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Functional brain effects of hand disuse in patients with trapeziometacarpal joint osteoarthritis: executed and imagined movements

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Abstract

The human trapeziometacarpal (TMC) joint has a crucial evolutionary importance as it permits rotation and opposition of the thumb to the other fingers. In chronic TMC joint osteoarthritis (i.e., rhizarthrosis), this motor ability, essential for pinching, grasping, and manipulating objects, may become difficult or impossible due to intolerable pain. Here, we assess whether patients with rhizarthrosis show signs of abnormal brain representation of hand movements. To this end, we studied 35 patients with rhizarthrosis, affecting predominantly one of the two hands, and 35 healthy subjects who underwent both behavioural and fMRI measures of brain activity during overtly executed or imagined thumb-to-finger-opposition movements. The patients with rhizarthrosis were slower than controls both in motor execution and imagination. In the patients, correlation between the motor execution and imagination times was preserved, even though such correlation was less strong than in normal controls. The fMRI measures showed reduced activation in the hand primary motor and dorsal premotor cortex for the patients only during explicit movements. This was true for both hands, yet more so for the most affected hand. No significant differences were seen for the motor imagery task. These results show that an orthopaedic disorder that reduces patients’ motoric repertoire in the absence of any neurological impairment is sufficient to induce neurofunctional changes in the cortical representation of hand movements. The substantial preservation of motor imagery with its neural counterparts distinguishes the neurological patterns of rhizarthrosis from those of complete immobilization or amputation suggesting that motor imagery may be used to boost motor recovery in rhizarthrosis after surgical treatment.

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Notes

  1. For example, two cycles of the thumb-to-finger opposition movement implied 8 taps, 4 taps for each cycle, whereas five cycles of the thumb-to-finger opposition movement (5 cycles) implied 20 taps.

  2. Total time/number of repetitions of the movement.

  3. For the patients, the data were labelled according to the more or less affected side and grouped accordingly.

  4. Subjects practiced the thumb-to-finger opposition task briefly until the desired 1 Hz pace was reached. It should be noted that this pace is roughly half of the tapping speed limit for both the patients and the controls (see the “Results’’ section, paragraph 3.1.4).

  5. The M.I. task used engages the participants in a subjective activity that does not lend itself by its nature to be objectively measured if not by asking the participants to report whether they had been able to perform the task.

  6. Even if this visual monitoring could not exclude the possibility that minimal movements might have occurred, we do not believe that the lack of an EMG recording represents a major issue (see also Zapparoli et al. 2013, footnote 5, page 535).

  7. One could rather argue that the patients’ reduced speed in motor imagery could be a sign of reduced cognitive competence. However, none of them had a single pathological score at the neuropsychological tests.

  8. Of course, an experiment in which subjects are challenged with forceful finger movements would have then introduced the likely confound of pain in the brain patterns of our subjects.

Abbreviations

TMC:

Trapeziometacarpal

TMS:

Transcranial magnetic stimulation

BOLD:

Blood oxygen-level dependent

fMRI:

Functional magnetic resonance imaging

FWER:

Family wise error rate

MRI:

Magnetic resonance imaging

SD:

Standard deviation

M1:

Primary motor cortex

S1:

Primary somatosensory cortex

M.E.:

Motor execution

M.I.:

Motor imagery

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Acknowledgements

This work was partially supported by the PRIN 2010-2011 grant to EP and by the PRIN 2010-2011 to MG [2010ENPRYE_005].

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Correspondence to Martina Gandola or Eraldo Paulesu.

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Gandola, M., Bruno, M., Zapparoli, L. et al. Functional brain effects of hand disuse in patients with trapeziometacarpal joint osteoarthritis: executed and imagined movements. Exp Brain Res 235, 3227–3241 (2017). https://doi.org/10.1007/s00221-017-5049-6

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  • DOI: https://doi.org/10.1007/s00221-017-5049-6

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