Elsevier

NeuroImage

Volume 45, Issue 2, 1 April 2009, Pages 500-511
NeuroImage

Short-term adaptation to a simple motor task: A physiological process preserved in multiple sclerosis

https://doi.org/10.1016/j.neuroimage.2008.12.006Get rights and content

Abstract

Short-term adaptation indicates the attenuation of the functional MRI (fMRI) response during repeated task execution. It is considered to be a physiological process, but it is unknown whether short-term adaptation changes significantly in patients with brain disorders, such as multiple sclerosis (MS). In order to investigate short-term adaptation during a repeated right-hand tapping task in both controls and in patients with MS, we analyzed the fMRI data collected in a large cohort of controls and MS patients who were recruited into a multi-centre European fMRI study. Four fMRI runs were acquired for each of the 55 controls and 56 MS patients at baseline and 33 controls and 26 MS patients at 1-year follow-up. The externally cued (1 Hz) right hand tapping movement was limited to 3 cm amplitude by using at all sites (7 at baseline and 6 at follow-up) identically manufactured wooden frames. No significant differences in cerebral activation were found between sites. Furthermore, our results showed linear response adaptation (i.e. reduced activation) from run 1 to run 4 (over a 25 minute period) in the primary motor area (contralateral more than ipsilateral), in the supplementary motor area and in the primary sensory cortex, sensory–motor cortex and cerebellum, bilaterally. This linear activation decay was the same in both control and patient groups, did not change between baseline and 1-year follow-up and was not influenced by the modest disease progression observed over 1 year. These findings confirm that the short-term adaptation to a simple motor task is a physiological process which is preserved in MS.

Introduction

The term “adaptation” is often used as a synonym of “plasticity” to indicate long-term changes or reorganisation in cortical activation pathways after brain injury, due e.g. to multiple sclerosis (MS) (Rocca et al., 2005, Enzinger and Fazekas, 2005, Buckle, 2005, Lee et al., 2000, Reddy et al., 2002a, Reddy et al., 2002b, Pantano et al., 2005, Pineiro et al., 2001) or stroke (Ward, 2005). However, adaptation or plasticity are terms also used to indicate short-term alterations in motor cortex excitability and/or changes in the location or extent of cortical representations following repeated task execution, as demonstrated in the motor cortex by transcranial magnetic stimulation (Butefisch et al., 2000, Ziemann et al., 2001, Classen et al., 1998), and also observed in different neural systems (Hagenbeek et al., 2007, Schafer et al., 2005, Dalton, 2000, Zufall and Leinders-Zufall, 2000, Strauss et al., 2005). Variations in BOLD activation similar to those often referred to as adaptation or plasticity have also been observed in motor skill acquisition, which is characterized by three main phases. During the early, highly attention-demanding phase both accuracy and stability of the task improve rapidly. During the intermediate phase, characterized by more established performance levels, accuracy and stability of the task advance more gradually until asymptotic performance is reached. The final phase of automatization or overlearning is characterized by feedforward instead of feedback control, allowing the performer to divert attention to other tasks (e.g. Puttemans et al. 2005). The BOLD signal variation observed during the three phases of motor skill acquisition therefore represent different mechanisms: changes in the first 2 phases represent effects of motor training, while changes in the last phase represent adaptation to an overlearned task. “Acute” motor plasticity has also been observed during surgery with intraoperative direct cortical stimulation, when cortical activated areas can be suddenly unmasked after tumour resection involving a second redundant site participating in the same movement (Duffau, 2001, Duffau, 2006).

It is however unclear whether adaptation in the motor cortex can be triggered in the short-term by brief performance of movements, or if repetitive performance of simple and unskilled but overlearned movements can cause representational changes.

Functional MRI (fMRI) is a non-invasive technique which began with the observation of signal loss around veins in MR images and has developed into a powerful tool that has revolutionized the study of human brain function (e.g. Jezzard and Buxton, 2006, McGonigle et al., 2000). fMRI is being applied increasingly in the clinical setting, with greatest interest directed towards clinical research (comparing groups of patients or patients receiving different treatments, or comparing patients with controls), but it can also be used in clinical practice for, e.g., presurgical planning in single subjects (Sorensen, 2006, Jezzard and Buxton, 2006, Bartsch et al., 2006, Enzinger and Fazekas, 2005). Often a single examination is assumed to give an accurate representation of a subject's functional neuroanatomy. However it has been shown that there are not only inter-subject, but also intra-subject variations in the BOLD contrast (Aguirre et al., 1998, McGonigle et al., 2000). Reproducibility of fMRI data has been a debated issue. Some studies show good or acceptable reproducibility (Loubinoux et al., 2001, Rombouts et al., 1998, Ramsey et al., 1998, Noll et al., 1997, Yetkin et al., 1996), others show high reproducibility for some tasks (e.g. hand and foot movement) but no reproducibility for other tasks (e.g. mouth movements) (Havel et al., 2006) or higher reproducibility in some cortical areas (e.g. motor cortex) than in others (e.g. basal ganglia and SMA) (Scholz et al., 2000). Further studies show substantial variation in data collected at different times or in different experiments (Miki et al., 2000, Zou et al., 2005, Ramsey et al., 1998), and others suggest that the locations of the activation areas on fMRI can be reproduced quite reliably, while their sizes fluctuates substantially (Alkadhi et al., 2002, Liu et al., 2004). One method of reducing the signal variability comprises acquiring more than one fMRI dataset and averaging the results. However, if adaptation is significant during multiple acquisitions, and if it differs significantly between controls and patients, then its effect on fMRI activation must be taken into account in the design and interpretation of such studies.

In this study, we used the term adaptation to indicate the attenuation of fMRI responses to continuous or repeated stimulation over time, which is an effect that has been observed in most neural systems at molecular, cellular, ensemble and systemic levels (Schafer et al. 2005, Strauss et al. 2005). This study investigates whether such adaptation is demonstrable using fMRI during repeated hand movements in a simple and well learned motor task, whether the activation decay is linear or exponential with time, and if it changes with the presence and/or progression of MS over a period of 1 year.

We hypothesized that adaptation to a simple task requiring no fine hand coordination and very little strength is detectable, since is a physiological process maybe due to a reduction of attention with time. We further postulated that the adaptation does not change significantly in MS patients compared to controls, and that it does not depend on age or level of disability. If these hypotheses are true, while adaptation may have a bearing on paradigm design, data from both patients and controls would be affected similarly and not including adaptation as a factor in the data analysis would not significantly change the study results. On the other hand, if the second hypothesis is not true, and adaptation varies between controls and patients, it will be essential to take this into account when analyzing and interpreting the results of similar studies. The primary aim of this study was therefore to evaluate whether or not it is necessary to take adaptation into account in the design and interpretation of a study using a repetitive simple motor task.

To address this question we analyzed a large data-set of fMRI scans acquired in a multi-centre study in controls and MS patients at baseline and one year follow-up, taking into consideration also subject age, and measures of disability such as hand dexterity, lesion load, and clinical scales. The baseline data have been previously analyzed to investigate differences between controls and MS patients in the fMRI activation elicited by hand movement and to relate these changes to clinical measures (Wegner et al., 2008).

Section snippets

Methods

The data included in the present paper were acquired at 8 sites: Department of Radiology, VU University Medical Centre, Amsterdam (Netherlands); MR Unit, Hospital Vall d'Hebron, Barcelona (Spain); Neurology/Neuroradiology Department, University of Basel, Basel (Switzerland); MR Research Unit, Medical University Graz, Graz (Austria); Queen Square Imaging Centre, Institute of Neurology, University College London, London (UK); Neuroimaging Research Unit, Scientific Institute and University,

Results

In the patient group, composed (as demonstrated in Table 1) of young subjects, mildly disabled, with low lesion load, there was a slight increase in the EDSS score between baseline and 1 year (p = 0.05) and a significant increase in T2 lesion load (p = 0.004) (Table 1).

Discussion

In this study the hand movement was standardised across patients and sites, and the subjects were trained to perform the task before fMRI scanning, so that it was well learned. Visual observation showed that the subjects performed the task correctly for the whole duration of the test. Analysis of variance did not show any significant differences between centres for the main effects of task (average of 4 runs), in agreement with results reported previously (Wegner et al., 2008, Zou et al., 2005

Conclusions

No significant between-centre differences were found in our multi-centre study. Our results showed that for 4 consecutive fMRI runs with right-hand tapping, a linear decay in activation over time was observed not only in the primary motor area, but also in the sensory cortex, SMA and cerebellum. This adaptation appears to be a physiological process expressed in both controls and patients, which is not influenced by the diagnosis of MS or its progression over a period of 1 year and is therefore

Acknowledgments

The authors would like to thank Prof. John Rothwell for his helpful comments on the manuscript.

The Queen Square Imaging Centre (QSIC) for funding the study and the QSIC's radiographers for their help with the data acquisition and handling of subjects. O. Ciccarelli is a Wellcome Advanced Clinical Fellow. The MS centre in Amsterdam is supported (grant 05-358c) by the Dutch MS Research Foundation (Voorschoten, The Netherlands). Further, the Dutch MS Research Foundation (Voorschoten, The

References (55)

  • RomboutsS.A. et al.

    Within-subject reproducibility of visual activation patterns with functional magnetic resonance imaging using multislice echo planar imaging

    Magn. Reson. Imaging

    (1998)
  • ScholzV.H. et al.

    Laterality, somatotopy and reproducibility of the basal ganglia and motor cortex during motor tasks

    Brain Res.

    (2000)
  • StraussM.M. et al.

    fMRI of sensitization to angry faces

    NeuroImage

    (2005)
  • AlkadhiH. et al.

    Reproducibility of primary motor cortex somatotopy under controlled conditions

    Am. J. Neuroradiol.

    (2002)
  • BartschA.J. et al.

    Diagnostic functional MRI: illustrated clinical applications and decision-making

    J. Magn. Reson. Imag.

    (2006)
  • BakshiR.

    Fatigue associated with multiple sclerosis: diagnosis, impact and management

    Mult. Scler.

    (2003)
  • BenwellN.M. et al.

    Primary sensorimotor cortex activation with task-performance after fatiguing hand exercise

    Exp. Brain Res.

    (2005)
  • BenwellN.M. et al.

    Reduced functional activation after fatiguing exercise is not confined to primary motor areas

    Exp. Brain Res.

    (2006)
  • BenwellN.M. et al.

    Changes in the functional MR signal in motor and non-motor areas during intermittent fatiguing hand exercise

    Exp. Brain Res.

    (2007)
  • BuckleG.J.

    Functional magnetic resonance imaging and multiple sclerosis: the evidence for neuronal plasticity

    J Neuroimag.

    (2005)
  • ButefischC.M. et al.

    Proc. Nat. Acad. Sci. U. S. A

    (2000)
  • ClassenJ. et al.

    Rapid plasticity of human cortical movement representation induced by practice

    J. Neurophys.

    (1998)
  • ColomboB. et al.

    MRI and motor evoked potential findings in nondisabled multiple sclerosis patients with and without symptoms of fatigue

    J. Neurol.

    (2000)
  • DaltonP.

    Psychophysical and behavioral characteristics of olfactory adaptation

    Chem. Senses

    (2000)
  • DonaldsonD.I. et al.

    Effective paradigm design

  • DuffauH.

    Acute functional reorganisation of the human motor cortex during resection of central lesions: a study using intraoperative brain mapping

    J. Neurol. Neurosurg. Psychiatry

    (2001)
  • HagenbeekR.E. et al.

    Nonlinear changes in brain activity during continuous word repetition: an event-related multiparametric functional MR imaging study

    AJNR Am. J. Neuroradiol.

    (2007)
  • Cited by (34)

    • The neural underpinnings of motor learning in people with neurodegenerative diseases: A scoping review

      2021, Neuroscience and Biobehavioral Reviews
      Citation Excerpt :

      There have been relatively few studies that measure brain activity during motor learning in people with MS. However, initial baseline measures show higher activation in many related motor learning regions. Initial hyperactivity of brain regions has been observed to decrease at a similar rate to healthy participants during simple task learning but decrease in an altered pattern during more complex motor learning tasks (Mancini et al., 2009; Tomassini et al., 2012). Demyelination of the corpus callosum characterized by white matter degradation and resting functional connectivity impairments, correlated with declines in explicit aspects of motor learning but not implicit motor learning ability compared to controls (Bonzano et al., 2011a; Fling et al., 2015; Peterson et al., 2017; Tomassini et al., 2012, 2011).

    • A greater involvement of posterior brain areas in interhemispheric transfer in autism: FMRI, DWI and behavioral evidences

      2015, NeuroImage: Clinical
      Citation Excerpt :

      The interstimulus intervals (ISIs) were longer than in the task outside the scanner, which allowed the hemodynamic response to return to baseline between trials. The ISI was varied pseudo-randomly between 5000 and 12,000 ms as follows: 6 × 5000 ms, 5 × 6000 ms, 4 × 7000 ms, 3 × 8000 ms, 1 × 10,000 ms, 1 × 11,000 ms, and 1 × 12,000 ms, with an average of about 7000 ms. In motor related areas, fMRI activation decays linearly over time during the repeated execution of motor response paradigms (Mancini et al., 2009); therefore, an event related design was chosen to optimize the detection sensitivity. Long ISIs improve the sensitivity of the signal (Price et al., 2006) and reduce predictability.

    • Plasticity of the motor system in multiple sclerosis

      2014, Neuroscience
      Citation Excerpt :

      The question of whether the basic mechanisms of rapid-onset central motor plasticity are available in patients with stable RRMS was assessed by two fMRI studies, though with inconsistent results. One of the studies showed a decay of regional brain activation by a tapping task over consecutive runs, with comparable changes in MS patients and matched controls (Mancini et al., 2009), while the other study demonstrated the absence of such task-specific reductions of activation (Morgen et al., 2004). This discrepancy indeed points out that direct inference from functional imaging studies on physiological mechanisms is limited, with BOLD signal changes indicating associated brain activation rather than establishing causal relationships.

    • Expert athletes activate somatosensory and motor planning regions of the brain when passively listening to familiar sports sounds

      2014, Brain and Cognition
      Citation Excerpt :

      Beilock et al. (2008) also found motor expertise effects in a fMRI experiment with three varying levels of hockey expertise: player, fan, and novice. Results revealed a positive correlation between hockey experience and neural activity in left dorsal premotor cortex, a region usually implemented in higher-level action selection and implementation (Haslinger et al., 2002), and a negative correlation between hockey experience and activity in right sensory-motor cortex, a lower level sensory-motor region implicated in the instantiation of movement (Bedard & Sanes, 2009; Mancini et al., 2009). Taken together these results suggest that experts engage in motor preparation in response to the perception of highly familiar stimuli, and that this has to do with their expertise with executing the specific action (Beilock et al., 2008; Calvo-Merino et al., 2005, 2006).

    View all citing articles on Scopus
    View full text