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Left or right temporal lesion might induce aggression or escape during awake surgery, respectively: role of the amygdala

Published online by Cambridge University Press:  24 June 2014

Nobusada Shinoura*
Affiliation:
Department of Neurosurgery, Komagome Metropolitan Hospital, Tokyo, Japan
Ryozi Yamada
Affiliation:
Department of Neurosurgery, Komagome Metropolitan Hospital, Tokyo, Japan
Yusuke Tabei
Affiliation:
Department of Neurosurgery, Komagome Metropolitan Hospital, Tokyo, Japan
Ryohei Otani
Affiliation:
Department of Neurosurgery, Komagome Metropolitan Hospital, Tokyo, Japan
Chihiro Itoi
Affiliation:
Department of Psychology, Chuo University of Literature, Tokyo, Japan
Seiko Saito
Affiliation:
Department of Psychology, Chuo University of Literature, Tokyo, Japan
Akira Midorikawa
Affiliation:
Department of Psychology, Chuo University of Literature, Tokyo, Japan
*
Nobusada Shinoura, Department of Neurosurgery, Komagome Metropolitan Hospital, 3-18-22 Hon-komagome, Bunkyo-ku, Tokyo 113-8677, Japan. Tel: +81 3 3823 2101; Fax: +81 3 3824 1552; E-mail: shinoura@cick.jp

Extract

Objective: Some patients with temporal lobe brain tumours show aggressive or escape behaviour during awake surgery. As the amygdala plays a critical role in coping with stress, we evaluated whether the left or right amygdala was involved in aggressive or escape behaviour in six patients undergoing awake surgery for temporal lobe brain tumours.

Methods: Brain tumours were located in the left temporal lobe in cases 1–3 and in the right temporal lobe in cases 4–6. In cases 1, 2, 4 and 5, the tumours invaded the amygdala.

Results: In case 1, the patient showed aggressive behaviour before partial removal of the left amygdala during awake surgery; just after partial removal of left amygdala, the patient was calm and cooperative. In case 2, the patient showed aggressive behaviour when the tumour near the left amygdala was removed. In case 3, the patient showed aggressive behaviour when awakening during awake surgery. In case 4, the patient showed escape behaviour when removal of the tumour near the right amygdala was initiated. In cases 5 and 6, patients showed escape behaviour upon awakening and upon initiation of tumour removal from the temporal lobe.

Conclusion: In conclusion, these results suggest that left or right temporal lesions might induce aggressive or escape behaviour during awake surgery, respectively, and that the amygdala on the respective side may play a role in these behaviours.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

1.Duffau, H, Lopes, M, Arthuis, F et al. Contribution of intraoperative electrical stimulations in surgery of low grade gliomas: a comparative study between two series without (1985-96) and with (1996-2003) functional mapping in the same institution. J Neurol Neurosurg Psychiat 2005;76:845851.CrossRefGoogle Scholar
2.Sanai, N, Mirzadeh, Z, Berger, MS.Functional outcome after language mapping for glioma resection. N Engl J Med 2008;358:1827.CrossRefGoogle ScholarPubMed
3.Shinoura, N, Yoshida, M, Yamada, R et al. Awake surgery with continuous task for resection of brain tumors in the primary motor area. J Clin Neurosci 2009;16:188194.CrossRefGoogle Scholar
4.Conte, V, Guzzetti, S, Porta, A, Tobaldini, E, Baratta, P, Stocchetti, N.Spectral analysis of heart rate variability during asleep-awake craniotomy for tumor resection. J Neurosurg Anesthesiol 2009;21:242247.CrossRefGoogle ScholarPubMed
5.Rauch, SL, Whalen, PJ, Shin, LM et al. Exaggerated amygdale response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biol Psychiat 2000;47:769776.CrossRefGoogle Scholar
6.Herpertz, SC, Dietrich, TM, Wenning, B et al. Evidence of abnormal amygdale functioning in borderline personality disorder: a functional MRI study. Biol Psychiat 2001;50:292298.CrossRefGoogle Scholar
7.Baas, D, Aleman, A, Kahn, RS.Lateralization of amygdala activation: a systemic review of functional neuroimaging studies. Brain Res Brain Res Rev 2004;45:96103.CrossRefGoogle Scholar
8.Machado, CJ, Kazama, AM, Bachevalier, J.Impact of amygdala, orbital frontal, or hippocampal lesions on threat avoidance and emotional reactivity in nonhuman primates. Emotion 2009;9:147163.CrossRefGoogle ScholarPubMed
9.New, AS, Hazlett, EA, Newmark, RE et al. Laboratory induced aggression: a positron emission tomography study of aggressive individuals with borderline personality disorder. Biol Psychiat 2009;66:11071114.CrossRefGoogle ScholarPubMed
10.Shinoura, N, Yamada, R, Kodama, T, Suzuki, Y, Takahashi, M, Yagi, K.Preoperative fMRI, tractography and continuous task during awake surgery for maintenance of motor function following surgical resection of metastatic tumor spread to the primary motor area. Minim Invasive Neurosurg 2005;48:8590.CrossRefGoogle Scholar
11.Berger, MS, Kincaid, J, Ojemann, GA, Lettich, E.Brain mapping techniques to maximize resection, safety, and seizure control in children with brain tumors. Neurosurgery 1989;25:786792.CrossRefGoogle ScholarPubMed
12.Damasio, H, Grabowski, T, Frank, R, Galaburda, AM, Damasio, AR.The return of Phineas Gage: clues about the brain from the skull of a famous patient. Science 1994;264:11021115.CrossRefGoogle ScholarPubMed
13.Quirk, GJ, Beer, JS.Prefrontal involvement in the regulation of emotion: convergence of rat and human studies. Curr Opin Neurobiol 2006;16:723727.CrossRefGoogle ScholarPubMed
14.Anderson, SW, Barrash, J, Bechara, A, Tranel, D.Impairments of emotion and real-world complex behavior following childhood- or adult-onset damage to ventromedial prefrontal cortex. J Int Neuropsychol Soc 2006;12:224235.CrossRefGoogle ScholarPubMed
15.Kluver, H, Bucy, PC.Psychic blindness and other symptoms following bilateral temporal lobectomy in rhesus monkeys. Am J Physiol 1937;119:352353.Google Scholar
16.Hitchcock, J, Davis, M.Lesions of the amygdala, but not cerebellum or red nucleus, block conditioned fear as measured with the potentiated startle paradigm. Behav Neurosci 1986;100:1122.CrossRefGoogle ScholarPubMed
17.Tranel, D, Hyman, BT.Neuropsychological correlates of bilateral amygdala damage. Arch Neurol 1990;47:349355.CrossRefGoogle ScholarPubMed
18.Buchanan, TW, Tranel, D, Adolphs, R.Anteromedial temporal lobe damage blocks startle modulation by fear and disgust. Behav Neurosci 2004;118:429437.CrossRefGoogle ScholarPubMed
19.Meletti, S, Tassi, L, Mai, R, Fini, N, Tassinari, CA, Russo, GL.Emotions induced by intracerebral electrical stimulation of the temporal lobe. Epilepsia 2006;47:4751.CrossRefGoogle ScholarPubMed
20.Kohler, CG, Carran, MA, Bilker, W, O'Connor, MJ, Sperling, MR.Association of fear auras with mood and anxiety disorders after temporal lobectomy. Epilepsia 2001;42:674681.CrossRefGoogle ScholarPubMed
21.Donegan, NH, Sanislow, CA, Blumberg, HP et al. Amygdala hyperreactivity in borderline personality disorder: implications for emotional dysregulation. Biol Psychiat 2003;54:12841293.CrossRefGoogle ScholarPubMed
22.van Elst, LT, Woermann, FG, Lemieux, L, Thompson, PJ, Trimble, MR.Affective aggression in patients with temporal lobe epilepsy: a quantitative MRI study of the amgdala. Brain 2000;123:234243.CrossRefGoogle Scholar
23.Sachdev, P, Smith, JS, Matheson, J, Last, P, Blumbergs, P.Amygdalo-hippocampectomy for pathological aggression. Aust Nz J Psychiat 1992;26:671676.CrossRefGoogle ScholarPubMed
24.Meunier, M, Bachevalier, J, Murray, EA, Malkova, L, Mishkin, M.Effects of aspiration versus neurotoxic lesions of the amygdala on emotional responses in monkeys. Eur J Neurosci 1999;11:44034418.CrossRefGoogle ScholarPubMed
25.Machado, CJ, Emery, NJ, Capitanio, JP, Mason, WA, Mendoza, SP, Amaral, DG.Bilateral neurotoxic amygdale lesions in rhesus monkeys (Macaca mulatto): consistent pattern of behavior across different social contexts. Behav Neurosci 2008;122:251266.CrossRefGoogle Scholar
26.Adolphs, R, Tranel, D, Denburg, N.Impaired emotional declarative memory following unilateral amygdale damage. Learn Memory 2000;7:180186.CrossRefGoogle Scholar
27.Smith, SD, Abou-Khalil, B, Zald, DH.Posttraumatic stress disorder in a patient with no left amygdale. J Abnorm Psychol 2008;117:479484.CrossRefGoogle Scholar
28.Anderson, AK, Spencer, DD, Fulbright, RK, Phelps, EA.Contribution of the anteromedial temporal lobes to the evaluation of facial emotion. Neuropsychology 2000;14:526536.CrossRefGoogle Scholar
29.Monkul, ES, Hatch, JP, Nicoletti, MA et al. Fronto-limbic brain structures in suicidal and non-suicidal female patients with major depressive disorder. Mol Psychiatr 2007;12:360366.CrossRefGoogle ScholarPubMed
30.Zald, DH, Lee, JT, Fluegel, KW, Pardo, JV.Aversive gustatory stimulation activates limbic circuits in humans. Brain 1998;121:11431154.CrossRefGoogle ScholarPubMed
31.Coleman-Mesches, K, McGaugh, JL.Differential effects of pretraining inactivation of the right or left amygdala on retention of inhibitory avoidance training. Behav Neurosci 1995;109:642647.CrossRefGoogle ScholarPubMed
32.Adamec, RE, Blundell, J, Collins, A.Neural plasticity and stress induced changes in defense in the rat. Neurosci Biobehav Rev 2001;25:721744.CrossRefGoogle ScholarPubMed