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01-06-2016 | Original Paper

Cerebellar fMRI Activation Increases with Increasing Working Memory Demands

Authors: M. Küper, P. Kaschani, M. Thürling, M. R. Stefanescu, R. G. Burciu, S. Göricke, S. Maderwald, M. E. Ladd, H. Hautzel, D. Timmann

Published in: The Cerebellum | Issue 3/2016

Abstract

The aim of the present study was to explore cerebellar contributions to the central executive in n-back working memory tasks using 7-T functional magnetic imaging (fMRI). We hypothesized that cerebellar activation increased with increasing working memory demands. Activations of the cerebellar cortex and dentate nuclei were compared between 0-back (serving as a motor control task), 1-back, and 2-back working memory tasks for both verbal and abstract modalities. A block design was used. Data of 27 participants (mean age 26.6 ± 3.8 years, female/male 12:15) were included in group statistical analysis. We observed that cerebellar cortical activations increased with higher central executive demands in n-back tasks independent of task modality. As confirmed by subtraction analyses, additional bilateral activations following higher executive demands were found primarily in four distinct cerebellar areas: (i) the border region of lobule VI and crus I, (ii) inferior parts of the lateral cerebellum (lobules crus II, VIIb, VIII, IX), (iii) posterior parts of the paravermal cerebellar cortex (lobules VI, crus I, crus II), and (iv) the inferior vermis (lobules VI, VIIb, VIII, IX). Dentate activations were observed for both verbal and abstract modalities. Task-related increases were less robust and detected for the verbal n-back tasks only. These results provide further evidence that the cerebellum participates in an amodal bilateral neuronal network representing the central executive during working memory n-back tasks.

K-H E, Chen S-HA, Ho M-HR, Desmond JE. A meta-analysis of cerebellar contributions to higher cognition from PET and fMRI studies. Hum Brain Mapp. 2014;35:593–615.CrossRef

Peterburs J, Bellebaum C, Koch B, Schwarz M, Daum I. Working memory and verbal fluency deficits following cerebellar lesions: relation to interindividual differences in patient variables. Cerebellum. 2010;9:375–83.CrossRefPubMed

Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. NeuroImage. 2009;44:489–501.CrossRefPubMed

Stoodley CJ, Schmahmann JD. Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex. 2010;46:831–44.CrossRefPubMedPubMedCentral

Baddeley AD, Hitch G. Working memory. Psychol. Learn. Motiv. 1st ed. New York: Academic Press; 1974. p. 47–89.

Baddeley null. The episodic buffer: a new component of working memory? Trends Cogn Sci 2000;4:417–23.

Smith EE, Jonides J. Storage and executive processes in the frontal lobes. Science. 1999;283:1657–61.CrossRefPubMed

Walter H, Bretschneider V, Grön G, Zurowski B, Wunderlich AP, Tomczak R, et al. Evidence for quantitative domain dominance for verbal and spatial working memory in frontal and parietal cortex. Cortex. 2003;39:897–911.CrossRefPubMed

Hautzel H, Mottaghy FM, Schmidt D, Zemb M, Shah NJ, Müller-Gärtner H-W, et al. Topographic segregation and convergence of verbal, object, shape and spatial working memory in humans. Neurosci Lett. 2002;323:156–60.CrossRefPubMed

10.

Rottschy C, Langner R, Dogan I, Reetz K, Laird AR, Schulz JB, et al. Modelling neural correlates of working memory: a coordinate-based meta-analysis. NeuroImage. 2012;60:830–46.CrossRefPubMedPubMedCentral

11.

Sternberg S. High-speed scanning in human memory. Science. 1966;153:652–4.CrossRefPubMed

12.

Cohen JD, Forman SD, Braver TS, Casey BJ, Servan-Schreiber D, Noll DC. Activation of the prefrontal cortex in a nonspatial working memory task with functional MRI. Hum Brain Mapp. 1993;1:293–304.CrossRef

13.

Hautzel H, Mottaghy FM, Specht K, Müller H-W, Krause BJ. Evidence of a modality-dependent role of the cerebellum in working memory? An fMRI study comparing verbal and abstract n-back tasks. NeuroImage. 2009;47:2073–82.CrossRefPubMed

14.

Thürling M, Hautzel H, Küper M, Stefanescu MR, Maderwald S, Ladd ME, et al. Involvement of the cerebellar cortex and nuclei in verbal and visuospatial working memory: a 7 T fMRI study. NeuroImage. 2012;62:1537–50.CrossRefPubMed

15.

Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9:97–113.CrossRefPubMed

16.

Arnoult MD, Attneave F. The quantitative study of shape and pattern perception. Psychol Bull. 1956;53:452–71.CrossRefPubMed

17.

Thürling M, Küper M, Stefanescu R, Maderwald S, Gizewski ER, Ladd ME, et al. Activation of the dentate nucleus in a verb generation task: a 7T MRI study. NeuroImage. 2011;57:1184–91.CrossRefPubMed

18.

Diedrichsen J. A spatially unbiased atlas template of the human cerebellum. NeuroImage. 2006;33:127–38.CrossRefPubMed

19.

Friston KJ, Frith CD, Turner R, Frackowiak RS. Characterizing evoked hemodynamics with fMRI. NeuroImage. 1995;2:157–65.CrossRefPubMed

20.

Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N. A probabilistic MR atlas of the human cerebellum. NeuroImage. 2009;46:39–46.CrossRefPubMed

21.

Schmahmann JD, Doyon J, McDonald D, Holmes C, Lavoie K, Hurwitz AS, et al. Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space. NeuroImage. 1999;10:233–60.CrossRefPubMed

22.

Diedrichsen J, Maderwald S, Küper M, Thürling M, Rabe K, Gizewski ER, et al. Imaging the deep cerebellar nuclei: a probabilistic atlas and normalization procedure. NeuroImage. 2011;54:1786–94.CrossRefPubMed

23.

Hayasaka S, Nichols TE. Validating cluster size inference: random field and permutation methods. NeuroImage. 2003;20:2343–56.CrossRefPubMed

24.

Küper M, Dimitrova A, Thürling M, Maderwald S, Roths J, Elles HG, et al. Evidence for a motor and a non-motor domain in the human dentate nucleus—an fMRI study. NeuroImage. 2011;54:2612–22.CrossRefPubMed

25.

Küper M, Thürling M, Stefanescu R, Maderwald S, Roths J, Elles HG, et al. Evidence for a motor somatotopy in the cerebellar dentate nucleus-an fMRI study in humans. Hum Brain Mapp. 2012;33:2741–9.CrossRefPubMed

26.

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

27.

Marvel CL, Desmond JE. Functional topography of the cerebellum in verbal working memory. Neuropsychol Rev. 2010;20:271–9.CrossRefPubMedPubMedCentral

28.

Chen SHA, Desmond JE. Temporal dynamics of cerebro-cerebellar network recruitment during a cognitive task. Neuropsychologia. 2005;43:1227–37.CrossRefPubMed

29.

Marvel CL, Desmond JE. The contributions of cerebro-cerebellar circuitry to executive verbal working memory. Cortex. 2010;46:880–95.CrossRefPubMedPubMedCentral

30.

Desmond JE, Gabrieli JD, Wagner AD, Ginier BL, Glover GH. Lobular patterns of cerebellar activation in verbal working-memory and finger-tapping tasks as revealed by functional MRI. J Neurosci. 1997;17:9675–85.PubMed

31.

Coffman KA, Dum RP, Strick PL. Cerebellar vermis is a target of projections from the motor areas in the cerebral cortex. Proc Natl Acad Sci U S A. 2011;108:16068–73.CrossRefPubMedPubMedCentral

32.

Glickstein M, Sultan F, Voogd J. Functional localization in the cerebellum. Cortex. 2011;47:59–80.CrossRefPubMed

33.

Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain. 1998;121:561–79.CrossRefPubMed

34.

Puget S, Boddaert N, Viguier D, Kieffer V, Bulteau C, Garnett M, et al. Injuries to inferior vermis and dentate nuclei predict poor neurological and neuropsychological outcome in children with malignant posterior fossa tumors. Cancer. 2009;115:1338–47.CrossRefPubMed

35.

Courchesne E, Yeung-Courchesne R, Press GA, Hesselink JR, Jernigan TL. Hypoplasia of cerebellar vermal lobules VI and VII in autism. N Engl J Med. 1988;318:1349–54.CrossRefPubMed

36.

Mostofsky SH, Mazzocco MM, Aakalu G, Warsofsky IS, Denckla MB, Reiss AL. Decreased cerebellar posterior vermis size in fragile X syndrome: correlation with neurocognitive performance. Neurology. 1998;50:121–30.CrossRefPubMed

37.

Stoodley CJ. Distinct regions of the cerebellum show gray matter decreases in autism, ADHD, and developmental dyslexia. Front Syst Neurosci. 2014;8:92.CrossRefPubMedPubMedCentral

38.

Berquin PC, Giedd JN, Jacobsen LK, Hamburger SD, Krain AL, Rapoport JL, et al. Cerebellum in attention-deficit hyperactivity disorder: a morphometric MRI study. Neurology. 1998;50:1087–93.CrossRefPubMed

39.

Bledsoe J, Semrud-Clikeman M, Pliszka SR. A magnetic resonance imaging study of the cerebellar vermis in chronically treated and treatment-naïve children with attention-deficit/hyperactivity disorder combined type. Biol Psychiatry. 2009;65:620–4.CrossRefPubMedPubMedCentral

40.

Willcutt EG, Doyle AE, Nigg JT, Faraone SV, Pennington BF. Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biol Psychiatry. 2005;57:1336–46.CrossRefPubMed

41.

Strick PL, Dum RP, Fiez JA. Cerebellum and nonmotor function. Annu Rev Neurosci. 2009;32:413–34.CrossRefPubMed

42.

Owen AM, McMillan KM, Laird AR, Bullmore E. N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp. 2005;25:46–59.CrossRefPubMed

43.

Nagel IE, Preuschhof C, Li S-C, Nyberg L, Bäckman L, Lindenberger U, et al. Load modulation of BOLD response and connectivity predicts working memory performance in younger and older adults. J Cogn Neurosci. 2011;23:2030–45.CrossRefPubMed

44.

Hashimoto M, Takahara D, Hirata Y, Inoue K, Miyachi S, Nambu A, et al. Motor and non-motor projections from the cerebellum to rostrocaudally distinct sectors of the dorsal premotor cortex in macaques. Eur J Neurosci. 2010;31:1402–13.CrossRefPubMed

45.

Kelly RM, Strick PL. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci. 2003;23:8432–44.PubMed

46.

Prevosto V, Graf W, Ugolini G. Cerebellar inputs to intraparietal cortex areas LIP and MIP: functional frameworks for adaptive control of eye movements, reaching, and arm/eye/head movement coordination. Cereb Cortex. 2010;20:214–28.CrossRefPubMedPubMedCentral

47.

Habas C, Kamdar N, Nguyen D, Prater K, Beckmann CF, Menon V, et al. Distinct cerebellar contributions to intrinsic connectivity networks. J Neurosci. 2009;29:8586–94.CrossRefPubMedPubMedCentral

48.

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

49.

Koziol LF, Budding D, Andreasen N, D’Arrigo S, Bulgheroni S, Imamizu H, et al. Consensus paper: the cerebellum’s role in movement and cognition. Cerebellum. 2014;13:151–77.CrossRefPubMedPubMedCentral

50.

Wolpert DM, Kawato M. Multiple paired forward and inverse models for motor control. Neural Netw. 1998;11:1317–29.CrossRefPubMed

51.

Imamizu H, Kuroda T, Miyauchi S, Yoshioka T, Kawato M. Modular organization of internal models of tools in the human cerebellum. Proc Natl Acad Sci. 2003;100:5461–6.CrossRefPubMedPubMedCentral

52.

Vandervert LR, Schimpf PH, Liu H. How working memory and the cerebellum collaborate to produce creativity and innovation. Creat Res J. 2007;19:1–18.CrossRef

53.

Koziol LF, Lutz JT. From movement to thought: the development of executive function. Appl Neuropsychol Child. 2013;2:104–15.CrossRefPubMed

Title: Cerebellar fMRI Activation Increases with Increasing Working Memory Demands
Authors: M. Küper
P. Kaschani
M. Thürling
M. R. Stefanescu
R. G. Burciu
S. Göricke
S. Maderwald
M. E. Ladd
H. Hautzel
D. Timmann
Publication date: 01-06-2016
Publisher: Springer US
Published in: The Cerebellum / Issue 3/2016
Print ISSN: 1473-4222
Electronic ISSN: 1473-4230
DOI: https://doi.org/10.1007/s12311-015-0703-7

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Cerebellar fMRI Activation Increases with Increasing Working Memory Demands

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