Published online before print December 2, 2002, doi: 10.1161/01.STR.0000044952.74952.F7
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(Stroke. 2003;34:3.)
© 2003 American Heart Association, Inc.
Letters to the Editor |
Why Nondominant Hand Movements Cause Bilateral Cortical Activation in Emission Imaging
Charleston, West Virginia
To the Editor:
The contribution of Kato et al1 contains important laterality related data. But the respected authors resort to undocumented and unwarranted assertions from the literature that one must address in order to arrive at a cogent interpretation of their data.
They used the 1963 article of Nyberg-Hensen and Rinvik2 to support the existence of 10% to 15% uncrossed pyramidal fibers in humans. This article, which is often used for this very purpose, states that "the only safe conclusion to be drawn from the available data is that there may probably be considerable variation with regard to the proportion of crossed and uncrossed corticospinal fibers in man," never offering or referring to such anatomical documentation in humans as asserted by Kato et al. On the other hand, the current techniques of cortical mapping with sufficient temporal resolution employing electroencephalography, magnetoencephalography, and transcranial magnetic stimulation (TMS) all have demonstrated sequential activation of the major followed by the minor hemisphere on moving the nondominant hand (see below). This temporal feature of bimanual coordination in humans translates into such daily life experiences as (1)) the double-click heard with snapping one’s fingers of both hands simultaneously (Derakhshan, unpublished data), (2) the melody lead of the right hand in piano playing3 (known to musicologists for 160 years), and (3) the precedence of the bowing hand to the fingering in violin playing, recently documented by Wiesendanger et al.4 This callosally mediated delay of 10 to 40 ms involving the nondominant hand requires an anatomical explanation not forthcoming from the (unmodified) doctrine of contralaterality of movement control in humans. It reflects the asymmetry occasioned by a 1-way callosal traffic (underpinning all executive functions), manifesting the activating role of the neuronal ensemble located in the major hemisphere over its counterpart in the minor.5,6 The same is reflected in laterality indexed nondominant weakness after callosal transection (natural or iatrogenic) or in ipsilateral paralysis seen in lesions affecting the major hemisphere,7 all due to a diaschisis on cessation of the activating influences mentioned earlier.8 This asymmetry, or laterality of movement control, is uniquely human, not seen in chimpanzees or other monkeys.9,10
Kato et al also refer to another report11 concerning an anatomic anomaly, ie, nondecussation of the pyramids in medulla oblongata, in the same vein of drawing unwarranted support for a conventional interpretation of their findings. The situation is indeed far more sophisticated and exciting than that depicted by the authors, as their data are in favor of the concept of directionality of the traffic from the major to the minor hemisphere in determining a subject’s neural (as opposed to ostensible) handedness.5–7
To recap: It is the major hemisphere that gears into action when any movement is willed, giving the contralateral dominant hand a head start equaling the interhemispheric transfer time (IHTT, measuring 10 to 40 ms). In the laboratory, the first acknowledgment of the precedence of the dominant over the nondominant limb came from Kristeva et al12 in 1979. Kristeva et al13 established the same in 1991 using magnetoencephalography, as did Chen et al14 in 1997, using TMS. Priori et al15 did the most elaborate study on both right- and left-handers, showing that the TMS-induced interruption of function lasted longer (by an amount equal to IHTT) on the nondominant side as the disrupting influence trailed along the callosum from the dominant to the nondominant side, arriving at the same conclusion as Chen et al, whose subjects were all right-handers. All those cited above have been silent as to the reason behind the finding, with occasional accusation of laziness on the part of the minor hemisphere by some16 or others who interpreted the result17 without any regard for the neurological syndromes adumbrated above and elsewhere.5–7
In this light, the right-handed patients and controls of Kato et al showed ipsilateral activation of the left hemisphere as they used their nondominant hand, as in numerous other studies they cited and many more18; none, however, were cognizant of the pathway that underpins the asymmetry of such findings, indexed as it is to the subject’s neural handedness: this pathway remains unchanged19 regardless of attempts to "convert" those wired for practicing according to a different mandate of nature (ie, right hemisphere controlling the left) than that of a majority who do things in a reverse manner, also according to their own natural mandate.
References
1. Kato H, Izumiama M, Koisumi H, Takahashi A, Itoyama Y. Near infrared spectroscopic topography as a tool to monitor motor reorganization after hemispheric stroke. Stroke. 2002; 33: 2032–2036.
2. Nyberg-Hansen R, Rinvik E. Some comments on the pyramidal tract with special reference to its individual variations in man. Acta Neurol Scand. 1963; 39: 1–30.[Medline] [Order article via Infotrieve]
3. Vernon LN. Synchronization of chords in artistic piano music. In: Seashore CE, ed. Studies in Psychology of Music, Vol 3. Iowa City, Iowa: University Press; 1936: 306–345.
4. Wiesendanger M, Baader A, Kazennikov O, Hanspeter N, Milani P. Bimanual coordination in violin playing. Oral presentation at the Music, Motor Control, and the Mind Symposium. Monte Verità, Ascona, Switzerland. May 15–18, 2002. Abstract.
5. Derakhshan I. Crossed nonaphasia in a dextral with left hemispheric lesions: handedness technically defined. Stroke. 2002; 33: 1749–1750. Letter.
6. Derakhshan I. Ipsilateral, but via the callosum: a technical definition of handedness. Arch Phys Med Rehabil.;. 2002; 83: 733–734.[Medline] [Order article via Infotrieve]
7. Derakhshan I. Ipsilateral cortical weakness: a key to the anatomy of handedness. Can J Neurol Sci. 2002; 69: 131. Abstract.
8. Gold L, Lauritzen M. Neuronal deactivation explains decreased cerebellar blood flow in response to focal cerebral ischemia or suppressed neocortical function. Proc Natl Acad Sci U S A. 2002; 99: 7699–7704.
9. Palmer AR. Chimpanzee right-handedness reconsidered: evaluating the evidence with funnel plots. Am J Phys Anthropol. 2002; 118: 191–199.[CrossRef][Medline] [Order article via Infotrieve]
10. Brinkman J, Kuypers HG. Cerebral control of contralateral and ipsilateral arm, hand and finger movements in the split-brain rhesus monkey. Brain. 1973; 96: 653–674.
11. Hosokawa S, Tsuji S, Uozumi T, Matsunaga K, Toda K, Ota S. Ipsilateral hemiplegia caused by right internal capsule and thalamic hemorrhage: demonstration of predominant ipsilateral innervation of motor and sensory systems by MRI, MEP, and SEP. Neurology. 1996; 46: 1146–1149.
12. Kristeva R, Deecke L, Keller R, Kornhuber HH. Cerebral potentials preceding unilateral and bilateral simultaneous finger movements. Electroencephalogr Clin Neurophysiol. 1979; 47: 229–238.[CrossRef][Medline] [Order article via Infotrieve]
13. Kristeva R, Cheyne D, Deecke L. Neuromagnetic fields accompanying unilateral and bilateral movements. Electroencephalogr Clin Neurophysiol. 1991; 81: 284–298.[CrossRef][Medline] [Order article via Infotrieve]
14. Chen R, Gerloff C, Hallett M, Cohen LG. Involvement of ipsilateral motor cortex in finger movements of different complexities. Ann Neurol. 1997; 41: 247–254.[CrossRef][Medline] [Order article via Infotrieve]
15. Priori A, Olivieri A, Donati E, Callea L, Bertolasi L, Rothwell JC. Human handedness and asymmetry of the motor cortical silent period. Exp Brain Res. 1999; 128: 390–396.[CrossRef][Medline] [Order article via Infotrieve]
16. Baldessari F, Cavallari P. Impairment in the control of coupled cycled movements of ipsilateral hand and foot after total callosotomy. Acta Psychol. 2002; 110: 289–304.[CrossRef][Medline] [Order article via Infotrieve]
17. Ziemann U, Ishii K, Borgheresi A, Yaseen Z, Battaglia F, Hallett M, Cincotta M, Wasserman EM. Dissociation of pathways mediating ipsilateral and contralateral motor-evoked potentials in human hand and arm muscles. J Physiol. 1999; 518: 895–906.
18. Nirkko AC, Ozdoba C, Redmond SM, Burki M, Schroth G, Hess CW, Wiesendanger M. Different ipsilateral representation for distal and proximal movements in the sensorimotor cortex: activation and deactivation patterns. Neuroimage. 2001; 13: 825–835.[Medline] [Order article via Infotrieve]
19. Siebner HR, Limmer C, Peinemann A, Drzezga A, Bloem BR, Schwaiger M, Conrad B. Long term consequences of switching handedness: a positron emission tomography study on handwriting in converted left handers. J Neurosci. 2002; 22: 2816–2825.
Department of Neurology, Tohoku University Graduate School of Medicine, Sendai, Japan
Department of Neurology, Nakae Hospital, Sendai, Japan
Department of Neuroendovascular Therapy, Tohoku University Graduate School of Medicine, Sendai, Japan
Advanced Research Laboratory, Hitachi Ltd, Saitama, Japan
Response
We thank Dr Derakhshan for his interest in our article.1 We read his letter with great interest. We certainly agree that there is a hemispheric dominance of movement control in humans, and that this dominance may contribute to motor functional recovery after stroke. This hemispheric asymmetry can be observed not only during bimanual skilled movements outlined by Dr Derakhshan but also during simple unilateral hand movements. In normal right-handed subjects, simple left-hand movements elicit not only activation of the right (contralateral) primary sensorimotor cortex but also significant activation of the left (ipsilateral) primary motor area, whereas right-hand movements result in activation of only the left (contralateral) primary sensorimotor cortex.2,3 This asymmetry was not always evident in our control subjects, possibly because of individual variations or the threshold chosen for the statistical analysis. Thus, the primary motor cortex may play a role in ipsilateral hand movements, with the left hemisphere playing a greater role than the right. This functional asymmetry might lead to a greater chance for left hemiparesis to recover better than right hemiparesis. Therefore, we thought that it was more than by chance that the 6 patients selected in our study, who recovered excellently from massive infarction of the MCA territory, were all left-hemiparetic.
On the other hand, the extent of recovery from poststroke hemiparesis is highly variable, whether hemiparesis is right or left. There may be a number of reasons for the difference—not only the location and the size of the lesion, but also the individual variations in anatomic and functional connections. In this context, the individual variations of the proportion of crossed and uncrossed corticospinal tract fibers could partly account for the difference in functional recovery. As Dr Derakhshan quoted from Nyberg-Hansen and Rinvik,4 "there may probably be considerable variations with regard to the proportion of crossed and uncrossed corticospinal fibers in man." And in addition, the authors mentioned the general norms in the same article: "75 per cent of all pyramidal fibers are usually said to course in the crossed lateral corticospinal tract, 10 per cent in the lateral uncrossed tract and the remainder in a ventral uncrossed tract."4
The pattern of cortical activation during paretic hand movements is very different from that induced during normal hand movements. Long-term functional recovery therefore may involve extensive reorganization of motor network within the brain, in addition to the recovery from acute reversible dysfunctions. When brain damage to the motor system is partial, recovery may be possible using the existing functional system or recruiting the adjacent cortical areas. However, when a motor system, such as the primary motor area, is destroyed, as in our cases, functionally related systems—such as the bilateral primary sensorimotor, premotor, and supplementary motor areas—need to substitute the function as an alternative if recovery occurs. Functional imaging studies have suggested that reorganization involving all of these areas may occur.1,5-7 In addition, learning (rehabilitation) may induce the formation of new synaptic connections.
Thus, there may be considerable options in producing the best recovery from stroke, although detailed mechanisms of recovery still remain to be elucidated. We have great interest in the ability of the adult human brain to adapt not only to environmental changes but also to lesion-induced reorganization throughout life. It is important to understand the mechanism of brain plasticity and possible ways to modulate it.
References
1. Kato H, Izumiyama M, Koizumi H, Takahashi A, Itoyama Y. Near-infrared spectroscopic topography as a tool to monitor reorganization after hemiparetic stroke: a comparison with functional MRI. Stroke. 2002; 33: 2032–2036.
2. Kim S-G, Asche J, Hendrich K, Ellerman JH, Merkle H, Ugurbil K, Georgopoulos AP. Functional magnetic resonance imaging of motor cortex: hemispheric asymmetry and handedness. Science. 1993; 261: 615–617.
3. Kawashima R, Yamada K, Kinomura S, Yamaguchi T, Matsui H, Yoshioka S, Fukuda H. Regional cerebral blood flow changes of cortical motor areas and prefrontal areas in humans related to ipsilateral and contralateral hand movement. Brain Res. 1993; 623: 33–40.[CrossRef][Medline] [Order article via Infotrieve]
4. Nyberg-Hansen R, Rinvik E. Some comments on the pyramidal tract, with special reference to its individual variations in man. Acta Neurol Scand. 1963; 39: 1–10.[Medline] [Order article via Infotrieve]
5. Weiller C, Chollet F, Friston KJ, Wise RJS, Frackoawick RSJ. Functional reorganization of the brain in recovery from striatocapsular infarction in man. Ann Neurol. 1992; 315: 463–472.
6. Cramer SC, Nelles G, Benson RR, Kaplan JD, Parker RA, Kwong KK, Kennedy DN, Finklestein SP, Rosen BR. A functional MRI study of subjects recovered from hemiparetic stroke. Stroke. 1997; 28: 2518–2527.
7. Cao Y, C’Olhaberriague L, Vikingstad EM, Levine SR, Welch KMA. Pilot study of functional MRI to assess cerebral activation of motor function after poststroke hemiparesis. Stroke. 1998; 29: 112–122.
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