Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-24T06:37:23.926Z Has data issue: false hasContentIssue false
  • English
  • Français

Role of Reversal Learning Impairment in Social Disinhibition following Severe Traumatic Brain Injury

Published online by Cambridge University Press:  12 January 2016

Katherine Osborne-Crowley ,
Skye McDonald  and
Jacqueline A. Rushby
Katherine Osborne-Crowley*
Affiliation:
School of Psychology, The University of New South Wales, New South Wales, Australia
Skye McDonald
Affiliation:
School of Psychology, The University of New South Wales, New South Wales, Australia
Jacqueline A. Rushby
Affiliation:
School of Psychology, The University of New South Wales, New South Wales, Australia
*
Correspondence and reprint requests to: Katherine Osborne-Crowley, School of Psychology, The University of New South Wales, New South Wales, 2052, Australia. E-mail: k.osbornecrowley@unsw.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

Objectives: The current study aimed to determine whether reversal learning impairments and feedback-related negativity (FRN), reflecting reward prediction error signals generated by negative feedback during the reversal learning tasks, were associated with social disinhibition in a group of participants with traumatic brain injury (TBI). Methods: Number of reversal errors on a social and a non-social reversal learning task and FRN were examined for 21 participants with TBI and 21 control participants matched for age. Participants with TBI were also divided into low and high disinhibition groups based on rated videotaped interviews. Results: Participants with TBI made more reversal errors and produced smaller amplitude FRNs than controls. Furthermore, participants with TBI high on social disinhibition made more reversal errors on the social reversal learning task than did those low on social disinhibition. FRN amplitude was not related to disinhibition. Conclusions: These results suggest that impairment in the ability to update behavior when social reinforcement contingencies change plays a role in social disinhibition after TBI. Furthermore, the social reversal learning task used in this study may be a useful neuropsychological tool for detecting susceptibility to acquired social disinhibition following TBI. Finally, that the FRN amplitude was not associated with social disinhibition suggests that reward prediction error signals are not critical for behavioral adaptation in the social domain. (JINS, 2016, 21, 303–313)

Keywords

Brain injuriesSocial disinhibitionOrbitofrontal cortex (OFC)Reversal learningSocial reinforcementFeedback-related negativity (FRN)Reward prediction error
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 22 , Issue 3 , March 2016 , pp. 303 - 313
Copyright
Copyright © The International Neuropsychological Society 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adolphs, R., Damasio, H., Tranel, D., & Damasio, A.R. (1996). Cortical systems for the recognition of emotion in facial expressions. The Journal of Neuroscience, 16(23), 7678–7687.Google Scholar
Arciniegas, D.B., & Wortzel, H.S. (2014). Emotional and behavioral dyscontrol after traumatic brain injury. Psychiatric Clinics of North America, 37(1), 31–53. doi:10.1016/j.psc.2013.12.001 Google Scholar
Bachevalier, J., & Loveland, K.A. (2006). The orbitofrontal–amygdala circuit and self-regulation of social–emotional behavior in autism. Neuroscience & Biobehavioral Reviews, 30(1), 97–117. doi:10.1016/j.neubiorev.2005.07.002 Google Scholar
Barrash, J., Tranel, D., & Anderson, S.W. (2000). Acquired personality disturbances associated with bilateral damage to the ventromedial prefrontal region. Developmental Neuropsychology, 18(3), 355–381. doi:10.1207/S1532694205Barrash CrossRefGoogle Scholar
Beer, J.S., John, O.P., Scabini, D., & Knight, R.T. (2006). Orbitofrontal cortex and social behavior: Integrating self-monitoring and emotion-cognition interactions. Journal of Cognitive Neuroscience, 18(6), 871–879. doi:10.1162/jocn.2006.18.6.871 CrossRefGoogle ScholarPubMed
Benson, P.J., & Perrett, D.I. (1991). Perception and recognition of photographic quality facial caricatures: Implications for the recognition of natural images. European Journal of Cognitive Psychology, 3(1), 105–135. doi:10.1080/09541449108406222 Google Scholar
Bigler, E.D. (2007). Anterior and middle cranial fossa in traumatic brain injury: Relevant neuroanatomy and neuropathology in the study of neuropsychological outcome. Neuropsychology, 21(5), 515–531. doi:10.1037/0894-4105.21.5.515 17784800 Google Scholar
Blair, R.J.R., & Cipolotti, L. (2000). Impaired social response reversal ‘A case of acquired sociopathy’. Brain, 123(6), 1122–1141. doi:10.1093/brain/123.6.1122 Google Scholar
Boksem, M.A., & De Cremer, D. (2010). Fairness concerns predict medial frontal negativity amplitude in ultimatum bargaining. Social Neuroscience, 5(1), 118–128. doi:10.1080/17470910903202666 Google Scholar
Brooks, N., & McKinlay, W. (1983). Personality and behavioural change after severe blunt head injury - A relative’s view. Journal of Neurology, Neurosurgery, & Psychiatry, 46(4), 336–344. doi:10.1136/jnnp.46.4.336 Google Scholar
Butter, C.M., Mishkin, M., & Mirsky, A.F. (1968). Emotional responses toward humans in monkeys with selective frontal lesions. Physiology & Behavior, 3(2), 213–215. doi:10.1016/0031-9384(68)90087-5 Google Scholar
Chase, H.W., Swainson, R., Durham, L., Benham, L., & Cools, R. (2011). Feedback-related negativity codes prediction error but not behavioral adjustment during probabilistic reversal learning. Journal of Cognitive Neuroscience, 23(4), 936–946. doi:10.1162/jocn.2010.21456 Google Scholar
Cicerone, K.D., & Tanenbaum, L.N. (1997). Disturbance of social cognition after traumatic orbitofrontal brain injury. Archives of Clinical Neuropsychology, 12(2), 173–188. doi:10.1093/arclin/12.2.173 Google Scholar
Cohen, M.X., & Ranganath, C. (2007). Reinforcement learning signals predict future decisions. The Journal of Neuroscience, 27(2), 371–378. doi:10.1523/JNEUROSCI.4421-06.2007 Google Scholar
Corrigan, J.D., Selassie, A.W., & Orman, J.A.L. (2010). The epidemiology of traumatic brain injury. The Journal of Head Trauma Rehabilitation, 25(2), 72–80. doi:10.1097/HTR.0b013e3181ccc8b4 Google Scholar
Cramer, D., & Howitt, D. (2004). The Sage dictionary of statistics: A practical resource for students in the social sciences. Thousand Oaks: Sage.CrossRefGoogle Scholar
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. doi:10.1126/science.8178168 CrossRefGoogle ScholarPubMed
Demaree, H.A., Everhart, D.E., Youngstrom, E.A., & Harrison, D.W. (2005). Brain lateralization of emotional processing: historical roots and a future incorporating “dominance”. Behavioral and Cognitive Neuroscience Reviews, 4(1), 3–20.Google Scholar
Dias, R., Robbins, T., & Roberts, A.C. (1997). Dissociable forms of inhibitory control within prefrontal cortex with an analog of the Wisconsin Card Sort Test: Restriction to novel situations and independence from “on-line” processing. The Journal of Neuroscience, 17(23), 9285–9297.CrossRefGoogle ScholarPubMed
Fellows, L.K., & Farah, M.J. (2003). Ventromedial frontal cortex mediates affective shifting in humans: Evidence from a reversal learning paradigm. Brain, 126(8), 1830–1837. doi:10.1093/brain/awg180 CrossRefGoogle ScholarPubMed
Franzen, E., & Myers, R. (1973). Neural control of social behavior: Prefrontal and anterior temporal cortex. Neuropsychologia, 11(2), 141–157. doi:10.1016/0028-3932(73)90002-X CrossRefGoogle ScholarPubMed
Gehring, W.J., & Willoughby, A.R. (2004). Are all medial frontal negativities created equal? Toward a richer empirical basis for theories of action monitoring. Errors, Conflicts, and the Brain. Current Opinions on Performance Monitoring, 14–20.Google Scholar
Gottfried, J.A., O’Doherty, J., & Dolan, R.J. (2003). Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science, 301(5636), 1104–1107. doi:10.1126/science.1087919 Google Scholar
Gould, K.R., Ponsford, J.L., Johnston, L., & Schonberger, M. (2011). Relationship between psychiatric disorders and 1-year psychosocial outcome following traumatic brain injury. Journal of Head Trauma Rehabilitation, 26(1), 79–89. doi:10.1097/Htr.0b013e3182036799 CrossRefGoogle ScholarPubMed
Gregory, C.A., Serra-Mestres, J., & Hodges, J.R. (1999). Early diagnosis of the frontal variant of frontotemporal dementia: How sensitive are standard neuroimaging and neuropsychologic tests? Cognitive and Behavioral Neurology, 12(2), 128–135.Google Scholar
Hajcak, G., Moser, J.S., Holroyd, C.B., & Simons, R.F. (2006). The feedback-related negativity reflects the binary evaluation of good versus bad outcomes. Biological Psychology, 71(2), 148–154. doi:10.1016/j.biopsycho.2005.04.001 CrossRefGoogle ScholarPubMed
Hajcak, G., Moser, J.S., Holroyd, C.B., & Simons, R.F. (2007). It’s worse than you thought: The feedback negativity and violations of reward prediction in gambling tasks. Psychophysiology, 44(6), 905–912. doi:10.1111/j.1469-8986.2007.00567.x Google Scholar
Heberlein, A.S., Padon, A.A., Gillihan, S.J., Farah, M.J., & Fellows, L.K. (2008). Ventromedial frontal lobe plays a critical role in facial emotion recognition. Journal of Cognitive Neuroscience, 20(4), 721–733. doi:10.1162/jocn.2008.20049 Google Scholar
Hikosaka, K., & Watanabe, M. (2004). Long‐and short‐range reward expectancy in the primate orbitofrontal cortex. European Journal of Neuroscience, 19(4), 1046–1054. doi:10.1111/j.0953-816X.2004.03120.x Google Scholar
Holroyd, C.B., & Coles, M.G.H. (2002). The neural basis of human error processing: Reinforcement learning, dopamine, and the error-related negativity. Psychological Review, 109(4), 679–709. doi:10.1037/0033-295X.109.4.679 12374324 Google Scholar
Holroyd, C.B., & Krigolson, O.E. (2007). Reward prediction error signals associated with a modified time estimation task. Psychophysiology, 44(6), 913–917. doi:10.1111/j.1469-8986.2007.00561.x Google Scholar
Holroyd, C.B., Krigolson, O.E., Baker, R., Lee, S., & Gibson, J. (2009). When is an error not a prediction error? An electrophysiological investigation. Cognitive, Affective, & Behavioral Neuroscience, 9(1), 59–70. doi:10.3758/CABN.9.1.59 CrossRefGoogle Scholar
Holroyd, C.B., Larsen, J.T., & Cohen, J.D. (2004). Context dependence of the event‐related brain potential associated with reward and punishment. Psychophysiology, 41(2), 245–253. doi:10.1111/j.1469-8986.2004.00152.x Google Scholar
Holroyd, C.B., Nieuwenhuis, S., Yeung, N., & Cohen, J.D. (2003). Errors in reward prediction are reflected in the event-related brain potential. Neuroreport, 14(18), 2481–2484. doi:10.1097/01.wnr.0000099601.41403.a5 CrossRefGoogle ScholarPubMed
Hornak, J., O’Doherty, J., Bramham, J., Rolls, E.T., Morris, R., Bullock, P., &Polkey, C. (2004). Reward-related reversal learning after surgical excisions in orbito-frontal or dorsolateral prefrontal cortex in humans. Journal of Cognitive Neuroscience, 16(3), 463–478. doi:10.1162/089892904322926791 Google Scholar
Hornberger, M., Geng, J., & Hodges, J.R. (2011). Convergent grey and white matter evidence of orbitofrontal cortex changes related to disinhibition in behavioural variant frontotemporal dementia. Brain, 134(9), 2502–2512. doi:10.1093/brain/awr173 Google Scholar
Izquierdo, A., Suda, R.K., & Murray, E.A. (2004). Bilateral orbital prefrontal cortex lesions in rhesus monkeys disrupt choices guided by both reward value and reward contingency. The Journal of Neuroscience, 24(34), 7540–7548. doi:10.1523/JNEUROSCI.1921-04.2004 CrossRefGoogle ScholarPubMed
Kaplan, J.T., & Zaidel, E. (2001). Error monitoring in the hemispheres: The effect of lateralized feedback on lexical decision. Cognition, 82(2), 157–178. doi:10.1016/S0010-0277(01)00150-0 Google Scholar
Kinnunen, K.M., Greenwood, R., Powell, J.H., Leech, R., Hawkins, P.C., Bonnelle, V., & Sharp, D.J. (2011). White matter damage and cognitive impairment after traumatic brain injury. Brain, 134(2), 449–463. doi:10.1093/brain/awq347 Google Scholar
Kringelbach, M.L., & Rolls, E.T. (2003). Neural correlates of rapid reversal learning in a simple model of human social interaction. Neuroimage, 20(2), 1371–1383. doi:10.1016/S1053-8119(03)00393-8 Google Scholar
Krueger, C.E., Laluz, V., Rosen, H.J., Neuhaus, J.M., Miller, B.L., & Kramer, J.H. (2011). Double dissociation in the anatomy of socioemotional disinhibition and executive functioning in dementia. Neuropsychology, 25(2), 249–259. doi:10.1037/a0021681 Google Scholar
Larson, M.J., Kelly, K.G., Stigge-Kaufman, D.A., Schmalfuss, I.M., & Perlstein, W.M. (2007). Reward context sensitivity impairment following severe TBI: An event-related potential investigation. Journal of the International Neuropsychological Society, 13(04), 615–625.Google Scholar
Lipszyc, J., Levin, H., Hanten, G., Hunter, J., Dennis, M., & Schachar, R. (2014). Frontal white matter damage impairs response inhibition in children following traumatic brain injury. Archives of Clinical Neuropsychology, 29(3), 289–299. doi:10.1093/arclin/acu004 Google Scholar
Lovibond, P.F., & Lovibond, S.H. (1995). The structure of negative emotional states: Comparison of the Depression Anxiety Stress Scales (DASS) with the Beck Depression and Anxiety Inventories. Behaviour Research and Therapy, 33(3), 335–343. doi:10.1016/0005-7967(94)00075-U Google Scholar
Luu, P., Tucker, D.M., Derryberry, D., Reed, M., & Poulsen, C. (2003). Electrophysiological responses to errors and feedback in the process of action regulation. Psychological Science, 14(1), 47–53. doi:10.1111/1467-9280.01417 12564753 Google Scholar
Machado, C.J., & Bachevalier, J. (2006). The impact of selective amygdala, orbital frontal cortex, or hippocampal formation lesions on established social relationships in rhesus monkeys (Macaca mulatta). Behavioral Neuroscience, 120(4), 761–786. doi:10.1037/0735-7044.120.4.761 Google Scholar
Mattson, A.J., & Levin, H.S. (1990). Frontal lobe dysfunction following closed head injury. A review of the literature. The Journal of Nervous and Mental Disease, 178(5), 282–291.Google Scholar
McKinlay, W., Brooks, N., Bond, M., Martinage, D., & Marshall, M. (1981). The short-term outcome of severe blunt head injury as reported by relatives of the injured persons. Journal of Neurology, Neurosurgery, & Psychiatry, 44(6), 527–533. doi:10.1136/jnnp.44.6.527 Google Scholar
Montagne, B., Kessels, R.P.C., De Haan, E.H.F., & Perrett, D.I. (2007). The emotion recognition task: A paradigm to measure the perception of facial emotional expressions at different intensities. Perceptual and Motor Skills, 104(2), 589–598. doi:10.2466/Pms.104.2.589-598 Google Scholar
Nakamura, K., Kawashima, R., Ito, K., Sugiura, M., Kato, T., Nakamura, A., & Fukuda, H. (1999). Activation of the right inferior frontal cortex during assessment of facial emotion. Journal of Neurophysiology, 82(3), 1610–1614.Google Scholar
Namiki, C., Yamada, M., Yoshida, H., Hanakawa, T., Fukuyama, H., & Murai, T. (2008). Small orbitofrontal traumatic lesions detected by high resolution MRI in a patient with major behavioural changes. Neurocase, 14(6), 474–479. doi:10.1080/13554790802459494 Google Scholar
Nieuwenhuis, S., Holroyd, C.B., Mol, N., & Coles, M.G. (2004). Reinforcement-related brain potentials from medial frontal cortex: Origins and functional significance. Neuroscience & Biobehavioral Reviews, 28(4), 441–448. doi:10.1016/j.neubiorev.2004.05.003 Google Scholar
Padoa-Schioppa, C., & Assad, J.A. (2006). Neurons in the orbitofrontal cortex encode economic value. Nature, 441(7090), 223–226. doi:10.1038/nature04676 Google Scholar
Rahman, S., Sahakian, B.J., Hodges, J.R., Rogers, R.D., & Robbins, T.W. (1999). Specific cognitive deficits in mild frontal variant frontotemporal dementia. Brain, 122(8), 1469–1493. doi:10.1093/brain/122.8.1469 Google Scholar
Rolls, E.T., Hornak, J., Wade, D., & McGrath, J. (1994). Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. Journal of Neurology, Neurosurgery, & Psychiatry, 57(12), 1518–1524. doi:10.1136/jnnp.57.12.1518 Google Scholar
Rosenberg, H., McDonald, S., Dethier, M., Kessels, R.P.C., & Westbrook, R.F. (2014). Facial emotion recognition deficits following moderate-severe traumatic brain injury (TBI): Re-examining the valence effect and the role of emotion intensity. Journal of the International Neuropsychological Society, 20(10), 994–1003. doi:10.1017/S1355617714000940 Google Scholar
Russell, W.R., & Smith, A. (1961). Post-traumatic amnesia in closed head injury. Archives of Neurology, 5(1), 4–17.Google Scholar
Sambrook, T.D., & Goslin, J. (2015). A neural reward prediction error revealed by a meta-analysis of ERPs using great grand averages. Psychological Bulletin, 141(1), 213–235. doi:10.1037/bul0000006 Google Scholar
Schoenbaum, G., Nugent, S.L., Saddoris, M.P., & Setlow, B. (2002). Orbitofrontal lesions in rats impair reversal but not acquisition of go, no-go odor discriminations. Neuroreport, 13(6), 885–890.Google Scholar
Schoenbaum, G., Roesch, M.R., Stalnaker, T.A., & Takahashi, Y.K. (2009). A new perspective on the role of the orbitofrontal cortex in adaptive behaviour. Nature Reviews. Neuroscience, 10(12), 885–892. doi:10.1038/nrn2753 Google Scholar
Schoenbaum, G., Takahashi, Y., Liu, T.L., & McDannald, M.A. (2011). Does the orbitofrontal cortex signal value? Annals of the New York Academy of Sciences, 1239(1), 87–99. doi:10.1111/j.1749-6632.2011.06210.x Google Scholar
Semlitsch, H.V., Anderer, P., Schuster, P., & Presslich, O. (1986). A solution for reliable and valid reduction of ocular artifacts, applied to the P300 ERP. Psychophysiology, 23(6), 695–703. doi:10.1111/j.1469-8986.1986.tb00696.x Google Scholar
Tate, R.L., Broe, G.A., & Lulham, J.M. (1989). Impairment after severe blunt head-injury - The results from a consecutive series of 100 patients. Acta Neurologica Scandinavica, 79(2), 97–107. doi:10.1111/j.1600-0404.1989.tb03719.x CrossRefGoogle ScholarPubMed
van der Helden, J., Boksem, M.A., & Blom, J.H. (2010). The importance of failure: Feedback-related negativity predicts motor learning efficiency. Cerebral Cortex, 20(7), 1596–1603. doi:10.1093/cercor/bhp224 Google Scholar
Walsh, M.M., & Anderson, J.R. (2011a). Learning from delayed feedback: Neural responses in temporal credit assignment. Cognitive, Affective, & Behavioral Neuroscience, 11(2), 131–143. doi:10.3758/s13415-011-0027-0 Google Scholar
Walsh, M.M., & Anderson, J.R. (2011b). Modulation of the feedback-related negativity by instruction and experience. Proceedings of the National Academy of Sciences of the United States of America, 108(47), 19048–19053. doi:10.1073/pnas.1117189108 Google Scholar
Yasuda, A., Sato, A., Miyawaki, K., Kumano, H., & Kuboki, T. (2004). Error-related negativity reflects detection of negative reward prediction error. Neuroreport, 15(16), 2561–2565.Google Scholar