., & Berns G. S . ( 2004). Human striatal responses to monetary reward depend on saliency. Neuron, 42(3), 509-517.
pmid: 15134646 url:
[65] Zuo X. N., Di Martino A., Kelly C., Shehzad Z. E., Gee D. G., Klein D. F., .. Milham M. P . ( 2010). The oscillating brain: Complex and reliable. NeuroImage, 49(2), 1432-1445.
pmid: 2856476 url:
[1] LI WenFu; TONG DanDan; QIU Jiang; ZHANG QingLin. The neural basis of scientific innovation problems solving[J]. Acta Psychologica Sinica, 2016, 48(4): 331-342.
Full text



Copyright © Acta Psychologica Sinica
Support by Beijing Magtech