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Mental images across the adult lifespan: a behavioural and fMRI investigation of motor execution and motor imagery

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Abstract

Motor imagery (M.I.) is a mental state in which real movements are evoked without overt actions. There is some behavioural evidence that M.I. declines with ageing. The neurofunctional correlates of these changes have been investigated only in two studies, but none of the these studies has measured explicit correlations between behavioural variables and the brain response, nor the correlation of M.I. and motor execution (M.E.) of the same acts in ageing. In this paper, we report a behavioural and functional magnetic resonance imaging (fMRI) experiment that aimed to address this issue. Twenty-four young subjects (27 ± 5.6 years) and twenty-four elderly subjects (60 ± 4.6 years) performed two block-design fMRI tasks requiring actual movement (M.E.) or the mental rehearsal (M.I.) of finger movements. Participants also underwent a behavioural mental chronometry test in which the temporal correlations between M.I. and M.E. were measured. We found significant neurofunctional and behavioural differences between the elderly subjects and the young subjects during the M.E. and the M.I. tasks: for the M.E. task, the elderly subjects showed increased activation in frontal and prefrontal (pre-SMA) cortices as if M.E. had become more cognitively demanding; during the M.I. task, the elderly over-recruited occipito-temporo-parietal areas, suggesting that they may also use a visual imagery strategy. We also found between-group behavioural differences in the mental chronometry task: M.I. and M.E. were highly correlated in the young participants but not in the elderly participants. The temporal discrepancy between M.I. and M.E. in the elderly subjects correlated with the brain regions that showed increased activation in the occipital lobe in the fMRI. The same index was correlated with the premotor regions in the younger subjects. These observations show that healthy elderly individuals have decreased or qualitatively different M.I. compared to younger subjects.

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Notes

  1. M.I. tasks can be explicit or implicit: in a typical implicit M.I. task, subjects are asked to judge whether a tool is oriented conveniently for being grasped with the right or with the left hand; it is assumed that a mental motor simulation process is used to solve the task. Another example of an implicit M.I. task is the hand laterality judgement task: subjects are asked to judge whether a picture depicts a left rather than a right hand; once debriefed, subjects typically report to have imagined their own hand at the orientation of the visual stimulus. On the other hand, in actual motor tasks, like the one adopted here, subjects are invited to mentally rehearse motor acts as if they were performing them but avoiding overt motor production.

  2. For the finger opposition task, there were minor differences between the fMRI and the task performed outside the scanner (during the behavioural task we varied the number of repetitions of the finger tapping (from 2 to 5 cycle). These were needed in order to collect meaningful behavioural data outside the scanner while keeping the subjects sufficiently involved in the task.

  3. When determining the ideal task for the experiments inside and outside the MRI scanner, a number of factors were taken into account, including compatibility with the fMRI environment and the magnitude of the cortical representation within the motor and premotor cortex for the body segment under investigation. We chose the finger opposition tasks because these tasks have been widely used in functional neuroimaging experiments (see for a review: Witt et al. 2008) and in M.I. investigations using both behavioural (see for example Sirigu et al. 1996) and neurofunctional techniques (see for example Guillot et al. 2009). Based on the same considerations, we decided not to use some interesting motor behaviours, such as pointing (Skoura et al. 2008), lifting one arm (Personnier et al. 2008), or walking (Skoura et al. 2005), despite the potential contribution these tasks could make to the investigation of M.I. in behavioural experiments.

  4. The group by task interaction effects are called “larger activations” or “additional activations,” depending on whether the reference group had rather than not some activations in the given area.

  5. A common objection to the concept of M.I. and its motoric nature as demonstrated by functional neuroimaging is that experimenters may occasionally miss small muscle contractions or even quasi-movements that their volunteers make during tasks. Similar to Jeannerod and Decety (1995), we conceptualise M.I. as a form of cognitive motor rehearsal deprived from an explicit motor outflow. For us, the occasional presence of a green light to spinal motor neurons that manifests itself with occasional motor twitches does not detract from the quality of the mental process under investigation. In addition, the exploration of the neurofunctional activations recorded during M.I. and the direct comparison with the neural activity of the executed motor task reinforces our suggestion. As in previous experiments, we observed commonalities and differences to strongly suggest the following: (1) the likely motoric nature of M.I. given the activation of motor/premotor cortices; (2) the much larger implementation of actual motor acts during M.E. (see the highly significant larger activation of M1/S1 in the M.E. task); and (3) the more cognitive nature of the M.I. task overall, as revealed by the recruitment of higher order premotor and parietal cortices during imagery, particularly in the younger participants.

  6. Our interpretation of the quality of mental imagery in the elderly relies on the distinctive fMRI patterns of the older subjects. We consider these an explicit neural signature because of the topographical distribution in occipital cortices of well-known functional properties. In principle, one could have used introspective descriptions of the M.I. experience to document departures from kinaesthetic imagery to visual imagery and used these departures to decipher the fMRI patterns. However, one may argue that there is no guarantee that introspective descriptions about the accuracy or style of the imagery procedure would be accurate. More crucially, the combination of introspective online descriptions of the quality of the imagery experience during fMRI would have changed the nature of our experiment quite dramatically by turning it into a meta-cognitive protocol about M.I., something very interesting but different from our intended scope. On the other hand, the post hoc correlation of the introspective descriptions with the fMRI activity would have proved temporally inaccurate and possibly difficult to analyse statistically. On the contrary, in our experiment, the emphasis was on explicitly measurable variables, such as the chronometric measures during M.E. and M.I. outside the scanner or the fMRI signal collected during standardised procedures and the ensuing correlations between the two sets of variables.

  7. We cannot claim evidence for a double functional anatomical dissociation, as we did not find significantly greater activations in motor-related structures in the younger subjects. Indeed, while the elderly subjects had greater activations in the occipital cortices, they still relied, in part, on the activity of motor cortices during M.I.

  8. It is worth reemphasising that the elderly also showed activation of the premotor cortices during their M.I. task. Therefore, we suggest that the “visual” mental imagery testified by the occipital additional activation might be a complementary strategy, rather than a completely alternative one.

  9. A similar interpretation was given by Zwergal et al. (2012) in a fMRI study on M.I. during imagined locomotion.

Abbreviations

BOLD:

Blood oxygen level dependent

FWE:

Family-wise error

fMRI:

Functional magnetic resonance imaging

M.E.:

Motor execution

MEP:

Motor-evoked potentials

M.I.:

Motor imagery

MRI:

Magnetic resonance imaging

SD:

Standard deviation

SMA:

Supplementary motor area

TMS:

Transcranial magnetic stimulation

rTMS:

Repetitive transcranial magnetic stimulation

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Acknowledgments

We thank the staff of the Department of Diagnostic Radiology and Bioimages of IRCCS Galeazzi and the Department of Neuroradiology of Niguarda Hospital.

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Authors and Affiliations

  1. Department of Psychology, University of Milano-Bicocca, Piazza dell’Ateneo Nuovo, 20126, Milan, Italy

    L. Zapparoli, P. Invernizzi, M. Verardi, M. Berlingeri & E. Paulesu

  2. Neuroradiology Department, Niguarda Ca’ Granda Hospital, Milan, Italy

    M. Sberna

  3. IRCCS Galeazzi, Milan, Italy

    A. De Santis, A. Zerbi, G. Banfi & E. Paulesu

  4. University of Milano Statale, Milan, Italy

    A. De Santis & G. Banfi

  5. Department of Humanistic Studies, University of Pavia, Pavia, Italy

    M. Gandola & G. Bottini

  6. Cognitive Neuropsychology Center, Niguarda Ca’ Granda Hospital, Milan, Italy

    G. Bottini

Authors
  1. L. Zapparoli
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  2. P. Invernizzi
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  3. M. Gandola
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  4. M. Verardi
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  5. M. Berlingeri
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  6. M. Sberna
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  7. A. De Santis
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  8. A. Zerbi
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  9. G. Banfi
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  10. G. Bottini
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  11. E. Paulesu
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Corresponding author

Correspondence to E. Paulesu.

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L. Zapparoli and P. Invernizzi contributed equally to the authorship of this paper.

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Zapparoli, L., Invernizzi, P., Gandola, M. et al. Mental images across the adult lifespan: a behavioural and fMRI investigation of motor execution and motor imagery. Exp Brain Res 224, 519–540 (2013). https://doi.org/10.1007/s00221-012-3331-1

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  • DOI: https://doi.org/10.1007/s00221-012-3331-1

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