r Human Brain Mapping 5:206–215(1997) r Motor Cortex and Hand Motor Skills: Structural Compliance in the Human Brain Katrin Amunts,1* Gottfried Schlaug,2* Lutz Ja¨ncke,3 Helmuth Steinmetz,4 Axel Schleicher,1 Andreas Dabringhaus,1 and Karl Zilles1 1C. & O. Vogt Brain Research Institute, Heinrich Heine University, Du¨sseldorf, Germany 2Department of Neurology, Beth Israel Hospital and Harvard Medical School, Boston, Massachusetts 3Institute of Medicine, Research Center Ju¨lich, Ju¨lich, Germany 4Department of Neurology, Heinrich Heine University, Du¨sseldorf, Germany r r Abstract: Recent studies in humans and nonhuman primates have shown that the functional organization of the human sensorimotor cortex changes following sensory stimulation or following the acquisition of motor skills. It is unknown whether functional plasticity in response to the acquisition of new motor skills and the continued performance of complicated bimanual movements for years is associated with structural changes in the organization of the motor cortex. Professional musicians, especially keyboard and string players, are a prototypical group for investigating these changes in the human brain. Using magnetic resonance images, we measured the length of the posterior wall of the precentral gyrus bordering the central sulcus (intrasulcal length of the precentral gyrus, ILPG) in horizontal sections through both hemispheres of right-handed keyboard players and of an age- and handedness-matched control group. Lacking a direct in vivo measurement of the primary motor cortex in humans, we assumed that the ILPG is a measure of the size of the primary motor cortex. Left-right asymmetry in the ILPG was analyzed and compared between both groups. Whereas controls exhibited a pronounced left-larger-than-right asymme- try, keyboard players had more symmetrical ILPG. The most pronounced differences in ILPG between keyboard players and controls were seen in the most dorsal part of the presumed cortical hand representation of both hemispheres. This was especially true in the nondominant right hemispheres. The size of the ILPG was negatively correlated with age of commencement of musical training in keyboard players, supporting our hypothesis that the human motor cortex can exhibit functionally induced and long-lasting structural adaptations. Hum. Brain Mapping 5:206–215, 1997. r 1997 Wiley-Liss, Inc. Key words: human motor cortex; asymmetry; plasticity; handedness; MRI; musicians; hand motor skill r r INTRODUCTION Electrophysiological and neuroimaging studies in Contract Grant sponsor: Deutsche Forschungsgemeinschaft; Con- humans revealed adaptive changes in the cortical tract Grant number: SFB 199, A6. motor hand representations in response to learning *Correspondence to: Katrin Amunts, C. & O. Vogt Brain Research and the acquirement of new motor skills [Jenkins et al., Institute, Heinrich Heine University, Du¨ sseldorf, Germany. E-mail: [email protected] or Gottfried Schlaug, Dept. of Neu- 1994; Pascual-Leone et al., 1993, 1995a,b; Schlaug et al., rology, Beth Israel Deaconess Medical Center, 330 Brookline Avenue, 1994; Karni et al., 1995]. Similar functional changes Boston, MA 02215, USA. E-mail: [email protected] have been reported after stimulation of primary so- Received for publication 22 January 1997; accepted 10 April 1997 matosensory and motor areas in nonhuman primates r 1997 Wiley-Liss, Inc. r Motor Cortex and Hand Motor Skills r and cats [Merzenich et al., 1988; Recanzone et al., 1990; Encouraged by our previous findings and by the Jacobs and Donoghue, 1991; Nudo et al., 1992; Wang et results of Elbert et al. [1995] and Schlaug et al. [1995b], al., 1995]. Pascual-Leone et al. [1995a] showed that we wanted to investigate whether the early commence- over the course of 5 days, as subjects learned a ment and long duration of motor learning and practice five-finger exercise on the piano, the cortical motor of complex bimanual finger movements in musicians areas targeting the long finger flexor and extensor might lead to persistent, macrostructural adaptations muscles enlarged. Others suggested that the early within the motor cortex, which may underlie the acquirement of fine sensorimotor skills leads to lasting representational plasticity observed in persons while functional changes, such as having a larger sensory acquiring and continuously performing fine motor finger representation in string players [Elbert et al., skills [Pascual-Leone et al., 1993, 1995a,b; Schlaug et 1995]. The underlying neurophysiological changes are al., 1994]. still a matter of intense research. Possible modifica- There is also previous evidence that the primary tions could include a strengthening of existing syn- motor cortex might show a structural correlate of apses, the formation of new synapses, or recruitment handedness. Several groups [White et al., 1994; Foundas of cortical tissue into the activated cortex that was et al., 1995; Amunts et al., 1996] have shown that previously not recruited [Donoghue and Sanes, 1988; estimates of the primary motor cortex revealed a Merzenich et al., 1988; Recanzone et al., 1990; Jacobs left-larger-than-right motor cortex size in right-handed and Donoghue, 1991; Nudo et al., 1992; Pascual-Leone subjects. While right-handers showed a left-larger-than- et al., 1993, 1995a,b; Karni et al., 1995; Jones et al., 1996; right motor cortex size (as indexed by the ILPG), Kleim et al., 1996]. left-handers showed a right-larger-than-left ILPG In a previous study, we found evidence for struc- [Amunts et al., 1996]. These interhemispheric asymme- tural adaptations in the interhemispheric connectivity tries were thought to represent structural correlates of of frontal motor-related regions between musicians handedness. A similar suggestion was made on the with a different commencement of musical training. basis of results from a postmortem study on human The anterior corpus callosum was larger in musicians brains with unknown handedness [White et al., 1994]. with an early commencement of musical training In roughly 2/3 of these brains, the left central sulcus (before age 7) compared to musicians starting later was deeper than the right. In this regard, it is also (after age 7) and right-handed controls [Schlaug et al., important that several studies have found evidence 1995a]. Since this structural difference was seen in that handedness and distal hand motor skills are much musicians with an early commencement of musical more symmetrical in professional musicians [Christ- training, it was argued that this might represent a man, 1993; Schlaug et al., 1995a; Waldron and Anton, structural cerebral adaptation (e.g., thicker myelinated 1995]. transcallosal fibers or a greater amount of transcallosal On the basis of all these findings we hypothesized fibers) which have been triggered by a requirement for that the size of cortical motor areas could differ performing and continuously practicing complicated between musicians with a history of intense bimanual bimanual finger movements. These results indicated hand skill training and appropriate nonmusician con- that the corpus callosum underwent an adaptation in trols. In this study, we attempted to answer the the young brain which seemed to coincide with the following questions: 1) Do keyboard players exhibit a late myelination of the corpus callosum [Yakovlev and more symmetrical cortical motor hand representation Lecours, 1967]. Since late-beginning musicians (some area as indexed by the ILPG than right-handed con- of the musicians in this study were quite accomplished trols? 2) If musicians indeed differ from controls, are performers) did not show this anatomical difference these differences correlated with the age of commence- and as a matter of fact did not differ significantly from ment of musical and motor training? a right-handed nonmusician control group, a selec- tional hypothesis (e.g., a larger anterior corpus callo- MATERIALS AND METHODS sum would endow a child to become skilled at playing a musical instrument at a young age) was deemed to Subjects be less likely to explain these anatomical differences. A selectional hypothesis would explain the structural The study was performed on male, right-handed differences in the brains of musicians compared with professional musicians. They were recruited from three controls as an effect of a selection of people with, for music conservatories as well as through personal example, larger corpora callosa inherent in the de- contacts. All of them were actively performing, classi- mands of musical training and competition. cally trained musicians who had either finished their r 207 r r Amunts et al. r education or were still students at a music school. No white matter, but excluding voxels that would corre- amateur musicians were included. All musicians were spond to cerebrospinal fluid. keyboard players, with 9 of them playing string instru- The MR volumes were spatially oriented and normal- ments in addition. These professional male musicians ized in the computerized Human Brain Atlas, whereby (n 5 21; mean age 5 26.9 years, SD 5 4.6) were com- only linear transformations were applied (for details pared to an age- and handedness-matched male con- concerning the Human Brain Atlas, see Roland and trol group (n 5 30; mean age 5 26.4 years, SD 5 3.9). Zilles [1994]). Normalization was performed in order The control subjects in this study were either nonmusi- to exclude the influence of intersubject variability in cians who had never played a musical instrument or absolute brain size when determining intrasulcal controls who had played an instrument for less than 1 lengths. All brains were spatially oriented according to year after age 10 (the latter group comprised about 1/3 the coordinate system of Talairach and Tournoux of our subjects). We will refer to this group as the [1988], which enabled us to perform the analyses on nonmusician control group. The control group did not horizontal sections which were parallel to the plane include professional typists, although some used type- determined by the anterior and posterior commissures writers and computer keyboards for personal commu- (AC-PC plane).