Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-22T19:10:28.913Z Has data issue: false hasContentIssue false

Contribution of the basal ganglia to spoken language: Is speech production like the other motor skills?

Published online by Cambridge University Press:  17 December 2014

Alexandre Zenon
Affiliation:
Institute of Neuroscience, School of Medicine, Université catholique de Louvain, UCL, B-1200 Brussels, Belgium. [email protected]
Etienne Olivier
Affiliation:
Institute of Neuroscience, School of Medicine, Université catholique de Louvain, UCL, B-1200 Brussels, Belgium. [email protected] FondazioneIstituto Italiano di Tecnologia (IIT), 16163 Genova, Italy. [email protected]

Abstract

Two of the roles assigned to the basal ganglia in spoken language parallel very well their contribution to motor behaviour: (1) their role in sequence processing, resulting in syntax deficits, and (2) their role in movement “vigor,” leading to “hypokinetic dysarthria” or “hypophonia.” This is an additional example of how the motor system has served the emergence of high-level cognitive functions, such as language.

Type
Open Peer Commentary
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alcock, K. J., Passingham, R. E., Watkins, K. E. & Vargha-Khadem, F. (2000a) Oral dyspraxia in inherited speech and language impairment and acquired dysphasia. Brain and Language 75(1):1733. doi: 10.1006/brln.2000.2322.CrossRefGoogle ScholarPubMed
Andres, M., Olivier, E. & Badets, A. (2008) Actions, words, and numbers: A motor contribution to semantic processing? Current Directions in Psychological Science 17(5):313–17. doi: 10.1111/j.1467-8721.2008.00597.x.CrossRefGoogle Scholar
Berridge, K. C. (2004) Motivation concepts in behavioral neuroscience. Physiology and Behavior 81(2):179209. doi: 10.1016/j.physbeh.2004.02.004.CrossRefGoogle ScholarPubMed
Boyd, L. A., Edwards, J. D., Siengsukon, C. S., Vidoni, E. D., Wessel, B. D. & Linsdell, M. A. (2009) Motor sequence chunking is impaired by basal ganglia stroke. Neurobiology of Learning and Memory 92(1):3544. doi: 10.1016/j.nlm.2009.02.009.CrossRefGoogle ScholarPubMed
Chan, S.-H., Ryan, L. & Bever, T. G. (2013) Role of the striatum in language: Syntactic and conceptual sequencing. Brain and Language 125(3):283–94. doi: 10.1016/j.bandl.2011.11.005.CrossRefGoogle ScholarPubMed
Clerget, E., Andres, M. & Olivier, E. (2013) Deficit in complex sequence processing after a virtual lesion of left BA45. PLOS ONE 8(6):e63722. doi: 10.1371/journal.pone.0063722.CrossRefGoogle ScholarPubMed
Clerget, E., Badets, A., Duque, J. & Olivier, E. (2011) Role of Broca's area in motor sequence programming: A cTBS study. NeuroReport 22(18):965–69. doi: 10.1097/WNR.0b013e32834d87cd.Google ScholarPubMed
Clerget, E., Poncin, W., Fadiga, L. & Olivier, E. (2012) Role of Broca's area in implicit motor skill learning: Evidence from continuous theta-burst magnetic stimulation. Journal of Cognitive Neuroscience 24(1):8092. doi: 10.1162/jocn_a_00108.CrossRefGoogle ScholarPubMed
Clerget, E., Winderickx, A., Fadiga, L. & Olivier, E. (2009) Role of Broca's area in encoding sequential human actions: A virtual lesion study. NeuroReport 20(16):1496–99. doi: 10.1097/WNR.0b013e3283329be8.CrossRefGoogle ScholarPubMed
Dehaene, S. & Cohen, L. (2007) Cultural recycling of cortical maps. Neuron 56(2):384–98. doi: 10.1016/j.neuron.2007.10.004.CrossRefGoogle ScholarPubMed
Desmurget, M. & Turner, R. S. (2008) Testing basal ganglia motor functions through reversible inactivations in the posterior internal globus pallidus. Journal of Neurophysiology 99(3):1057–76. doi: 10.1152/jn.01010.2007.CrossRefGoogle ScholarPubMed
Desmurget, M. & Turner, R. S. (2010) Motor sequences and the basal ganglia: Kinematics, not habits. Journal of Neuroscience 30(22):7685–90. doi: 10.1523/JNEUROSCI.0163-10.2010.CrossRefGoogle Scholar
Fadiga, L., Craighero, L. & D'Ausilio, A. (2009) Broca's area in language, action, and music. Annals of the New York Academy of Sciences 1169(1):448–58. doi: 10.1111/j.1749-6632.2009.04582.x.CrossRefGoogle ScholarPubMed
Gopnik, M. (1990a) Feature-blind grammar and dysphasia. Nature 344(6268):715. doi: 10.1038/344715a0.CrossRefGoogle Scholar
Graybiel, A. M. (2008) Habits, rituals, and the evaluative brain. Annual Review of Neuroscience 31:359–87. doi: 10.1146/annurev.neuro.29.051605.112851.CrossRefGoogle ScholarPubMed
Kotz, S. A., Schwartze, M. & Schmidt-Kassow, M. (2009) Non-motor basal ganglia functions: A review and proposal for a model of sensory predictability in auditory language perception. Cortex 45(8):982–90. doi: 10.1016/j.cortex.2009.02.010.CrossRefGoogle Scholar
Kurniawan, I. T., Seymour, B., Talmi, D., Yoshida, W., Chater, N. & Dolan, R. J. (2010) Choosing to make an effort: The role of striatum in signaling physical effort of a chosen action. Journal of Neurophysiology 104(1):313–21. doi: 10.1152/jn.00027.2010.CrossRefGoogle ScholarPubMed
Mazzoni, P., Hristova, A. & Krakauer, J. W. (2007) Why don't we move faster? Parkinson's disease, movement vigor, and implicit motivation. The Journal of Neuroscience 27(27):7105–16. doi: 10.1523/JNEUROSCI.0264-07.2007.CrossRefGoogle ScholarPubMed
Mimura, M., Oeda, R. & Kawamura, M. (2006) Impaired decision-making in Parkinson's disease. Parkinsonism and Related Disorders 12(3):169–75. doi: 10.1016/j.parkreldis.2005.12.003.Google ScholarPubMed
Niv, Y., Joel, D. & Dayan, P. (2006) A normative perspective on motivation. Trends in Cognitive Sciences 10(8):375–81. doi: 10.1016/j.tics.2006.06.010.CrossRefGoogle ScholarPubMed
Obeso, J. A., Jahanshahi, M., Alvarez, L., Macias, R., Pedroso, I., Wilkinson, L., Pavon, N., Day, B., Pinto, S., Rodríguez-Oroz, M. C., Tejeiro, J., Artieda, J., Talelli, P., Swayne, O., Rodríguez, R., Bhatia, K., Rodriguez-Dias, M., Lopez, G., Guridi, J. & Rothwell, J. C. (2009) What can man do without basal ganglia motor output? The effect of combined unilateral subthalamotomy and pallidotomy in a patient with Parkinson's disease. Experimental Neurology 220(2):283–92. doi: 10.1016/j.expneurol.2009.08.030.CrossRefGoogle Scholar
Olivier, E., Davare, M., Andres, M. & Fadiga, L. (2007) Precision grasping in humans: From motor control to cognition. Current Opinion in Neurobiology 17(6):644–48. doi: 10.1016/j.conb.2008.01.008.CrossRefGoogle ScholarPubMed
Pell, M. D. & Monetta, L. (2008) How Parkinson's disease affects non-verbal communication and language processing. Language and Linguistics Compass 2(5):739–59. doi: 10.1111/j.1749-818X.2008.00074.x.CrossRefGoogle Scholar
Sakai, K., Kitaguchi, K. & Hikosaka, O. (2003) Chunking during human visuomotor sequence learning. Experimental Brain Research 152(2):229–42. doi: 10.1007/s00221-003-1548-8.CrossRefGoogle ScholarPubMed
Schmidt, L., Forgeot d'Arc, B., Lafargue, G., Galanaud, D., Czernecki, V., Grabli, D., Schübach, M., Hartmann, A., Lévy, R., Dubois, B. & Pessiglione, M. (2008) Disconnecting force from money: Effects of basal ganglia damage on incentive motivation. Brain: A Journal of Neurology 131 (Pt. 5): 1303–10. doi: 10.1093/brain/awn045.CrossRefGoogle ScholarPubMed
Smith, M. C., Smith, M. K. & Ellgring, H. (1996) Spontaneous and posed facial expression in Parkinson's disease. Journal of the International Neuropsychological Society 2(5):383–91.CrossRefGoogle ScholarPubMed
Takikawa, Y., Kawagoe, R., Itoh, H., Nakahara, H. & Hikosaka, O. (2002) Modulation of saccadic eye movements by predicted reward outcome. Experimental Brain Research 142(2):284–91. doi: 10.1007/s00221-001-0928-1.CrossRefGoogle ScholarPubMed
Tettamanti, M. & Weniger, D. (2006) Broca's area: A supramodal hierarchical processor? Cortex 42(4):491–94.Google ScholarPubMed
Tremblay, P.-L., Bedard, M.-A., Langlois, D., Blanchet, P. J., Lemay, M. & Parent, M. (2010) Movement chunking during sequence learning is a dopamine-dependant process: A study conducted in Parkinson's disease. Experimental Brain Research. 205(3):375–85. doi: 10.1007/s00221-010-2372-6.CrossRefGoogle ScholarPubMed
Tremblay, P.-L., Bedard, M.-A., Levesque, M., Chebli, M., Parent, M., Courtemanche, R. & Blanchet, P. J. (2009) Motor sequence learning in primate: Role of the D2 receptor in movement chunking during consolidation. Behavioural Brain Research 198(1):231–39. doi: 10.1016/j.bbr.2008.11.002.CrossRefGoogle ScholarPubMed
Turner, R. S. & Desmurget, M. (2010) Basal ganglia contributions to motor control: A vigorous tutor. Current Opinion in Neurobiology 20(6):704–16. doi: 10.1016/j.conb.2010.08.022.CrossRefGoogle ScholarPubMed
Ullman, M. T. (2006) Is Broca's area part of a basal ganglia thalamocortical circuit? Cortex 42(4):480–85. doi: 10.1016/S0010-9452(08)70382-4.CrossRefGoogle ScholarPubMed
Verwey, W. B. (1996) Buffer loading and chunking in sequential keypressing. Journal of Experimental Psychology: Human Perception and Performance 22(3):544–62.Google Scholar
Verwey, W. B. (2001) Concatenating familiar movement sequences: The versatile cognitive processor. Acta Psychologica 106:6995.CrossRefGoogle ScholarPubMed
Verwey, W. B. & Eikelboom, T. (2003) Evidence for lasting sequence segmentation in the discrete sequence-production task. Journal of Motor Behavior 35(2):171–81. doi: 10.1080/00222890309602131.CrossRefGoogle ScholarPubMed
Watkins, K. E., Dronkers, N. F. & Vargha-Khadem, F. (2002a) Behavioural analysis of an inherited speech and language disorder: Comparison with acquired aphasia. Brain: A Journal of Neurology 125 (Pt. 3): 452–64.CrossRefGoogle ScholarPubMed
Wymbs, N. F., Bassett, D. S., Mucha, P. J., Porter, M. A. & Grafton, S. T. (2012) Differential recruitment of the sensorimotor putamen and frontoparietal cortex during motor chunking in humans. Neuron 74(5):936–46. doi: 10.1016/j.neuron.2012.03.038.CrossRefGoogle ScholarPubMed