Visuospatial Organization and Recall in Cerebellar Ataxia


Poor visuospatial skills can disrupt activities of daily living. The cerebellum has been implicated in visuospatial processing, and patients with cerebellar injury often exhibit poor visuospatial skills, as measured by impaired memory for the figure within the Rey-Osterrieth complex figure task (ROCF). Visuospatial skills are an inherent aspect of the ROCF; however, figure organization (i.e., the order in which the figure is reconstructed by the participant) can influence recall ability. The objective of this study was to examine and compare visuospatial and organization skills in people with cerebellar ataxia. We administered the ROCF to patients diagnosed with cerebellar ataxia and healthy controls. The cerebellar ataxia group included patients that carried a diagnosis of spinocerebellar ataxia (any subtype), autosomal dominant cerebellar ataxia, or cerebellar ataxia with unknown etiology. Primary outcome measures were organization and recall performance on the ROCF, with supplemental information derived from cognitive tests of visuospatial perception, working memory, processing speed, and motor function. Cerebellar ataxia patients revealed impaired figure organization relative to that of controls. Figure copy was impaired in the patients, but their subsequent recall performance was normal, suggesting compensation from initial organization and copying strategies. In controls, figure organization predicted recall performance, but this relationship was not observed in the patients. Instead, processing speed predicted patients’ recall accuracy. Supplemental tasks indicated that visual perception was intact in the cerebellar ataxia group and that performance deficits were more closely tied to organization strategies than with visuospatial skills.

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  1. 1.

    Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain. 1998;121(Pt 4):561–79.

    PubMed  Article  Google Scholar 

  2. 2.

    Molinari M, Leggio MG. Cerebellar information processing and visuospatial functions. Cerebellum. 2007;6(3):214–20.

    PubMed  Article  Google Scholar 

  3. 3.

    O’Halloran CJ, Kinsella GJ, Storey E. The cerebellum and neuropsychological functioning: a critical review. J Clin Exp Neuropsychol. 2012;34(1):35–56.

    PubMed  Article  Google Scholar 

  4. 4.

    Fancellu R, Paridi D, Tomasello C, Panzeri M, Castaldo A, Genitrini S, et al. Longitudinal study of cognitive and psychiatric functions in spinocerebellar ataxia types 1 and 2. J Neurol. 2013;260(12):3134–43.

    PubMed  Article  Google Scholar 

  5. 5.

    Molinari M, Petrosini L, Misciagna S, Leggio MG. Visuospatial abilities in cerebellar disorders. J Neurol Neurosurg Psychiatry. 2004;75(2):235–40.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. 6.

    Tedesco AM, Chiricozzi FR, Clausi S, Lupo M, Molinari M, Leggio MG. The cerebellar cognitive profile. Brain. 2011;134(Pt 12):3672–86.

    PubMed  Article  Google Scholar 

  7. 7.

    Fink GR, Marshall JC, Shah NJ, Weiss PH, Halligan PW, Grosse-Ruyken M, et al. Line bisection judgments implicate right parietal cortex and cerebellum as assessed by fMRI. Neurology. 2000;54(6):1324–31.

    CAS  PubMed  Article  Google Scholar 

  8. 8.

    Lee TM, Liu HL, Hung KN, Pu J, Ng YB, Mak AK, et al. The cerebellum’s involvement in the judgment of spatial orientation: a functional magnetic resonance imaging study. Neuropsychologia. 2005;43(13):1870–7.

    PubMed  Article  Google Scholar 

  9. 9.

    Baier B, Muller NG, Dieterich M. What part of the cerebellum contributes to a visuospatial working memory task? Ann Neurol. 2014;76(5):754–7.

    PubMed  Article  Google Scholar 

  10. 10.

    Miall RC, Christensen LOD, Cain O, Stanley J. Disruption of state estimation in the human lateral cerebellum. PLoS Biol. 2007;5(11):2733–44.

    CAS  Article  Google Scholar 

  11. 11.

    Shadmehr R, Smith MA, Krakauer JW. Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci. 2010;33:89–108.

    CAS  PubMed  Article  Google Scholar 

  12. 12.

    Ito M. Cerebellar microcomplexes. Int Rev Neurobiol. 1997;41:475–87.

    CAS  PubMed  Article  Google Scholar 

  13. 13.

    Schwartz E. National Ataxia Foundation [Available from:].

  14. 14.

    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(1–2):95–8.

    PubMed  Article  Google Scholar 

  15. 15.

    Gleason CE, Gangnon RE, Fischer BL, Mahoney JE. Increased risk for falling associated with subtle cognitive impairment: secondary analysis of a randomized clinical trial. Dement Geriatr Cogn Disord. 2009;27(6):557–63.

    PubMed  PubMed Central  Article  Google Scholar 

  16. 16.

    Paradise M, McCade D, Hickie IB, Diamond K, Lewis SJ, Naismith SL. Caregiver burden in mild cognitive impairment. Aging Ment Health. 2015;19(1):72–8.

    PubMed  Article  Google Scholar 

  17. 17.

    Schmahmann JD. Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J Neuropsychiatr Clin Neurosci. 2004;16(3):367–78.

    Article  Google Scholar 

  18. 18.

    Rey A. Psychological examination in cases of traumatic encephalopathy. Arch Psychol. 1941;28(112):286–340.

    Google Scholar 

  19. 19.

    Burk K, Globas C, Bosch S, Graber S, Abele M, Brice A, et al. Cognitive deficits in spinocerebellar ataxia 2. Brain. 1999;122(Pt 4):769–77.

    PubMed  Article  Google Scholar 

  20. 20.

    Globas C, Bosch S, Zuhlke C, Daum I, Dichgans J, Burk K. The cerebellum and cognition. Intellectual function in spinocerebellar ataxia type 6 (SCA6). J Neurol. 2003;250(12):1482–7.

    CAS  PubMed  Article  Google Scholar 

  21. 21.

    Braga-Neto P, Pedroso JL, Alessi H, Dutra LA, Felicio AC, Minett T, et al. Cerebellar cognitive affective syndrome in Machado Joseph disease: core clinical features. Cerebellum. 2012;11(2):549–56.

    PubMed  Article  Google Scholar 

  22. 22.

    Burk K, Globas C, Bosch S, Klockgether T, Zuhlke C, Daum I, et al. Cognitive deficits in spinocerebellar ataxia type 1, 2, and 3. J Neurol. 2003;250(2):207–11.

    CAS  PubMed  Article  Google Scholar 

  23. 23.

    Orsi L, D’Agata F, Caroppo P, Franco A, Caglio MM, Avidano F, et al. Neuropsychological picture of 33 spinocerebellar ataxia cases. J Clin Exp Neuropsychol. 2011;33(3):315–25.

    PubMed  Article  Google Scholar 

  24. 24.

    Le Pira F, Giuffrida S, Maci T, Marturano L, Tarantello R, Zappala G, et al. Dissociation between motor and cognitive impairments in SCA2: evidence from a follow-up study. J Neurol. 2007;254(10):1455–6.

    PubMed  Article  Google Scholar 

  25. 25.

    Osterrieth PA. The challenge of copying a complex figure. Arch Psychol. 1944;30(117–20):205–353.

    Google Scholar 

  26. 26.

    Shin MS, Park SY, Park SR, Seol SH, Kwon JS. Clinical and empirical applications of the Rey-Osterrieth Complex Figure Test. Nat Protoc. 2006;1(2):892–9.

    PubMed  Article  Google Scholar 

  27. 27.

    Savage CR, Baer L, Keuthen NJ, Brown HD, Rauch SL, Jenike MA. Organizational strategies mediate nonverbal memory impairment in obsessive-compulsive disorder. Biol Psychiatry. 1999;45(7):905–16.

    CAS  PubMed  Article  Google Scholar 

  28. 28.

    Savage CR, Deckersbach T, Wilhelm S, Rauch SL, Baer L, Reid T, et al. Strategic processing and episodic memory impairment in obsessive compulsive disorder. Neuropsychology. 2000;14(1):141–51.

    CAS  PubMed  Article  Google Scholar 

  29. 29.

    Stoodley CJ, MacMore JP, Makris N, Sherman JC, Schmahmann JD. Location of lesion determines motor vs. cognitive consequences in patients with cerebellar stroke. Neuroimage Clin. 2016;12:765–75.

    PubMed  PubMed Central  Article  Google Scholar 

  30. 30.

    Starowicz-Filip A, Chrobak AA, Milczarek O, Kwiatkowski S. The visuospatial functions in children after cerebellar low-grade astrocytoma surgery: a contribution to the pediatric neuropsychology of the cerebellum. J Neuropsychol. 2015;11:201-221.

  31. 31.

    Jolliffe T, BaronCohen S. Are people with autism and Asperger syndrome faster than normal on the embedded figures test? J Child Psychol Psychiatry. 1997;38(5):527–34.

    CAS  PubMed  Article  Google Scholar 

  32. 32.

    Seidman LJ, Lanca M, Kremen WS, Faraone SV, Tsuang MT. Organizational and visual memory deficits in schizophrenia and bipolar psychoses using the Rey-Osterrieth complex figure: effects of duration of illness. J Clin Exp Neuropsychol. 2003;25(7):949–64.

    PubMed  Article  Google Scholar 

  33. 33.

    Silverstein SM, Osborn LM, Palumbo DR. Rey-Osterrieth Complex Figure Test performance in acute, chronic, and remitted schizophrenia patients. J Clin Psychol. 1998;54(7):985–94.

    CAS  PubMed  Article  Google Scholar 

  34. 34.

    John CH, Hemsley DR. Gestalt perception in schizophrenia. Eur Arch Psychiatry Clin Neurosci. 1992;241(4):215–21.

    CAS  PubMed  Article  Google Scholar 

  35. 35.

    Becker EB, Stoodley CJ. Autism spectrum disorder and the cerebellum. Int Rev Neurobiol. 2013;113:1–34.

    CAS  PubMed  Article  Google Scholar 

  36. 36.

    Andreasen NC, Pierson R. The role of the cerebellum in schizophrenia. Biol Psychiatry. 2008;64(2):81–8.

    PubMed  PubMed Central  Article  Google Scholar 

  37. 37.

    Bennettlevy J. Determinants of performance on the Rey-Osterrieth Complex Figure Test—an analysis, and a new technique for single-case assessment. Br J Clin Psychol. 1984;23(May):109–19.

    Article  Google Scholar 

  38. 38.

    Martens R, Hurks PPM, Jolles J. Organizational strategy use in children aged 5–7: standardization and validity of the Rey Complex Figure Organizational Strategy Score (RCF-OSS). Clin Neuropsychol. 2014;28(6):954–73.

    CAS  PubMed  Article  Google Scholar 

  39. 39.

    Happe F, Frith U. The weak coherence account: detail-focused cognitive style in autism spectrum disorders. J Autism Dev Disord. 2006;36(1):5–25.

    PubMed  Article  Google Scholar 

  40. 40.

    Schmahmann JD, Pandya DN. Anatomical investigation of projections to the basis pontis from posterior parietal association cortices in rhesus monkey. J Comp Neurol. 1989;289(1):53–73.

    CAS  PubMed  Article  Google Scholar 

  41. 41.

    Clower DM, West RA, Lynch JC, Strick PL. The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. J Neurosci. 2001;21(16):6283–91.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  42. 42.

    Dum RP, Strick PL. An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. J Neurophysiol. 2003;89(1):634–9.

    PubMed  Article  Google Scholar 

  43. 43.

    Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106(5):2322–45.

    PubMed  PubMed Central  Article  Google Scholar 

  44. 44.

    O’Reilly JX, Beckmann CF, Tomassini V, Ramnani N, Johansen-Berg H. Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. Cereb Cortex. 2010;20(4):953–65.

    PubMed  Article  Google Scholar 

  45. 45.

    Caron MJ, Mottron L, Berthiaume C, Dawson M. Cognitive mechanisms, specificity and neural underpinnings of visuospatial peaks in autism. Brain. 2006;129(Pt 7):1789–802.

    PubMed  Article  Google Scholar 

  46. 46.

    Shah A, Frith U. Why do autistic individuals show superior performance on the block design task. J Child Psychol Psychiatry. 1993;34(8):1351–64.

    CAS  PubMed  Article  Google Scholar 

  47. 47.

    Caffarra P, Vezzadini G, Dieci F, Zonato F, Venneri A. Rey-Osterrieth complex figure: normative values in an Italian population sample. Neurol Sci. 2002;22(6):443–7.

    CAS  PubMed  Article  Google Scholar 

  48. 48.

    Meyers JE, Meyers KR. Rey complex figure test and recognition trial professional manual: psychological assessment. Odessa: Psychological Assessment Resources: 1995.

  49. 49.

    Lezak MD. The complex figure test (CFT): copy administration. In: Neuropsychological assessment. 2nd ed. New York: Oxford University Press; 1983. p. 395–402.

  50. 50.

    Wechsler Adult Intelligence Scale (WAIS). J Consult Psychol. 1955;19(4):319–20.

    Google Scholar 

  51. 51.

    Forn C, Ripolles P, Cruz-Gomez AJ, Belenguer A, Gonzalez-Torre JA, Avila C. Task-load manipulation in the symbol digit modalities test: an alternative measure of information processing speed. Brain Cogn. 2013;82(2):152–60.

    CAS  PubMed  Article  Google Scholar 

  52. 52.

    Smith A. Symbol digit modalities test. Los Angeles: Western Psychological Services; 1982.

    Google Scholar 

  53. 53.

    Arango-Lasprilla JC, Rivera D, Rodriguez G, Garza MT, Galarza-Del-Angel J, Rodriguez W, et al. Symbol digit modalities test: normative data for the Latin American Spanish speaking adult population. NeuroRehabilitation. 2015;37(4):625–38.

    CAS  PubMed  Article  Google Scholar 

  54. 54.

    Wechsler D. Wechsler adult intelligence scale-third edition: administration and scoring manual. San Antonio: Psychological Corporation; 1997.

    Google Scholar 

  55. 55.

    Broshek DK, Barth JT, editors. The Halstead–Reitan neuropsychological test battery. New York: Wiley; 2000.

    Google Scholar 

  56. 56.

    Radloff LS. The CES-D scale: a self-report depression scale for research in the general population. Appl Psychol Meas. 1977;1:385–401.

    Article  Google Scholar 

  57. 57.

    Ashendorf L, Jefferson AL, Green RC, Stern RA. Test-retest stability on the WRAT-3 reading subtest in geriatric cognitive evaluations. J Clin Exp Neuropsychol. 2009;31(5):605–10.

    PubMed  Article  Google Scholar 

  58. 58.

    Wilkinson GS. WRAT-3: wide range achievement test administration manual. Wide Range, Incorporated; 1993.

  59. 59.

    Trouillas P, Takayanagi T, Hallett M, Currier RD, Subramony SH, Wessel K, et al. International Cooperative Ataxia Rating Scale for pharmacological assessment of the cerebellar syndrome. J Neurol Sci. 1997;145(2):205–11.

    CAS  PubMed  Article  Google Scholar 

  60. 60.

    Salthouse TA. Aging and measures of processing speed. Biol Psychol. 2000;54(1–3):35–54.

    CAS  PubMed  Article  Google Scholar 

  61. 61.

    Nocentini U, Giordano A, Di Vincenzo S, Panella M, Pasqualetti P. The Symbol Digit Modalities Test—oral version: Italian normative data. Funct Neurol. 2006;21(2):93–6.

    PubMed  Google Scholar 

  62. 62.

    Joy S, Kaplan E, Fein D. Speed and memory in the eWAIS-III digit symbol—coding subtest across the adult lifespan. Arch Clin Neuropsychol. 2004;19(6):759–67.

    PubMed  Article  Google Scholar 

  63. 63.

    Cepeda NJ, Blackwell KA, Munakata Y. Speed isn’t everything: complex processing speed measures mask individual differences and developmental changes in executive control. Dev Sci. 2013;16(2):269–86.

    PubMed  PubMed Central  Article  Google Scholar 

  64. 64.

    Bellebaum C, Daum I. Cerebellar involvement in executive control. Cerebellum. 2007;6(3):184–92.

    PubMed  Article  Google Scholar 

  65. 65.

    Schmahmann JD, Weilburg JB, Sherman JC. The neuropsychiatry of the cerebellum—insights from the clinic. Cerebellum. 2007;6(3):254–67.

    PubMed  Article  Google Scholar 

  66. 66.

    D’Agata F, Caroppo P, Boghi A, Coriasco M, Caglio M, Baudino B, et al. Linking coordinative and executive dysfunctions to atrophy in spinocerebellar ataxia 2 patients. Brain Struct Funct. 2011;216(3):275–88.

    PubMed  Article  CAS  Google Scholar 

  67. 67.

    Leggio MG, Tedesco AM, Chiricozzi FR, Clausi S, Orsini A, Molinari M. Cognitive sequencing impairment in patients with focal or atrophic cerebellar damage. Brain. 2008;131(Pt 5):1332–43.

    CAS  PubMed  Article  Google Scholar 

  68. 68.

    Ito M. Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci. 2008;9(4):304–13.

    CAS  PubMed  Article  Google Scholar 

  69. 69.

    Nixon PD, Passingham RE. The cerebellum and cognition: cerebellar lesions impair sequence learning but not conditional visuomotor learning in monkeys. Neuropsychologia. 2000;38(7):1054–72.

    CAS  PubMed  Article  Google Scholar 

  70. 70.

    Gomez-Beldarrain M, Garcia-Monco JC, Rubio B, Pascual-Leone A. Effect of focal cerebellar lesions on procedural learning in the serial reaction time task. Exp Brain Res. 1998;120(1):25–30.

    CAS  PubMed  Article  Google Scholar 

  71. 71.

    Toni I, Krams M, Turner R, Passingham RE. The time course of changes during motor sequence learning: a whole-brain fMRI study. NeuroImage. 1998;8(1):50–61.

    CAS  PubMed  Article  Google Scholar 

  72. 72.

    Molinari M, Grammaldo LG, Petrosini L. Cerebellar contribution to spatial event processing: right/left discrimination abilities in rats. Eur J Neurosci. 1997;9(9):1986–92.

    CAS  PubMed  Article  Google Scholar 

  73. 73.

    Leggio MG, Neri P, Graziano A, Mandolesi L, Molinari M, Petrosini L. Cerebellar contribution to spatial event processing: characterization of procedural learning. Exp Brain Res. 1999;127(1):1–11.

    CAS  PubMed  Article  Google Scholar 

  74. 74.

    Petrosini L, Molinari M, DellAnna ME. Cerebellar contribution to spatial event processing: Morris water maze and T-maze. Eur J Neurosci. 1996;8(9):1882–96.

    CAS  PubMed  Article  Google Scholar 

  75. 75.

    De Lucia N, Trojano L, Senese VP, Conson M. Mental simulation of drawing actions enhances delayed recall of a complex figure. Exp Brain Res. 2016;234(10):2935–43.

    PubMed  Article  Google Scholar 

  76. 76.

    Imamizu H, Kawato M. Cerebellar internal models: implications for the dexterous use of tools. Cerebellum. 2012;11(2):325–35.

    CAS  PubMed  Article  Google Scholar 

  77. 77.

    Higuchi S, Imamizu H, Kawato M. Cerebellar activity evoked by common tool-use execution and imagery tasks: an fMRI study. Cortex. 2007;43(3):350–8.

    PubMed  Article  Google Scholar 

  78. 78.

    Manto MU. The wide spectrum of spinocerebellar ataxias (SCAs). Cerebellum. 2005;4(1):2–6.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  79. 79.

    Fastenau PS, Denburg NL, Hufford BJ. Adult norms for the Rey-Osterrieth complex figure test and for supplemental recognition and matching trials from the extended complex figure test. Clin Neuropsychol. 1999;13(1):30–47.

    CAS  PubMed  Article  Google Scholar 

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We would like to thank the faculty, staff, patients, and family members of the Johns Hopkins Ataxia Center.


Funding for this study was provided by the Gordon and Marilyn Macklin Foundation and the Margaret Q. Landenberger Research Foundation.

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Correspondence to Cherie Marvel.

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Electronic Supplementary Material

Supplement 1

Example of Level 5 Figure Organization. This video shows an ataxia patient’s actual process of drawing the ROCF during the copy condition, sped up 35 fold. This approach was assigned a level 5 figure organization, and exemplifies the overall less efficient figure organization employed by the ataxia group. (AVI 6869 kb)

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Slapik, M., Kronemer, S.I., Morgan, O. et al. Visuospatial Organization and Recall in Cerebellar Ataxia. Cerebellum 18, 33–46 (2019).

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  • Cerebellum
  • Ataxia
  • Visuospatial
  • Memory
  • Organization
  • Cognition