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Emotions and Their Cognitive Control in Children With Cerebellar Tumors

Published online by Cambridge University Press:  04 October 2010

TALAR HOPYAN*
Affiliation:
Program in Neurosciences and Mental Health, Hospital for Sick Children, Toronto, Ontario, Canada Department of Otolaryngology, Hospital for Sick Children, Toronto, Ontario, Canada Department of Psychology, University of Toronto, Toronto, Ontario, Canada
SUZANNE LAUGHLIN
Affiliation:
Program in Neurosciences and Mental Health, Hospital for Sick Children, Toronto, Ontario, Canada Department Diagnostic Imaging, Hospital for Sick Children, Toronto, Ontario, Canada
MAUREEN DENNIS
Affiliation:
Program in Neurosciences and Mental Health, Hospital for Sick Children, Toronto, Ontario, Canada Department of Psychology, University of Toronto, Toronto, Ontario, Canada Department of Surgery, University of Toronto, Toronto, Ontario, Canada
*
*Correspondence and reprint requests to: Talar Hopyan, Program in Neurosciences and Mental Health, Department of Otolaryngology, The Hospital for Sick Children, 555 University Avenue, Toronto, Ontario, M5G 1X8, Canada. Email: t.hopyan@utoronto.ca

Abstract

A constellation of deficits, termed the cerebellar cognitive affective syndrome (CCAS), has been reported following acquired cerebellar lesions. We studied emotion identification and the cognitive control of emotion in children treated for acquired tumors of the cerebellum. Participants were 37 children (7–16 years) treated for cerebellar tumors (19 benign astrocytomas (AST), 18 malignant medulloblastomas (MB), and 37 matched controls (CON). The Emotion Identification Task investigated recognition of happy and sad emotions in music. In two cognitive control tasks, we investigated whether children could identify emotion in situations in which the emotion in the music and the emotion in the lyrics was either congruent or incongruent. Children with cerebellar tumors identified emotion as accurately and quickly as controls (p > .05), although there was a significant interaction of emotions and group (p < .01), with the MB group performing less accurately identifying sad emotions, and both cerebellar tumor groups were impaired in the cognitive control of emotions (p < .01). The fact that childhood acquired cerebellar tumors disrupt cognitive control of emotion rather than emotion identification provides some support for a model of the CCAS as a disorder, not so much of emotion as of the regulation of emotion by cognition. (JINS, 2010, 16, 1027–1038.)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2010

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References

REFERENCES

Aarsen, F.K., Van Dongen, H.R., Paquier, P.F., Van Mourik, M., Catsman-Berrevoets, C.E. (2004). Long-term sequelae in children after cerebellar astrocytoma surgery. Neurology, 62, 13111316.CrossRefGoogle ScholarPubMed
Baillieux, H., De Smet, H.J., Dobbeleir, A., Paquier, P.F., De Deyn, P.P., & Mariën, P. (2010). Cognitive and affective disturbances following focal cerebellar damage in adults: A neuropsychological and SPECT study. Cortex, 46, 869879.CrossRefGoogle ScholarPubMed
Balkwill, L.L., & Thompson, W.F. (1999). A cross-cultural investigation of the perception of emotion in music: Psychophysical and cultural cues. Music Perception, 17, 4364.CrossRefGoogle Scholar
Bigand, E., Filipic, S., & Lalitte, P. (2005). The time course of emotional responses to music. Annals of the New York Academy of Sciences, 1060, 429437.CrossRefGoogle ScholarPubMed
Blood, A.J. & Zatorre, R.J. (2001). Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion. Proceedings of the National Academy of Sciences of the United States of America, 98, 1181811823.CrossRefGoogle ScholarPubMed
Blood, A.J., Zatorre, R.J., Bermudez, P., & Evans, A.C. (1999). Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions. Nature Neuroscience, 2, 382387.CrossRefGoogle ScholarPubMed
Brown, S., Martinez, M.J., & Parsons, L.M. (2004). Passive music listening spontaneously engages limbic and paralimbic systems. Neuroreport, 15, 20332037.CrossRefGoogle ScholarPubMed
Callan, D.E., Kawato, M., Parsons, L., & Turner, R. 2007. Speech and song: The role of the cerebellum. The Cerebellum, 6, 321327.CrossRefGoogle Scholar
Copeland, D.R., deMoor, C., Moore, B.D. 3rd & Ater, J.L. (1999). Neurocognitive development of children after a cerebellar tumor in infancy: A longitudinal study. Journal of Clinical Oncology, 17, 34763486.CrossRefGoogle ScholarPubMed
Dalla Bella, S., Peretz, I., Rousseau, L., & Gosselin, N. (2001). A developmental study of the affective value of tempo and mode in music. Cognition, 80, B1B10.CrossRefGoogle ScholarPubMed
Dennis, M., Spiegler, B.J., Hetherington, C.R., & Greenberg, M.L. (1996). Neuropsychological sequelae of the treatment of children with medulloblastoma. Journal of Neuro-Oncology, 29, 91101.CrossRefGoogle ScholarPubMed
Dennis, M., Edelstein, K., Hetherington, R., Copeland, K., Frederick, J., Blaser, S.E., et al. (2004). Neurobiology of perceptual and motor timing in children with spina bifida in relation to cerebellar volume. Brain, 127, 12921301.CrossRefGoogle ScholarPubMed
Dennis, M., Hopyan, T., Juranek, J., Cirino, P.T., Hasan, K.M., & Fletcher, J. (2009). Strong-meter and weak-meter rhythm identification in spina bifida meningomyelocele and volumetric parcellation of rhythm-relevant cerebellar regions. Annals of the New York Academy of Sciences, 1169, 8488.CrossRefGoogle ScholarPubMed
Eprime (Version 1.1) software. Psychology Software Tools, Inc.Google Scholar
Exner, C., Weniger, G., & Eva, I. (2004). Cerebellar lesions in the PICA but not SCA territory impair cognition. Neurology, 63, 21322135.CrossRefGoogle Scholar
Fritz, T., Jentschke, S., Gosselin, N., Sammler, D., Peretz, I., Turner, R., et al. (2009). Universal recognition of three basic emotions in music. Current Biology, 19, 573576.CrossRefGoogle ScholarPubMed
Gabrielsson, A., & Juslin, P. (1996). Emotional expression in music performance: Between the performer’s intention and the listener’s experience. Psychology of Music, 24, 6891.CrossRefGoogle Scholar
Glickstein, M., Sultan, F., & Voogd, J. (2009). Functional localization in the cerebellum. Cortex [Epub ahead of print].Google ScholarPubMed
Gosselin, N., Peretz, I., Noulhiane, M., Hasboun, D., Beckett, C., Baulac, M., et al. (2005). Impaired recognition of scary music following unilateral temporal lobe excision. Brain, 128, 628640.CrossRefGoogle ScholarPubMed
Gross, J.J., Richards, J.M., & John, O.P. (2006). Emotion regulation in couples and families: Pathways to dysfunction and health. In Snyder, D.K., Simpson, J.A., & Hughes, J.N. (Eds.), Emotion regulation in everyday life. Washington DC: American Psychological Association.CrossRefGoogle Scholar
Habas, C., Kamdar, N., Nguyen, D., Prater, K., Beckmann, C.F., Menon, V., et al. (2009). Distinct cerebellar contributions to intrinsic connectivity networks. The Journal of Neuroscience, 29, 85868594.CrossRefGoogle ScholarPubMed
Heideman, R.L., Packer, R.J., Albright, L.A., Freeman, C.R., & Rorke, L.B. (1993). Tumors of the central nervous system. In Pizzo, P.A., & Poplack, D.G. (Eds), Principles and practice of pediatric oncology (2nd ed.). Philadelphia: JB Lippincott Company.Google Scholar
Hetherington, R., Dennis, M., & Spiegler, B. (2000). Perception and estimation of time in long-term survivors of childhood posterior fossa tumors. Journal of the International Neuropsychological Society, 6, 682692.CrossRefGoogle ScholarPubMed
Hevner, K. (1935). The affective character of the major and minor modes in music. American Journal of Psychology, 47, 103118.CrossRefGoogle Scholar
Hodgkins, P.R., Harris, C.M., Shawkat, F.S., Thompson, D.A., Chong, K., Timms, C., et al. (2004). Joubert syndrome: Long-term follow-up. Developmental Medicine and Child Neurology, 46, 694699.CrossRefGoogle ScholarPubMed
Hopyan, T., Schellenberg, E.G., & Dennis, M. (2009). Perception of strong-meter and weak-meter rhythms in children with spina bifida meningomyelocele. Journal of the International Neuropsychological Society, 15, 521528.CrossRefGoogle ScholarPubMed
Juslin, P. (1997). Emotional communication in music performance: A functionalist perspective and some data. Music Perception, 14, 383418.CrossRefGoogle Scholar
Koelsch, S., Fritz, T., v. Cramon, D.Y., Muller, K., & Friederici, A.D. (2006). Investigating emotion with music: An fMRI study. Human Brain Mapping, 27, 239250.CrossRefGoogle ScholarPubMed
Konczak, J., Schoch, B., Dimitrova, A., Gizewki, E., & Timmann, D. (2005). Functional recovery of children and adolescents after cerebellar tumour resection. Brain, 128, 14281441.CrossRefGoogle ScholarPubMed
Krumhansl, C.L. (1997). An exploratory study of musical emotions and psychophysiology. Canadian Journal of Experimental Psychology, 51, 336352.CrossRefGoogle ScholarPubMed
Levisohn, L., Cronin-Golomb, A., & Schmahmann, D. (2000). Neuropsychological consequences of cerebellar tumour resection in children: Cerebellar cognitive affective syndrome in a paediatric population. Brain, 123, 10411050.CrossRefGoogle Scholar
Maria, B.L., Hoang, K.B., Tusa, R.J., Mancuso, A.A., Hamed, L.M., Quisling, R.G., et al. (1997). “Joubert syndrome” revisited: Key ocular motor signs with magnetic resonance imaging correlation. Journal of Child Neurology, 12, 423430.CrossRefGoogle ScholarPubMed
Morris, W.N., & Reilly, N.P. (1987). Toward the self-regulation of mood: Theory and research. Motivation and Emotion, 11, 215249.CrossRefGoogle Scholar
Mostofsky, S.H., Kunze, J.C., Cutting, L.E., Lederman, H.M., & Denckla, M.B. (2000). Judgment of duration in individuals with ataxia-telangiectasia. Developmental Neuropsychology, 17, 6374.CrossRefGoogle ScholarPubMed
Mulhern, R.K., Kepner, J.L., Thomas, P.R., Armstrong, F.D., Friedman, H.S., & Kun, L.E. (1998). Neuropsychological functioning of survivors of childhood medulloblastoma randomized to receive conventional or reduced-dose craniospinal irradiation: A pediatric oncology group study. Journal of Clinical Oncology, 16, 17231728.CrossRefGoogle ScholarPubMed
Ochsner, K.N., Bunge, S.A., Gross, J.J., & Gabrieli, J.D. (2002). Rethinking feelings: An fMRI study of the cognitive regulation of emotion. Journal of Cognitive Neuroscience, 14, 12151229.CrossRefGoogle ScholarPubMed
Ochsner, K.N., Ray, R.D., Cooper, J.C., Robertson, E.R., Chopra, S., Gabrieli, J.D.E., et al. (2004). For better or for worse: Neural systems supporting the cognitive down- and up-regulation of negative emotion. Neuroimage, 23, 483499.CrossRefGoogle ScholarPubMed
Peretz, I., Gagnon, L., & Bouchard, B. (1998). Music and emotion: Perceptual determinants, immediacy, and isolation after brain damage. Cognition, 68, 111141.CrossRefGoogle ScholarPubMed
Pierson, R., Westmoreland Corson, P., Sears, L.L., Alicata, D., Magnotta, V., O’Leary, D., et al. (2002). Manual and semiautomated measurement of cerebellar subregions on MR images. Neuroimage, 17, 6176.CrossRefGoogle ScholarPubMed
Richter, S., Schoch, B., Kaiser, O., Groetschel, H., Dimitrova, A., Hein-Kropp, C., et al. (2005). Behavioral and affective changes in children and adolescents with chronic cerebellar lesions. Neuroscience Letters, 381, 102107.CrossRefGoogle ScholarPubMed
Rigg, M.G. (1937). An experiment to determine how accurately college students can interpret the intended meaning of musical compositions. Journal of Experimental Psychology, 21, 223229.CrossRefGoogle Scholar
Rigg, M.G. (1940). Speed as a determiner of musical mood. Journal of Experimental Psychology, 27, 566571.CrossRefGoogle Scholar
Riva, D., & Giorgi, C. (2000). The cerebellum contributes to higher functions during development: Evidence from a series of children surgically treated for posterior fossa tumours. Brain, 123, 10511061.CrossRefGoogle ScholarPubMed
Roncadin, C., Dennis, M., Greenberg, M., & Spiegler, B.J. (2008). Adverse medical events associated with childhood posterior fossa tumors: Natural history and relation to very long-term neurobehavioral outcome. Child’s Nervous System, 24, 9951002.CrossRefGoogle ScholarPubMed
Rønning, C., Sundet, K., Due-Tonnessen, B., Lundar, T., & Helseth, E. (2005). Persistent cognitive dysfunction secondary to cerebellar injury in patients treated for posterior fossa tumors in childhood. Pediatric Neurosurgery, 41, 1521.CrossRefGoogle ScholarPubMed
Schmahmann, J.D. (2001). The cerebellar cognitive affective syndrome: Clinical correlations of the dysmetria of thought hypothesis. International Review of Psychiatry, 13, 313322.CrossRefGoogle Scholar
Schmahmann, J.D. (2004). Disorders of the cerebellum: Ataxia, dysmetria of thoughts, and the cerebellar cognitive affective syndrome. Journal of Neuropsychiatry and Clinical Neuroscience, 16, 367378.CrossRefGoogle ScholarPubMed
Schmahmann, J.D., & Sherman, J.C. (1998). The cerebellar cognitive affective syndrome. Brain, 121, 561579.CrossRefGoogle ScholarPubMed
Schmahmann, J.D., Weilburg, J.B., & Sherman, J.C. (2007). The neuropsychiatry of the cerebellum: Insight from the clinic. The Cerebellum, 6, 254267.CrossRefGoogle ScholarPubMed
Schoch, B., Dimitrova, A., Gizewski, E.R., & Timmann, D. (2006). Functional localization in the human cerebellum based on voxelwise statistical analysis: A study of 90 patients. NeuroImage, 30, 3651.CrossRefGoogle Scholar
Steinlin, M., Imfeld, S., Zulauf, P., Boltshauser, E., Lovblad, K.O., Luthy, A.R., et al. (2003). Neuropsychological long-term sequelae after posterior fossa tumour resection during childhood. Brain, 126, 19982008.CrossRefGoogle ScholarPubMed
Stoodley, C.J., & Schmahmann, J.D. (2009). Functional topography in the human cerebellum: A meta-analysis of neuroimaging studies. Neuroimage, 44, 489501.CrossRefGoogle ScholarPubMed
Stoodley, C.J., & Schmahmann, J.D. (2010). Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex, 46, 831844.CrossRefGoogle ScholarPubMed
Strother, D.R., Pollack, I.F., Fisher, P.G., Hunter, J.V., Woo, S.Y., Pomeroy, S.L., et al. (2002). Principles and practice of pediatric oncology (4th ed.). In Pizzo, P.A., & Poplack, D.G. (Eds.), Tumors of the central nervous system (pp. 751824). Philadelphia: Lippincott Williams & Wilkins.Google Scholar
Tavano, A., & Borgatti, R. (2010). Evidence for a link among cognition, language and emotion in cerebellar malformations. Cortex, 46, 907918.CrossRefGoogle ScholarPubMed
Tavano, A., Fabbor, F., & Borgatti, R. (2007). Language and social cognition in children with cerebellar dysgenesis. Folia Phoniatrica et Logopedica, 59, 201209.CrossRefGoogle Scholar
Tavano, A., Grasso, R., Gagliardi, C., Triulzi, F., Bresolin, N., Fabbro, F., et al. (2007). Disorders of cognitive and affective development in cerebellar malformations. Brain, 130, 26462660.CrossRefGoogle ScholarPubMed
Valenta, E.M., Brancati, F., & Dallapiccola, B. (2008). Genotypes and phenotypes of joubert syndrome and related disorders. European Journal of Medical Genetics, 51, 123.CrossRefGoogle Scholar
Vaquero, E., Gómez, C.M., Quintero, E.A., González-Rosa, J.J., & Márquez, J. (2008). Differential prefrontal-like deficit in children after cerebellar astrocytoma and medulloblastoma tumor. Behavioral Brain Function, 4, 18.CrossRefGoogle ScholarPubMed
Walter, A.W., Mulhern, R.K., Gajjar, A., Heideman, R.L., Reardon, D., Sanford, R.A., et al. (1999). Survival and neurodevelopmental outcome of young children with medulloblastoma at St. Jude Children’s Research Hospital. Journal of Clinical Oncology, 17, 37203728.CrossRefGoogle ScholarPubMed
Wechsler, D. (1999). Wechsler abbreviated scale of intelligence (WASI). San Antonio: Psychological Corporation.Google Scholar