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Published in: The Cerebellum 1/2019

01-02-2019 | Original Paper

Visuospatial Organization and Recall in Cerebellar Ataxia

Authors: Mitchell Slapik, Sharif I. Kronemer, Owen Morgan, Ryan Bloes, Seth Lieberman, Jordan Mandel, Liana Rosenthal, Cherie Marvel

Published in: The Cerebellum | Issue 1/2019

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Abstract

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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Literature
1.
go back to reference Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain. 1998;121(Pt 4):561–79.PubMedCrossRef Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain. 1998;121(Pt 4):561–79.PubMedCrossRef
2.
go back to reference Molinari M, Leggio MG. Cerebellar information processing and visuospatial functions. Cerebellum. 2007;6(3):214–20.PubMedCrossRef Molinari M, Leggio MG. Cerebellar information processing and visuospatial functions. Cerebellum. 2007;6(3):214–20.PubMedCrossRef
3.
go back to reference O’Halloran CJ, Kinsella GJ, Storey E. The cerebellum and neuropsychological functioning: a critical review. J Clin Exp Neuropsychol. 2012;34(1):35–56.PubMedCrossRef O’Halloran CJ, Kinsella GJ, Storey E. The cerebellum and neuropsychological functioning: a critical review. J Clin Exp Neuropsychol. 2012;34(1):35–56.PubMedCrossRef
4.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
5.
go back to reference Molinari M, Petrosini L, Misciagna S, Leggio MG. Visuospatial abilities in cerebellar disorders. J Neurol Neurosurg Psychiatry. 2004;75(2):235–40.PubMedPubMedCentral Molinari M, Petrosini L, Misciagna S, Leggio MG. Visuospatial abilities in cerebellar disorders. J Neurol Neurosurg Psychiatry. 2004;75(2):235–40.PubMedPubMedCentral
6.
go back to reference Tedesco AM, Chiricozzi FR, Clausi S, Lupo M, Molinari M, Leggio MG. The cerebellar cognitive profile. Brain. 2011;134(Pt 12):3672–86.PubMedCrossRef Tedesco AM, Chiricozzi FR, Clausi S, Lupo M, Molinari M, Leggio MG. The cerebellar cognitive profile. Brain. 2011;134(Pt 12):3672–86.PubMedCrossRef
7.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
8.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
9.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
10.
go back to reference Miall RC, Christensen LOD, Cain O, Stanley J. Disruption of state estimation in the human lateral cerebellum. PLoS Biol. 2007;5(11):2733–44.CrossRef Miall RC, Christensen LOD, Cain O, Stanley J. Disruption of state estimation in the human lateral cerebellum. PLoS Biol. 2007;5(11):2733–44.CrossRef
11.
go back to reference Shadmehr R, Smith MA, Krakauer JW. Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci. 2010;33:89–108.PubMedCrossRef Shadmehr R, Smith MA, Krakauer JW. Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci. 2010;33:89–108.PubMedCrossRef
14.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
15.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
16.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
17.
go back to reference 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.CrossRef 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.CrossRef
18.
go back to reference Rey A. Psychological examination in cases of traumatic encephalopathy. Arch Psychol. 1941;28(112):286–340. Rey A. Psychological examination in cases of traumatic encephalopathy. Arch Psychol. 1941;28(112):286–340.
19.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
20.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
21.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
22.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
23.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
24.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
25.
go back to reference Osterrieth PA. The challenge of copying a complex figure. Arch Psychol. 1944;30(117–20):205–353. Osterrieth PA. The challenge of copying a complex figure. Arch Psychol. 1944;30(117–20):205–353.
26.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
27.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
28.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
29.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
30.
go back to reference 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. 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.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
32.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
33.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
34.
go back to reference John CH, Hemsley DR. Gestalt perception in schizophrenia. Eur Arch Psychiatry Clin Neurosci. 1992;241(4):215–21.PubMedCrossRef John CH, Hemsley DR. Gestalt perception in schizophrenia. Eur Arch Psychiatry Clin Neurosci. 1992;241(4):215–21.PubMedCrossRef
35.
go back to reference Becker EB, Stoodley CJ. Autism spectrum disorder and the cerebellum. Int Rev Neurobiol. 2013;113:1–34.PubMedCrossRef Becker EB, Stoodley CJ. Autism spectrum disorder and the cerebellum. Int Rev Neurobiol. 2013;113:1–34.PubMedCrossRef
37.
go back to reference 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.CrossRef 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.CrossRef
38.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
39.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
40.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
41.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
42.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
43.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
44.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
45.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
46.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
47.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
48.
go back to reference Meyers JE, Meyers KR. Rey complex figure test and recognition trial professional manual: psychological assessment. Odessa: Psychological Assessment Resources: 1995. Meyers JE, Meyers KR. Rey complex figure test and recognition trial professional manual: psychological assessment. Odessa: Psychological Assessment Resources: 1995.
49.
go back to reference Lezak MD. The complex figure test (CFT): copy administration. In: Neuropsychological assessment. 2nd ed. New York: Oxford University Press; 1983. p. 395–402. Lezak MD. The complex figure test (CFT): copy administration. In: Neuropsychological assessment. 2nd ed. New York: Oxford University Press; 1983. p. 395–402.
50.
go back to reference Wechsler Adult Intelligence Scale (WAIS). J Consult Psychol. 1955;19(4):319–20. Wechsler Adult Intelligence Scale (WAIS). J Consult Psychol. 1955;19(4):319–20.
51.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
52.
go back to reference Smith A. Symbol digit modalities test. Los Angeles: Western Psychological Services; 1982. Smith A. Symbol digit modalities test. Los Angeles: Western Psychological Services; 1982.
53.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
54.
go back to reference Wechsler D. Wechsler adult intelligence scale-third edition: administration and scoring manual. San Antonio: Psychological Corporation; 1997. Wechsler D. Wechsler adult intelligence scale-third edition: administration and scoring manual. San Antonio: Psychological Corporation; 1997.
55.
go back to reference Broshek DK, Barth JT, editors. The Halstead–Reitan neuropsychological test battery. New York: Wiley; 2000. Broshek DK, Barth JT, editors. The Halstead–Reitan neuropsychological test battery. New York: Wiley; 2000.
56.
go back to reference Radloff LS. The CES-D scale: a self-report depression scale for research in the general population. Appl Psychol Meas. 1977;1:385–401.CrossRef Radloff LS. The CES-D scale: a self-report depression scale for research in the general population. Appl Psychol Meas. 1977;1:385–401.CrossRef
57.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
58.
go back to reference Wilkinson GS. WRAT-3: wide range achievement test administration manual. Wide Range, Incorporated; 1993. Wilkinson GS. WRAT-3: wide range achievement test administration manual. Wide Range, Incorporated; 1993.
59.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
60.
61.
go back to reference 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 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
62.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
63.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
64.
65.
go back to reference Schmahmann JD, Weilburg JB, Sherman JC. The neuropsychiatry of the cerebellum—insights from the clinic. Cerebellum. 2007;6(3):254–67.PubMedCrossRef Schmahmann JD, Weilburg JB, Sherman JC. The neuropsychiatry of the cerebellum—insights from the clinic. Cerebellum. 2007;6(3):254–67.PubMedCrossRef
66.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
67.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
68.
go back to reference Ito M. Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci. 2008;9(4):304–13.PubMedCrossRef Ito M. Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci. 2008;9(4):304–13.PubMedCrossRef
69.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
70.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
71.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
72.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
73.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
74.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
75.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
76.
go back to reference Imamizu H, Kawato M. Cerebellar internal models: implications for the dexterous use of tools. Cerebellum. 2012;11(2):325–35.PubMedCrossRef Imamizu H, Kawato M. Cerebellar internal models: implications for the dexterous use of tools. Cerebellum. 2012;11(2):325–35.PubMedCrossRef
77.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
78.
79.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
Metadata
Title
Visuospatial Organization and Recall in Cerebellar Ataxia
Authors
Mitchell Slapik
Sharif I. Kronemer
Owen Morgan
Ryan Bloes
Seth Lieberman
Jordan Mandel
Liana Rosenthal
Cherie Marvel
Publication date
01-02-2019
Publisher
Springer US
Published in
The Cerebellum / Issue 1/2019
Print ISSN: 1473-4222
Electronic ISSN: 1473-4230
DOI
https://doi.org/10.1007/s12311-018-0948-z

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