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Neuropsychologia 41 (2003) 401406

Motor cortex hand area and speech: implications for the development of language
Ingo Gerrit Meister a , Babak Boroojerdi a , Henrik Foltys a , Roland Sparing a , Walter Huber b , Rudolf Tpper a,
a

Department of Neurology, University Hospital RWTH Aachen, Pauwelsstrae 30, Aachen 52074, Germany b Department of Neurolinguistics, University Hospital RWTH Aachen, Aachen 52074, Germany Received 25 February 2002; received in revised form 2 September 2002; accepted 5 September 2002

Abstract Recently a growing body of evidence has suggested that a functional link exists between the hand motor area of the language dominant hemisphere and the regions subserving language processing. We examined the excitability of the hand motor area and the leg motor area during reading aloud and during non-verbal oral movements using transcranial magnetic stimulation (TMS). During reading aloud, but not before or afterwards, excitability was increased in the hand motor area of the dominant hemisphere. This reading effect was found to be independent of the duration of speech. No such effect could be found in the contralateral hemisphere. The excitability of the leg area of the motor cortex remained unchanged during reading aloud. The excitability during non-verbal oral movements was slightly increased in both hemispheres. Our results are consistent with previous ndings and may indicate a specic functional connection between the hand motor area and the cortical language network. 2002 Elsevier Science Ltd. All rights reserved.
Keywords: Hand motor cortex; Speech; Transcranial magnetic stimulation; Language development

1. Introduction Behavioral, neuropsychological and neurophysiological data suggest that there is some functional overlap in the neural networks that process language and movement [4,5,7,9,11,13]. The results of these studies may explain the observation that speech is often accompanied by gestures, which could have developed during the evolution of language. Neurobiological support for this hypothesis is given by Rizzolatti and Arbib [1,10], who argue that the activation of mirror neurons in the motor cortex when observing grasping movements is an evolutionary step in the development of language. On the basis of this hypothesis there may be phylogenetically old connections between the motor cortex and the language areas. Recent neurophysiological studies have found evidence for an impact of reading on the activity of motor cortical areas not involved in speech during reading. A study by Tokimura et al. used transcranial magnetis stimulation in right-handed subjects to assess the excitability of the hand
Corresponding author. Tel.: +49-241-8089630; fax: +49-241-8082444. E-mail address: rtoepper@ukaachen.de (R. Tpper).

area of the motor cortex at rest and during reading aloud, spontaneous speech and sound production without speech [13]. There was an enhancement of the excitability of the left motor hand area during reading aloud and of the motor hand areas of both hemispheres during spontaneous speech. Sound production without speech had no effect. A second study using the same technique found that the enhancement of activation of the left hand area of the motor cortex is not only present during reading aloud but also when reading is anticipated due to a prior warning stimulus [11]. The results of these two studies support the hypothesis that there is a functional connection between language-related cortical areas and the hand area of the motor cortex of the dominant hemisphere but several questions, however, remain open. For example, the authors of the rst study could not explain the bilateral enhancement of excitability during spontaneous speech. They speculate that spontaneous speech is more related to gesturing than reading and thus there may be an overow of activation to the contralateral hemisphere. A further question which has not been addressed by the previous studies is whether the effect of reading aloud is specic for the hand area of the motor cortex and whether it is present only during reading. If so, this would indicate a specic functional connection between cortical areas

0028-3932/02/$ see front matter 2002 Elsevier Science Ltd. All rights reserved. PII: S 0 0 2 8 - 3 9 3 2 ( 0 2 ) 0 0 1 7 9 - 3

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processing language and hand movements. The present study assessed the excitability of the hand area and the leg area of the motor cortex to investigate the topographic specicity of the effect of reading aloud on the motor cortex. In addition, time points before, during and after speech were tested to investigate the temporal specicity of this phenomenon. The task included reading of written words, which, unlike spontaneous speech, allowed the investigation of dened time points before, during and after articulation.

subjects (n = 5) were required to purse their lips repetitively without vocalization after having been presented a black circle on the screen (non-verbal oral movement condition). Overall, the following conditions were used: experimental: single wordsreading aloud, triple wordsreading aloud; baseline: non-letter stringspassive viewing; control: black circlesnonverbal oral movements. All conditions were tested in one trial, with 10 items each. The total of 40 items was presented in random order. All stimuli were presented on a 17 in. computer screen. 2.3. Transcranial magnetic stimulation Transcranial magnetic stimulation (TMS) was applied with a Magstim 200 stimulator (Magstim Co, UK) using a gure-of eight coil. The coil was placed on the scalp and the site of stimulation was adjusted in order to elicit motor evoked potentials (MEP) with maximum amplitude in the contralateral rst dorsal interosseus (FDI) muscle. MEP were obtained with surface electrodes placed over the FDI and the metacarpophalangeal joint (reference electrode) using Ag/AgCl electrodes. The output of the magnetic stimulator was adjusted to about 120% of the motor threshold at rest. The resting motor threshold was dened as the lowest stimulation intensity that evoked ve MEP with >50 V peak-to-peak amplitude in 10 trials in the relaxed FDI muscle. In four subjects, we also studied excitability changes of the leg motor area during reading aloud. In order to measure the excitability of the leg motor area, a circular TMS-coil was used, which was held over the vertex. The stimulus intensity was adjusted to obtain MEP amplitudes of 0.10.5 mV. The leg MEPs were obtained from the tibialis anterior muscle bilaterally. 2.4. Procedure Subjects sat in a reclining chair and were instructed to focus their attention on the computer screen on which the different types of stimuli were presented. In separate trials, TMS was administered at 0, 300, 600, 1200 or 2000 ms after onset of stimulus presentation for each hemisphere. Since on average onset of speech started 500 ms after stimulus onset and the average duration of reading was 400 ms for one word and 1000 ms for three words, the points of stimulation were therefore placed before, during and after reading aloud (Fig. 2). Each of the 10 trials consisted of 40 items randomly ordered across conditions. One magnetic stimulus was applied for each item. Thus, 10 MEP were obtained for each trial and condition. The peak-to-peak amplitudes were averaged, and mean MEP amplitudes obtained during experimental conditions were normalized to the mean MEP obtained during viewing non-letter strings (baseline condition). Thus,

2. Methods 2.1. Subjects Eleven healthy normal volunteers (all right-handed males) were included. The mean age was 26.3 years (range 2034 years). None of the subjects had a history of neurological disorders, including seizures. The protocol was approved by the local ethics committee and all subjects gave their informed consent. 2.2. Stimuli and tasks We used two sets of stimuli which the subjects had to read: single concrete nouns of high frequency consisting of one or two syllables (e.g. German Haus, Kragen; cf. English house, collar) and triples of semantically unrelated nouns with the same linguistic feature as the single words (e.g. German Tiger-Nebel-Tonne, cf. English tiger-fog-barrel). These sets were constructed so as to choose stimuli of different time spans for articulation in order to determine whether changes in motor cortex excitability depended on the duration of articulation and whether the changes persisted over the whole act of reading. As a baseline condition, meaningless gures consisting of non-letter strings were presented, matched to the letters in font size, but not resembling the letters in shape. These had to be viewed passively (non-letter string condition, see Fig. 1). For the two experimental conditions and the baseline condition, sets of 30 items were developed and divided into blocks of 10 items. One block per condition was randomly selected for each trial. In a control experiment, we wished to examine whether the effects on motor excitability were speech-dependent. The

Fig. 1. Example of non-letter strings that were presented as baseline condition.

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Fig. 2. Time course of the experiment. The arrow indicates the stimulus onset; along the scale the TMS time points are marked. The grey bar shows the average duration of speech for one word, the white bar the average duration of speech for reading three words.

relative amplitudes were calculated which indicated the change in cortical excitability in response to speech or non-speech movements compared to a baseline and allowed a direct comparison among different trials and subjects. 2.5. Statistical analysis The amplitudes of the baseline conditions of the two hemispheres were compared with the Mann-Whitney U-test. Relative amplitudes were created by dividing the amplitudes of the experimental conditions by the corresponding baseline amplitudes. The statistical analysis of the relative amplitudes was performed with the ANOVA-test as well as the Mann-Whitney U-Wilcoxon rank sum test using commercially available statistical software packages (SPSS and SuperANOVA). The mean relative amplitudes of the speech

conditions, the non-speech condition and the leg motor area condition were compared with the mean relative amplitudes of the corresponding baseline condition. This was done for each time condition and for the right and left hemisphere stimulation separately.

3. Results 3.1. Reading conditions The comparison of the mean MEP amplitudes following the presentation of the non-letter string condition revealed no signicant differences between the different time points of TMS. Thus, as expected, passive viewing of non-letter strings could be used as a baseline condition. Analysis of

Fig. 3. Mean MEP amplitudes of the reading conditions relative to the baseline (nonsense string letter condition) for stimulation of the left hemisphere. Black bars indicate conditions that are signicantly different from baseline. The bars below indicate the average time of speech for one word and three words.

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Fig. 4. Mean MEP amplitudes of the reading conditions relative to the baseline (nonsense string letter condition) for stimulation of the right hemisphere. The bars below indicate the average time of speech for one word and three words.

the mean relative amplitudes of left hemisphere stimulation with the Mann-Whitney U-Wilcoxon rank sum test yielded signicant increases in the normalized MEP amplitudes at 600 ms after stimulus onset for the one word condition (mean relative amplitude 1.48; P = 0.0069) and both 600 ms and 1200 ms in the three word condition (mean relative amplitudes 1.75 and 1.29; P < 0.0001 and 0.0005, respectively). Motor cortex excitability was therefore signicantly increased in the language dominant hemisphere while the subjects were reading aloud. No signicant changes were observed before and after reading (Fig. 3). In contrast to the results obtained from left hemisphere stimulation, MEP amplitudes following right motor cortex stimulation remained unchanged during reading of one or three words (Fig. 4). Thus, reading aloud had no inuence on the excitability of the hand area of the motor cortex of the non-dominant hemisphere. In the ANOVA an overall effect of stimulation time as well as of stimulus condition (P = 0.019, and P = 0.006, respectively) was found; there was no overall effect of stimulation site but a signicant interaction existed between stimulation time and stimulation site (P = 0.04). In the contrast analysis, there was a signicant effect of stimulation site for TMS at 600 ms after stimulus onset (P = 0.001) and a strong trend for 1200 ms after stimulus onset (P = 0.068). For the other time points no signicant effect was found. Taken together, the ANOVA-results indicate an increase in the excitability of the hand area of the left motor cortex compared to the right motor cortex during reading aloud.

3.2. Control conditions The analysis of the non-speech condition revealed an MEP amplitude increment which just reached statistical signicance during oral movements bilaterally (mean relative amplitudes 1.46 for left hemisphere stimulation and 1.20 for right hemisphere stimulation, P = 0.04). This bilateral effect was found for TMS at 600 ms only, i.e. while oral movement was going on. The analysis of the stimulation of the leg motor areas before, during and after reading one word yielded no signicant changes in MEP amplitudes, with the exception of the condition after speech for left hemisphere stimulation and reading one word, where we found a signicant decrease of the MEP amplitudes (P = 0.014). This, however, is most likely due to the small number of subjects investigated in this condition and will not be discussed further.

4. Discussion This study shows that during reading aloud the excitability of the primary motor hand area is increased in the language-dominant hemisphere. This effect is not present in the primary motor area of the leg and lasts while speech is ongoing, but does not occur before or after articulation. Our ndings are consistent with previous studies which reported enhancement in hand motor excitability during reading and spontaneous speech [11,13]. However, these studies did not look at the duration of the enhancement of motor cortex excitability and did not investigate cortical

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motor areas other than the hand area of the motor cortex. In the present study reading stimuli of different length were presented to determine whether the effects on the excitability of the hand motor area is present only at the onset of speech or persists during articulation. Twelve hundred milliseconds after stimulus onset, that is, 700 ms after average speech onset, there was a signicant enhancement of excitability only for the three word condition but not for the one word condition. This corresponds to the different durations of speech in the two conditions: at this time point reading of three words was still ongoing whereas reading of one word had nished. At 2000 ms after stimulus onset, when speech had nished in both conditions, there were no signicant excitability changes of the hand motor area. Thus, the effects seem to correspond to the duration of speech. Furthermore, we examined the excitability of the primary motor area of the leg during speech. There was a slight enhancement of excitability in the left hemisphere, which was not, however, signicantly different from baseline and was not specic for articulation. We therefore conclude that there is no language specic effect in the leg motor area comparable to that seen in the hand motor area. Thus, the excitability changes are likely to be specic for the hand motor cortex. There was an enhancement in MEP amplitudes during non-verbal oral movements following stimulation of either hemisphere. This effect may be due to an excitation of both motor cortices during non-speech movement. This is in accordance with imaging studies looking at the involvement of the primary motor cortex during nonsense articulation. These studies were unable to nd enhanced activity in the primary motor cortex of the language dominant hemisphere [8,14]. As language and speech emerge from a highly complex system, it is challenging to disentangle the underlying components responsible for the enhancement effect of hand motor cortex excitability. Speech movement results from coordinated activities of oral, laryngeal and pharyngeal muscles under the control of higher linguistic functions such as retrieval of words from the mental lexicon and phonological encoding of their sound structures. The classical posterior and anterior language areas are crucially involved. Programming of articulation appears to specically involve Brocas area and/or the adjacent anterior insula. In contrast, execution of articulation requires bilateral motor activity and therefore can be ruled out as a source of our enhancement effect. It is also unlikely that the enhancement in hand motor cortex excitability during reading is merely due to a coactivation within primary motor areas engaged in vocalization and/or articulation. If so, a bilateral rather than a unilateral left |hemisphere effect should be found. Furthermore, a recent TMS study [12] investigating the cortical motor preparation for vocalization found a robust right hemisphere predominance immediately preceding vocalization. Therefore, it is unlikely that the enhanced excitability seen in the present study is dependent on vocalization, but rather would seem to be due to coactivation of the dominant hand motor cortex with higher levels of the cortical language network.

An example for a close interaction of the hand motor cortex and language areas is writing. It may be speculated that the effect seen in this study is due to a close functional connection between reading and writing. A previous study [13], however, found that silent reading left the excitability of the hand motor cortex uninuenced. It is, therefore, unlikely that this readingwriting link is the only explanation for the functional connection between hand motor cortex and language. The present results can be integrated into theories of language development. It is currently a matter of controversy which role hand movements and gesture production may have played in the evolution of language and speech. Our study supports a theory that favors a strong evolutionary link between the cortical hand area and the development of language. This hypothesis [1,10] emerges from the existence of so-called mirror neurons that are active both during observation and execution of tasks such as grasping objects. These neurons are located in an area of the cortex of macaque monkeys that seems to correspond to Brocas area in the human cortex [3]. The proponents of this theory argue that such an observation/execution matching system can bridge the gap between action and communication about action and thus forms the neural basis of the development of language. According to this theory, there should be phylogenetically old links between motor hand and language areas, and these would be responsible for the effect we found. Several ndings emphasize the assumption of a functional coupling between speech and hand motor area of the language dominant hemisphere. One obvious link between these two regions is the fact that involuntary gestures are often performed during speech. Iverson and Goldin-Meadow [7] studied the behaviour of subjects born blind and found that they gestured during speech even when they knew their opposite was blind, as well. This indicates that gesturing is a behaviour integral to the speech process itself. There are also examples of a reversed activation of the language or speech system through gesturing. Neuropsychological results indicate that gestural movements can facilitate word retrieval in both normal subjects and in aphasic patients. Rauscher et al. [9] examined subjects who had to describe animated action cartoons and were allowed or not allowed to gesture while speaking. They found that restriction of gesturing increased the difculty of lexical access for speech with spatial content. Hanlon et al. [5] demonstrated that in aphasic patients the process of naming an object could be facilitated by their pointing with their dominant arm to a screen on which the object was presented. Arden and Huber (unpublished observation) found that this effect applies not only to semantic correctness, but also to the speed of naming, irrespective of the type of aphasia. Hadar et al. [4] examined gesturing in brain damaged patients and found that word retrieval could be facilitated through gesturing. Further support comes from recent functional imaging studies that dealt with the cortical representation of gestures. Hermsdrfer et al. [6] found activation of the premotor cortex during discrimination of hand gestures. Choi et al. [2]

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I.G. Meister et al. / Neuropsychologia 41 (2003) 401406 [3] Gallese V, Fadiga L, Fogassi L, Rizzolatti G. Action recognition in the premotor cortex. Brain 1996;119:593609. [4] Hadar U, Wenkert-Olenik D, Krauss R, Soroker N. Gesture and the processing of speech: neuropsychological evidence. Brain and Language 1998;62:10726. [5] Hanlon RE, Brown JW, Gerstman LJ. Enhancement of naming in nonuent aphasia through gesture. Brain and Language 1990;38:298 314. [6] Hermsdrfer J, Goldenberg G, Wachsmuth C, Conrad B, CeballosBaumann AO, Bartenstein P, et al. Cortical correlates of gesture processing: clues to the cerebral mechanisms underlying apraxia during the imitation of meaningless gestures. NeuroImage 2001;14:14961. [7] Iverson JM, Goldin-Meadow S. Why people gesture when they speak. Nature 1998;396:228. [8] Murphy K, Coreld DR, Guz A, Fink GR, Wise RJ, Harrison J, et al. Cerebral areas associated with motor control of speech in humans. Journal of Applied Physiology 1997;83:143847. [9] Rauscher FH, Krauss RM, Chen YS. Gesture, speech, and lexical access: the role of lexical movements in speech production. Psychological Science 1996;7:22631. [10] Rizzolatti G, Arbib MA. Language within our grasp. Trends in Neuroscience 1998;21:18894. [11] Seyal M, Mull B, Bhullar N, Ahmad T, Gage B. Anticipation and execution of a simple reading task enhance corticospinal excitability. Clinical Neurophysiology 1999;110:4249. [12] Terao Y, Ugawa Y, Enomoto H, Furubayashi T, Shiio Y, Machii K, et al. Hemispheric lateralization in the cortical motor preparation for human vocalization. Journal of Neuroscience 2001;21:16009. [13] Tokimura H, Tokimura Y, Oliviero A, Asakura T, Rothwell JC. Speech-induced changes in corticospinal excitability. Annals of Neurology 1996;40:62834. [14] Wise RJ, Greene J, Buchel C, Scott SK. Brain regions involved in articulation. Lancet 1999;353:105761.

observed additional activation of the left hemisphere parietal and premotor areas when performing gestures compared to nger movement irrespective of the hand that was used, indicating a strong lateralization to the dominant hemisphere when gesturing. In conclusion, our study shows that there is a lateralized enhancement of the excitability of the hand motor area of the language dominant hemisphere that is presumably due to a functional link between the hand area of the motor cortex and language areas. This supports the hypothesis that there are phylogenetically old connections between the two regions which evolved during the evolution of speech. Acknowledgements We thank S. Fellows for helpful remarks on the manuscript. This work was supported by a grant from IZKF and START program of the Medical Faculty, Aachen and by Deutsche Forschungsgemeinschaft (KFO 112/1). References
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