Abstract
There is a common saying for expressing familiarity with something. It refers to our hands, and strangely enough, in English, one says to know something like the back of the hand, whereas in other cultures, for example, Italy, Spain and France, the same expression is with the palm. Previous behavioural data have suggested that our ability to visually discriminate a right from a left hand is influenced by perspective. This behavioural finding has remained without neurophysiological counterparts. We used an implicit motor imagery task in which 30 right-handed subjects were asked to decide whether a picture portrayed a right rather than a left hand during an fMRI event-related experiment. Both views (back and palm) were used, and the hands were rotated by 45° in 8 possible angles. We replicated previous behavioural evidence by showing faster reaction times for the back-view and view-specific interaction effects with the angle of rotation: for the back view, the longest RTs were with the hand facing down at 180°; for the palm view, the longest RTs were at 90° with the hand pointing away from the midline. In addition, the RTs were particularly faster for back views of the right hand. fMRI measurements revealed a stronger BOLD signal increase in left premotor and parietal cortices for stimuli viewed from the palm, whereas back-view stimuli were associated with stronger occipital activations, suggesting a view-specific cognitive strategy: more visually oriented for the back of the hand; more in need of the support of a motoric imagery process for the palms. Right-hand back views were associated with comparatively smaller BOLD responses, attesting, together with the faster reaction times, to the lesser need for neural labour because of greater familiarity with that view of the hand. These differences suggest the existence of brain-encoded, view-dependent representations of body segments.
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Notes
As far as we were able to document, for the aforementioned idiomatic expression, reference to the back of the hand is made only in English-speaking countries. The palm is the view of choice in French, Greek, Hebrew, Korean, Italian, Portuguese, Rumanian, Spanish, and Turkish. Other cultures adopt different expressions: Finnish, German, and Norwegian favour the pockets (an alternate expression in Italian and Swedish as well); Albanians, Russians and the Swedish favour the tips of their fingers; in Chinese, one refers to the whole hand or foot; in Arabic, one refers to the whole self. Interestingly, Japanese doesn’t seem to have any equivalent idiomatic expression.
The preceding paragraphs are admittedly focused on what is considered an explicit form motor imagery, a mental process that we do not consider as fully equivalent of implicit motor imagery, as discussed in the following paragraphs.
The terminology used for the data of ter Horst et al. (2010), is that of the authors: they presented stimuli that cold be rotated in the coronal, longitudinal or antero-posterior direction (see their Fig. 1). The terminology can be best understood if one starts from the back-view of the hand pointing up: the first axis of rotation is within the coronal plane (6 possible angles around a transvers axis orthogobally crossing the centre of the carpus). Hands could also be rotated over the longitudinal axis, crossing the hand from the wrist to the top of the middle finger. Here, there were only two possible rotations, at 0° for the back-view and at 180°, for the palm-view. These manipulations of the stimuli were the same as in our paper. ter Horst et al (2010) also had a third potential axis of rotation to generate three different varieties of stimuli and manipulate the perspective of depth of the pointing direction of each given hand stimulus. This is generated by a rotation along a third axis that crosses the wrist in a transverse (from left to right) direction. In that experiment, the authors started with 12 stimuli in a canonical back-view, then they added stimuli rotated over the longitudinal axis to end-up with the whole set of 72 stimuli. They claimed that the greater the variety of rotations the greater the need for a mental imagery of a motoric nature.
The involvement of the primary motor cortex is definitely more contentious as shown by a recent ALE meta-analysis that investigated the neural networks of motor imagery in both explicit and implicit forms (Hétu et al. 2013).
The typical RT for this task is approximately 1 s, which suggests that events with a 400 ms window capture only part of the process that takes place during a HLT.
Given the resolution if ERPs, it is impossible to make firm functional interpretations of the meaning of signals sampled by a parietal electrode. For example, the same ERP signal may originate from very different regions. A parietal signal originating from the human homologue of area (Galletti et al. 1995) would point to a visuo-oculomotor source of an effect hardly differentiable from the integration processes needed for reaching behaviour; on the other hand, a signal captured by the same electrode but originating from the ventral portion of the intra-parietal region would point to a visuo-motor integration process for grasping objects.
The control fMRI experiment is very explicit in tackling motoric hand behaviours. We reasoned that a direct comparison with such data should be an even more direct strategy than any indirect reference to the literature on hand motor control.
Another possible way to indicate that the mental rotation of one stimulus is compatible with biomechanical constraints is to refer to the direction of its rotation, e.g. “clockwise/counter-clockwise” (see, for example, de Lange et al. 2006).
Accordingly, the contribution of the laterality of the motor response was controlled for in the analyses of the MI task at the second level as well.
The RTs measured in implicit motor imagery tasks are generally considered more objective measures than RTs for the introspective assessment of the completion of an explicit motor imagery task such as, for example, a finger-tapping task.
We therefore assume that if one physical constraint exists to determine the Italian, French or Spanish idioms, this must be justified by a familiarity with local features, such as palm lines, rather than with the whole hand shape or its spatial configuration.
The authors classified hand rotations according to the extent to which the resulting hand position was awkward rather than comfortable for someone imagining the position from his or her own perspective.
The use of the wording “motor planning” is not a casual one. After 20 years of fMRI studies, one may look at the involvement of the premotor cortices in tasks such as our own with little surprise. Yet, the demonstration of the activation of such cortices on tasks that in principle could be performed by using purely visual cues and strategies still remains one of the major empirical advances, with conceptual implications, in modern cognitive neuroscience in showing the important contribution of the visuo-motor integration processes that might occur automatically even for such tasks.
To us, the partial dissociations described here are also remarkable because, if anything, the adoption of an event-related design, with a complete randomization of the stimuli, may work against the possibility of finding a dissociation. The subjects, not knowing which kind of stimulus was occurring next, may have had all possible strategies active at the same time: yet, a view effect and a view-by-hand interaction effect were detectable in the fMRI data.
By definition, un-modulated and modulated analyses do not necessarily have to give overlapping results (see, for example, Kehoe et al. 2013). On the other hand, the characterisation of RT-independent and RT-dependent fMRI patterns makes the functional anatomical assessment more complete.
The lack of an advantage for the dominant hand in left-handers under natural conditions was also previously noted by Takeda et al. (Takeda et al. 2009).
There is evidence however, that the hemispheric lateralization of similar effects in motor imagery task is driven by the nature of the imagery task itself, the explicit motor imagery task having a less obvious pattern of hemispheric lateralization (see for example Kuhtz-Buschbeck et al. 2003; Sabaté et al. 2004; Michelon et al. 2006; Stinear et al. 2007; Malouin et al. 2012). Furthermore, the HLT may prove less “left-hemispheric” if compared with the more semantically oriented a grip selection task, as suggested by the data of Daprati et al. (2010). See below.
Abbreviations
- ALE:
-
Activation likelihood estimation
- BOLD:
-
Blood oxygen level dependent
- fMRI:
-
Functional magnetic resonance imaging
- FWE:
-
Family-wise error
- FDR:
-
False discovery rate
- HLT:
-
Hand laterality task
- ISI:
-
Inter-stimulus interval
- LHD:
-
Left-hemisphere damage
- RHD:
-
Right-hemisphere damage
- ME:
-
Motor execution
- MI:
-
Motor imagery
- MRI:
-
Magnetic resonance imaging
- RTs:
-
Reaction times
- SD:
-
Standard deviation
- SMA:
-
Supplementary motor area
- SVC:
-
Small-volume correction
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Acknowledgments
We are grateful to the staff of the Department of Diagnostic Radiology and Bioimages of IRCCS Galeazzi for their invaluable help. This paper was supported in part by a PRIN grant 2010 to E.P. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. No additional external funding was received for this study.
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Appendix
Appendix
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Zapparoli, L., Invernizzi, P., Gandola, M. et al. Like the back of the (right) hand? A new fMRI look on the hand laterality task. Exp Brain Res 232, 3873–3895 (2014). https://doi.org/10.1007/s00221-014-4065-z
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DOI: https://doi.org/10.1007/s00221-014-4065-z