Skip to main content
Log in

Neural correlates of adaptation to gradual and to sudden visuomotor distortions in humans

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

This study aimed at scrutinizing the neural correlates of sensorimotor adaptation. Subjects were exposed either to a gradually (group G) or to a suddenly introduced perturbation (group S) followed by a test of aftereffects. They were also exposed to a control condition equated for their movement errors during the adaptation condition. We registered subjects’ brain activity by functional magnetic resonance imaging. Behavioral data revealed no difference between aftereffects in G and S, while imaging data suggest different neural correlates. Direct comparison between groups showed more adaptation-related activation in left cingulate and inferior frontal as well as right caudate and temporal areas in S than in G. In contrast, no neural activity was related more to G than to S and no common activations were found for both groups. Within-group analyses further revealed right inferior parietal lobe, cerebellar and cingulate cortex activity in group S and activation of frontal lobe and left cerebellum in group G for a contrast between adaptation condition and baseline. Less brain activity was observed when controlled for movement errors: the contrast between adaptation and control condition yielded left occipital lobe activity in group S, and left posterior dentate nucleus and brainstem activity in group G. The present data confirm an involvement of the cerebellar cortex in error processing during sudden adaptation, since this activation was found for the contrast ‘adaptation–baseline’ but not for ‘adaptation–control.’ In addition, our data suggest an involvement of deep cerebellar nuclei in the adaptation to gradually introduced distortions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Anguera JA, Russell CA, Noll DC, Seidler RD (2007) Neural correlates associated with intermanual transfer of sensorimotor adaptation. Brain Res 1185:136–151

    Article  CAS  PubMed  Google Scholar 

  • Balslev D, Nielsen FA, Frutiger SA, Sidtis JJ, Christiansen TB, Svarer C, Strother SC, Rottenberg DA, Hansen LK, Paulson OB, Law I (2002) Cluster analysis of activity-time series in motor learning. Hum Brain Mapp 15:135–145

    Article  PubMed  Google Scholar 

  • Benson BL, Anguera JA, Seidler RD (2011) A spatial explicit strategy reduces error but interferes with sensorimotor adaptation. J Neurophysiol 105:2843–2851

    Article  PubMed Central  PubMed  Google Scholar 

  • Bock O (2005) Components of sensorimotor adaptation in young and elderly subjects. Exp Brain Res 160:259–263

    Article  PubMed  Google Scholar 

  • Bock O, Schmitz G (2011) Adaptation to rotated visual feedback depends on the number and spread of target directions. Exp Brain Res 209:409–413

    Article  PubMed  Google Scholar 

  • Buch ER, Young S, Contreras-Vidal JL (2003) Visuomotor adaptation in normal aging. Learn Mem 10:55–63

    Article  PubMed Central  PubMed  Google Scholar 

  • Carter CS, Braver TS, Barch DM, Botvinick MM, Noll D, Cohen JD (1998) Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280:747–749

    Article  CAS  PubMed  Google Scholar 

  • Clower DM, Hoffman JM, Votaw JR, Faber TL, Woods RP, Alexander GE (1996) Role of posterior parietal cortex in the recalibration of visually guided reaching. Nature 383:618–621

    Article  CAS  PubMed  Google Scholar 

  • Cressmann EK, Franks IM, Enns JT, Chua R (2006) No automatic pilot for visually guided aiming based on colour. Exp Brain Res 171:174–183

    Article  Google Scholar 

  • Criscimagna-Hemminger SE, Bastian AJ, Shadmehr R (2010) Size of error affects cerebellar contributions to motor learning. J Neurophysiol 103:2275–2284

    Article  PubMed Central  PubMed  Google Scholar 

  • Della-Maggiore V, McIntosh AR (2005) Time course of changes in brain activity and functional connectivity associated with long-term adaptation to a rotational transformation. J Neurophysiol 93:2254–2262

    Article  PubMed  Google Scholar 

  • Dewar R (1971) Adaptation to displaced vision: variations on the “prismatic shaping” technique. Percept Psychophys 9:155–157

    Google Scholar 

  • Diedrichsen J, Hashambhoy Y, Rane T, Shadmehr R (2005) Neural correlates of reach errors. J Neurosci 25:9919–9931

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N (2009) A probabilistic MR atlas of the human cerebellum. Neuroimage 46:39–46

    Article  PubMed  Google Scholar 

  • Dimitrova A, Zeljko D, Schwarze F, Maschke M, Gerwig M, Frings M, Beck A, Aurich V, Forsting M, Timmann D (2006) Probabilistic 3D MRI atlas of the human cerebellar dentate/interposed nuclei. Neuroimage 30:12–25

    Article  CAS  PubMed  Google Scholar 

  • Donchin O, Francis JT, Shadmehr R (2003) Quantifying generalization from trial-by-trial behavior of adaptive systems that learn with basis functions: theory and experiments in human motor control. J Neurosci 23:9032–9045

    CAS  PubMed  Google Scholar 

  • Ebenholtz SM, Mayer D (1968) Rate of adaptation under constant and varied optical tilt. Percept Mot Skills 26:507–509

    Article  CAS  PubMed  Google Scholar 

  • Fine MS, Thoroughman KA (2006) Motor adaptation to single force pulses: sensitive to direction but insensitive to within-movement pulse placement and magnitude. J Neurophysiol 96:710–720

    Article  PubMed  Google Scholar 

  • Fine MS, Thoroughman KA (2007) Trial-by-trial transformation of error into sensorimotor adaptation changes with environmental dynamics. J Neurophysiol 98:1392–1404

    Article  PubMed  Google Scholar 

  • Floyer-Lea A, Matthews PM (2004) Changing brain networks for visuomotor control with increased movement automaticity. J Neurophysiol 92:2405–2412

    Google Scholar 

  • Flament D, Ellermann J, Kim SG, Ugurbil K, Ebner TJ (1996) Functional magnetic resonance imaging of cerebellar activation during the learning of a visuomotor dissociation task. Hum Brain Mapp 4:210–226

    Article  CAS  PubMed  Google Scholar 

  • Galea JM, Sami SA, Albert NB, Miall RC (2010) Secondary tasks impair adaptation to step- and gradual-visual displacements. Exp Brain Res 202:473–484

    Article  CAS  PubMed  Google Scholar 

  • Gibo TL, Criscimagna-Hemminger SE, Okamura AM, Bastian AJ (2013) Cerebellar motor learning: are environment dynamics more important than error size? J Neurophysiol 110(2):322–333

    Article  PubMed  Google Scholar 

  • Girgenrath M, Bock O, Seitz RJ (2007) An fMRI study of brain activation in a visual adaptation task: activation limited to sensory guidance. Exp Brain Res 184:561–569

    Article  PubMed  Google Scholar 

  • Grafton ST, Schmitt P, Van Horn J, Diedrichsen J (2008) Neural substrates of visuomotor learning based on improved feedback control and prediction. Neuroimage 39:1383–1395

    Article  PubMed Central  PubMed  Google Scholar 

  • Graydon FX, Friston KJ, Thomas CG, Brooks VB, Menon RS (2005) Learning-related fMRI activation associated with a rotational visuomotor transformation. Brain Res Cogn Brain Res 22:373–383

    Google Scholar 

  • Imamizu H, Miyauchi S, Tamada T, Sasaki Y, Takino R, Putz B, Yoshioka T, Kawato M (2000) Human cerebellar activity reflecting an acquired internal model of a new tool. Nature 403:192–195

    Article  CAS  PubMed  Google Scholar 

  • Imamizu H, Kuroda T, Miyauchi S, Yoshioka T, Kawato M (2003) Modular organization of internal models of tools in the human cerebellum. Proc Natl Acad Sci USA 100:5461–5466

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ingram HA, van Donkelaar P, Cole J, Vercher JL, Gauthier GM, Miall RC (2000) The role of proprioception and attention in a visuomotor adaptation task. Exp Brain Res 132:114–126

    Article  CAS  PubMed  Google Scholar 

  • Inoue K, Kawashima R, Satoh K, Kinomura S, Sugiura M, Goto R, Ito M, Fukuda H (2000) A PET study of visuomotor learning under optical rotation. Neuroimage 11:505–516

    Article  CAS  PubMed  Google Scholar 

  • Kagerer FA, Contreras-Vidal JL, Bo J, Clark JE (2006) Abrupt, but not gradual visuomotor distortion facilitates adaptation in children with developmental coordination disorder. Hum Mov Sci 25(4–5):622–633

    Google Scholar 

  • Kagerer FA, Contreras-Vidal JL, Stelmach GE (1997) Adaptation to gradual as compared with sudden visuo-motor distortions. Exp Brain Res 115:557–561

    Article  CAS  PubMed  Google Scholar 

  • Keisler A, Shadmehr R (2010) A shared resource between declarative memory and motor memory. J Neurosci 30(44):14817–14823

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Klassen J, Tong C, Flanagan JR (2005) Learning and recall of incremental kinematic and dynamic sensorimotor transformations. Exp Brain Res 164:250–259

    Article  PubMed  Google Scholar 

  • Krakauer JW, Ghilardi MF, Mentis M, Barnes A, Veytsman M, Eidelberg D, Ghez C (2004) Differential cortical and subcortical activations in learning rotations and gains for reaching: a PET study. J Neurophysiol 91:924–933

    Google Scholar 

  • Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas CS, Rainey L, Kochunov PV, Nickerson D, Mikiten SA, Fox PT (2000) Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp 10:120–131

    Article  CAS  PubMed  Google Scholar 

  • Lang W, Lang M, Podreka I, Steiner M, Uhl F, Suess E, Müller C, Deecke L et al (1988) DC-potential shifts and regional cerebral blood flow reveal frontal cortex involvement in human visuomotor learning. Exp Brain Res 71:353–364

    Google Scholar 

  • Luaute J, Schwartz S, Rossetti Y, Spiridon M, Rode G, Boisson D, Vuilleumier P (2009) Dynamic changes in brain activity during prism adaptation. J Neurosci 29:169–178

    Article  CAS  PubMed  Google Scholar 

  • Malfait N, Ostry DJ (2004) Is interlimb transfer of force-field adaptation a cognitive response to the sudden introduction of load? J Neurosci 24:8084–8089

    Article  CAS  PubMed  Google Scholar 

  • Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT (1996) Throwing while looking through prisms. I. Focal olivocerebellar lesions impair adaptation. Brain 119(Pt 4):1183–1198

    Article  PubMed  Google Scholar 

  • Maschke M, Gomez CM, Ebner TJ, Konczak J (2004) Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements. J Neurophysiol 91:230–238

    Article  PubMed  Google Scholar 

  • Michel C, Pisella L, Prablanc C, Rode G, Rossetti Y (2007) Enhancing visuomotor adaptation by reducing error signals: single-step (aware) versus multiple-step (unaware) exposure to wedge prisms. J Cogn Neurosci 19:341–350

    Article  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  CAS  PubMed  Google Scholar 

  • Orban de Xivry JJ, Criscimagna-Hemminger SE, Shadmehr R (2011) Contributions of the motor cortex to adaptive control of reaching depend on the perturbation schedule. Cereb Cortex 21:1475–1484

    Article  PubMed Central  PubMed  Google Scholar 

  • Rabe K, Livne O, Gizewski ER, Aurich V, Beck A, Timmann D, Donchin O (2009) Adaptation to visuomotor rotation and force field perturbation is correlated to different brain areas in patients with cerebellar degeneration. J Neurophysiol 101:1961–1971

    Article  CAS  PubMed  Google Scholar 

  • Robertson EM, Miall RC (1999) Visuomotor adaptation during inactivation of the dentate nucleus. Neuroreport 10:1029–1034

    Google Scholar 

  • Schaefer SY, Shelly IL, Thoroughman KA (2012) Beside the point: motor adaptation without feedback-based error correction in task-irrelevant conditions. J Neurophysiol 107:1247–1256

    Article  PubMed Central  PubMed  Google Scholar 

  • Scheidt RA, Dingwell JB, Mussa-Ivaldi FA (2001) Learning to move amid uncertainty. J Neurophysiol 86:971–985

    CAS  PubMed  Google Scholar 

  • Schlerf JE, Xu J, Klemfuss NM, Griffiths TL, Ivry RB (2013) Individuals with cerebellar degeneration show similar adaptation deficits with large and small visuomotor errors. J Neurophysiol 109:1164–1173

    Article  PubMed Central  PubMed  Google Scholar 

  • Seidler RD, Noll DC, Chintalapati P (2006) Bilateral basal ganglia activation associated with sensorimotor adaptation. Exp Brain Res 175:544–555

    Article  CAS  PubMed  Google Scholar 

  • Semrau JA, Daitch AL, Thoroughman KA (2012) Environmental experience within and across testing days determines the strength of human visuomotor adaptation. Exp Brain Res 216:409–418

    Article  PubMed  Google Scholar 

  • Shadmehr R, Holcomb HH (1997) Neural correlates of motor memory consolidation. Science 277:821–825

    Article  CAS  PubMed  Google Scholar 

  • Smith MA, Ghazizadeh A, Shadmehr R (2006) Interacting adaptive processes with different timescales underlie short-term motor learning. PLoS Biol 4:e179

    Article  PubMed Central  PubMed  Google Scholar 

  • Takahashi CD, Scheidt RA, Reinkensmeyer DJ (2001) Impedance control and internal model formation when reaching in a randomly varying dynamical environment. J Neurophysiol 86:1047–1051

    CAS  PubMed  Google Scholar 

  • Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain: 3-dimensional proportional system: an approach to cerebral imaging. Georg Thieme, Stuttgart

    Google Scholar 

  • Tanaka H, Krakauer JW, Sejnowski TJ (2012) Generalization and multirate models of motor adaptation. Neural Comput 24:939–966

    Article  PubMed Central  PubMed  Google Scholar 

  • Taylor JA, Ivry RB (2011) Flexible cognitive strategies during motor learning. PLoS Comput Biol 7:e1001096

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Taylor JA, Wojaczynski GJ, Ivry RB (2011) Trial-by-trial analysis of intermanual transfer during visuomotor adaptation. J Neurophysiol 106:3157–3172

    Article  PubMed Central  PubMed  Google Scholar 

  • Tseng YW, Diedrichsen J, Krakauer JW, Shadmehr R, Bastian AJ (2007) Sensory prediction errors drive cerebellum-dependent adaptation of reaching. J Neurophysiol 98:54–62

    Article  PubMed  Google Scholar 

  • Tunik E, Schmitt PJ, Grafton ST (2007) BOLD coherence reveals segregated functional neural interactions when adapting to distinct torque perturbations. J Neurophysiol 97:2107–2120

    Article  PubMed Central  PubMed  Google Scholar 

  • Venkatakrishnan A, Banquet JP, Burnod Y, Contreras-vidal JL (2011) Parkinson’s disease differentially affects adaptation to gradual as compared to sudden visuomotor distortions. Hum Mov Sci 30:760–769

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang J, Joshi M, Lei Y (2011) The extent of interlimb transfer following adaptation to a novel visuomotor condition does not depend on awareness of the condition. J Neurophysiol 106:259–264

    Article  PubMed Central  PubMed  Google Scholar 

  • Werner S, Bock O, Timmann D (2009) The effect of cerebellar cortical degeneration on adaptive plasticity and movement control. Exp Brain Res 193:189–196

    Article  PubMed  Google Scholar 

  • Werner S, Bock O, Gizewski ER, Schoch B, Timmann D (2010) Visuomotor adaptive improvement and after effects are impaired differentially following cerebellar lesions in SCA and PICA territory. Exp Brain Res 201:429–439

    Article  PubMed Central  PubMed  Google Scholar 

  • Wolpert DM, Ghahramani Z, Jordan MI (1995) An internal model for sensorimotor integration. Science 269:1880–1882

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a scholarship of the German Sport University for female young scientists awarded to SW and by DFG Grant Bo 649/8 awarded to OB. Responsibility for contents rests with the authors. Thanks are due to Prof. Patrick Bedard and Markus Thürling for helpful discussions of the imaging data. Thanks also go to L. Geisen and H. Elles for software development and A. Brol and R. Pistor for assisting with data collection and processing.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Susen Werner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Werner, S., Schorn, C.F., Bock, O. et al. Neural correlates of adaptation to gradual and to sudden visuomotor distortions in humans. Exp Brain Res 232, 1145–1156 (2014). https://doi.org/10.1007/s00221-014-3824-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-014-3824-1

Keywords

Navigation