BACKGROUND: Damage to the cerebellum may lead to motor dysfunctions, but also to the neuropsychological deficits that comprise the Cerebellar Cognitive Affective Syndrome (CCAS). It can affect executive functions, attention, memory, visuospatial functions, language, and emotions. Our goal was to determine which neuropsychological tests could be effectively used to identify this syndrome during a short examination. METHODS: Twenty-five patients with an isolated cerebellar lesion and 25 matched healthy controls were examined using an extensive neuropsychological battery. RESULTS: Logistic regression models and sub-models were computed for individual tests, as well as for the full battery. The best results were produced by a model combining patient education level, the number of errors on the California Verbal Learning Test, and time on Prague Stroop Test (Dots). CONCLUSIONS: Based on the results, we suggest that a condensed battery of neuropsychological tests can be used to detect CCAS. The tests are easy to administer and could be helpful in both research and clinical settings.

Department of Neurology and Centre of Clinical Neuroscience 1st Faculty of Medicine Charles University and General University Hospital Prague Prague Czech Republic

Department of Neurology Hospital České Budějovice a s České Budějovice Czech Republic

Department of Neurology Thomayer Hospital Prague Czech Republic

Department of Neurosurgery and Neurooncology 1st Faculty of Medicine Charles University and Military University Hospital Prague Czech Republic

Department of Psychology Faculty of Arts Charles University Prague Czech Republic

Faculty of Nuclear Sciences and Physical Engineering Czech Technical University Prague Czech Republic

See more in PubMed

Leiner HC, Leiner AL, Dow RS. Does the cerebellum contribute to mental skills? Behav Neurosci. 1986;100:443–454. doi: 10.1037/0735-7044.100.4.443. PubMed DOI

Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain. 1998;121:561–579. doi: 10.1093/brain/121.4.561. PubMed DOI

Manto M, Mariën P. Schmahmann’s syndrome-identification of the third cornerstone of clinical ataxiology. Cerebellum Ataxias. 2015;2:2. doi: 10.1186/s40673-015-0023-1. PubMed DOI PMC

O’Halloran CJ, Kinsella GJ, Storey E. The cerebellum and neuropsychological functioning: a critical review. J Clin Exp Neuropsychol. 2012;34:35–56. doi: 10.1080/13803395.2011.614599. PubMed DOI

Bellebaum C, Daum I. Cerebellar involvement in executive control. Cerebellum. 2007;6:184–192. doi: 10.1080/14734220601169707. PubMed DOI

Gottwald B, Wilde B, Mihajlovic Z, Mehdorn HM. Evidence for distinct cognitive deficits after focal cerebellar lesions. J Neurol Neurosurg Psychiatry. 2004;75:1524–1531. doi: 10.1136/jnnp.2003.018093. PubMed DOI PMC

De Smet HJ, Paquier P, Verhoeven J, Mariën P. The cerebellum: its role in language and related cognitive and affective functions. Brain Lang. 2013;127:334-42. PubMed

Molinari M, Leggio MG. Cerebellar information processing and visuospatial functions. Cerebellum. 2007;6:214–220. doi: 10.1080/14734220701230870. PubMed DOI

Schutter DJLG, Van Honk J. The cerebellum on the rise in human emotion. Cerebellum. 2005;4:290–294. doi: 10.1080/14734220500348584. PubMed DOI

Mills NP, DelBello MP, Adler CM, Strakowski SM. MRI analysis of cerebellar vermal abnormalities in bipolar disorder. Am J Psychiat. 2005;162:1530–1533. doi: 10.1176/appi.ajp.162.8.1530. PubMed DOI

Tedesco AM, Chiricozzi FR, Clausi S, Lupo M, Molinari M, Leggio MG. The cerebellar cognitive profile. Brain. 2011;134:3669–3683. doi: 10.1093/brain/awr266. PubMed DOI

Komaba Y, Osono E, Kitamura S, Katayama Y. Crossed cerebellocerebral diaschisis in patients with cerebellar stroke. Acta Neurol Scand. 2000;101:8–12. doi: 10.1034/j.1600-0404.2000.00002.x. PubMed DOI

Manes F, Villamil AR, Ameriso S, Roca M, Torralva T. “real life” executive deficits in patients with focal vascular lesions affecting the cerebellum. J Neurol Sci. 2009;283:95–98. doi: 10.1016/j.jns.2009.02.316. PubMed DOI

Reitan RM. Trail making test: manual for administration and scoring. South Tucson, AZ: Reitan Neuropsychology Laboratory; 1992.

Libon DJ, Mattson RE, Blosser G, Kaplan E, Malamut BL, Sands LP, Swenson R, Cloud BS. A nine-word dementia version of the California verbal learning test. Clin Neuropsychol. 1996;10:237–44.

Osterrieth PA. Le test de copie d’une figure complexe; contribution à l’étude de la perception et de la mémoire. Arch Psychol (Geneve). 1944;30:206–356.

Tombaugh TN, Kozak J, Rees L. Normative data stratified by age and education for two measures of verbal fluency: FAS and animal naming. Arch Clin Neuropsychol. 1999;14:167–177. PubMed

Preiss M, Bartoš A, Cermáková R, Nondek M, Benešová M, Rodriguez M, Nikolai T. Neuropsychologická baterie Psychiatrického centra Praha. Klinické vyšetrení základních kognitivních funkcí. 3. Prague: PCP; 2012.

Dubois B, Slachevsky A, Litvan I, Pillon B. The FAB: a frontal assessment battery at bedside. Neurol. 2000;55:1621–1626. doi: 10.1212/WNL.55.11.1621. PubMed DOI

Regard M, Strauss E, Knapp P. Childrens’ production on verbal and non-verbal fluency tasks. Percept Mot Skills. 1982;55(3):839–844. doi: 10.2466/pms.1982.55.3.839. PubMed DOI

Bezdíček O, Lukavský J, Štepánková H, Nikolai T, Axelrod BN, Michalec J, Kopeček M. The Prague Stroop test: normative standards in older Czech adults and discriminative validity for mild cognitive impairment in Parkinson’s disease. J Clin Exp Neuropsyc. 2015;37:794–807. PubMed

Terry PC, Lane AM. User guide for the Brunel mood scale (BRUMS). Australia: University of Southern Queensland; 2003.

Trouillas P, Takayanagi T, Hallett M, Currier RD, Subramony SH, Wessel K, Coutinho P. International cooperative ataxia rating scale for pharmacological assessment of the cerebellar syndrome. J Neurol Sci. 1997;145:205–211. doi: 10.1016/S0022-510X(96)00231-6. PubMed DOI

Bolceková E, Fiala J, Rusina R, Kukal J, Buncová M, Ostrý S, et al. Zhoršení kognitivních funkcí a snížení perfuze v kontralaterálním frontálním laloku u pacientů s lézí mozečku [Cognitive Deficit And Contralateral Frontal Hypoperfusion In Patients With Cerebellar Lesions] Cesk Slov Neurol N. 2012;75:595–601.

Vahdani B, Razavi F, Mousavi SM. A high performing meta-heuristic for training of support vector regression in performance forecasting of supply chain. Neural Comp Appli. 2016;27:2441–2451. doi: 10.1007/s00521-015-2015-8. DOI

Zheng T, Xie W, Xu LL, He XY, Zhang Y, You MR, Yang G, Chan Y. A machine learning-based framework to identify type 2 diabetes thorough electronic health records. Int J Med Info. 2017;97:120–127. doi: 10.1016/j.ijmedinf.2016.09.014. PubMed DOI PMC

Martinez AM, Webb GI, Chen SL, Zaidi NA. Scalable learning of Bayesian network classifiers. J Mac Lear Res. 2016;17:44.

Mojzes M, Klimt M, Kukal J, Bukovsky I, Vrba J, Pitel J. Feature selection via competitive levy flights, in: proc. Int Joint Conf Neural Net (IJCNN). 2016:3731–6.

Mehrabian A, Epstein N. A measure of emotional empathy. J Pers. 1972;40:525–43. PubMed

Stančák A. Skrátená verzia MMPI/100. Bratislava: Psychodiagnostické a didaktické testy; 1989.

Desmond JE, Fiez JA. Neuroimaging studies of the cerebellum: language, learning and memory. Trends Cognit Sci. 1998;2:355–62. PubMed

Andreasen NC, O'Leary DS, Paradiso S, Cizadlo T, Arndt S, Watkins GL, et al. The cerebellum plays a role in conscious episodic memory retrieval. Hum Brain Mapp. 1999;8:226–34. PubMed PMC

Cabeza R, St Jacques P. Functional neuroimaging of autobiographical memory. Trends Cognit Sci. 2007;11:219–27. PubMed

Desmond JE, Gabrieli JD, Glover GH. Dissociation of frontal and cerebellar activity in a cognitive task: evidence for a distinction between selection and search. NeuroImage. 1998;7:368–76. PubMed

Karatekin C, Lazareff JA, Asarnow RF. Relevance of the cerebellar hemispheres for executive functions. Pediatr Neurol. 2000;22:106–12. PubMed

Molinari M, Petrosini L, Misciagna S, Leggio MG. Visuospatial abilities in cerebellar disorders. J Neurol Neurosurg Psychiatry. 2004;75:235–40. PubMed PMC

Leiner HC, Leiner AL, Dow RS. Reappraising the cerebellum: what does the hindbrain contribute to the forebrain? Behav Neurosci. 1989;103:998–1008. PubMed

Botez MI, Botez T, Elie R, Attig E. Role of the cerebellum in complex human behavior. The Italian J Neurol Sci. 1989;10:291–300. PubMed

Daum I, Ackermann H, Schugens MM, Reimold C, Dichgans J, Birbaumer N. The cerebellum and cognitive functions in humans. Behav Neurosci. 1993;107:411–9. PubMed

Appollonio IM, Grafman J, Schwartz V, Massaquoi S, Hallett M. Memory in patients with cerebellar degeneration. Neurol. 1993;43:1536. PubMed

Bracke-Tolkmitt R, Linden A, Canavan AGM, Rockstroh B, Scholz E, Wessel KDHC, Diener HC. The cerebellum contributes to mental skills. Behav Neurosci. 1989;103:442–6.

Fiez JA, Petersen SE, Cheney MK, Raichle ME. Impaired non-motor learning and error detection associated with cerebellar damage. Brain. 1992;115:155–78. PubMed

Daum I, Ackermann H. Neuropsychological abnormalities in cerebellar syndromes-fact or fiction? Inter Rev Neurobiol. 1997;41:455–471. doi: 10.1016/S0074-7742(08)60365-7. PubMed DOI

Schmahmann JD. Dysmetria of thought: clinical consequences of cerebellar dysfunction on cognition and affect. Trends Cogn Sci. 1998;2:362–71. PubMed

Stoodley CJ, Schmahmann JD. The cerebellum and language: evidence from patients with cerebellar degeneration. Brain Lang. 2009;110:149–53. PubMed

Schmahmann JD. An emerging concept: the cerebellar contribution to higher function. Arch Neurol. 1991;48:1178–1187. doi: 10.1001/archneur.1991.00530230086029. PubMed DOI

Zakzanis KK, Mraz R, Graham SJ. An fMRI study of the Trail Making Test. Neuropsychologia. 2005;43:1878–86. PubMed