Speech production is one of the most complex and rapid motor behaviors, and it involves a precise coordination of more than 100 laryngeal, orofacial, and respiratory muscles. Yet we lack a complete understanding of laryngeal motor cortical control during production of speech and other voluntary laryngeal behaviors. In recent years, a number of studies have confirmed the laryngeal motor cortical representation in humans and have provided some information about its interactions with other cortical and subcortical regions that are principally involved in vocal motor control of speech production. In this review, the authors discuss the organization of the peripheral and central laryngeal control based on neuroimaging and electrical stimulation studies in humans and neuroanatomical tracing studies in nonhuman primates. It is hypothesized that the location of the laryngeal motor cortex in the primary motor cortex and its direct connections with the brain stem laryngeal motoneurons in humans, as opposed to its location in the premotor cortex with only indirect connections to the laryngeal motoneurons in nonhuman primates, may represent one of the major evolutionary developments in humans toward the ability to speak and vocalize voluntarily.
Alario FX, Chainay H., Lehericy S., Cohen L.2006. The role of the supplementary motor area (SMA) in word production. Brain Res1076:129-43.
2.
Bauer G., Gerstenbrand F., Hengl W.1980. Involuntary motor phenomena in the locked-in syndrome . J Neurol223:191-8.
3.
Bernard JF, Villanueva L., Carroue J., Le Bars D.1990. Efferent projections from the subnucleus reticularis dorsalis (SRD): a Phaseolus vulgaris leucoagglutinin study in the rat. Neurosci Lett116:257-62.
4.
Bohland JW, Guenther FH2006. An fMRI investigation of syllable sequence production . Neuroimage32:821-41.
5.
Brown S., Laird AR, Pfordresher PQ, Thelen SM, Turkeltaub P., Liotti M.2009. The somatotopy of speech: phonation and articulation in the human motor cortex. Brain Cogn70: 31-41.
6.
Brown S., Ngan E., Liotti M.2008. A larynx area in the human motor cortex. Cereb Cortex18:837-45.
7.
Coude G., Ferrari P., Roda F., Maranesi M., Rozzi S., Fogassi L.2009. Ventral premotor cortex of the macaque monkey controls conditioned vocalization. Presented at the Society for Neuroscience , Chicago (IL).
8.
de Zubicaray GI, McMahon KL2009. Auditory context effects in picture naming investigated with event-related fMRI. Cogn Affect Behav Neurosci9:260-9.
9.
Dujardin E., Jurgens U.2005. Afferents of vocalization-controlling periaqueductal regions in the squirrel monkey. Brain Res1034: 114-31.
10.
Fadiga L., Fogassi L., Gallese V., Rizzolatti G.2000. Visuomotor neurons: ambiguity of the dicharge or `motor’ perception? Int J Psychophysiol35(2-3):165-77.
11.
Farley GR1997. Neural firing in ventrolateral thalamic nucleus during conditioned vocal behavior in cats. Exp Brain Res115:493-506.
12.
Fiebach CJ, Friederici AD, Smith EE, Swinney D.2007. Lateral inferotemporal cortex maintains conceptual-semantic representations in verbal working memory. J Cogn Neurosci19: 2035-49.
13.
Foester O.1936. Motorische Felder und Bahnen. Berlin : Springer.
14.
Galgano J., Froud K.2008. Evidence of the voice-related cortical potential: an electroencephalographic study. Neuroimage41:1313-23.
15.
Ghosh SS, Tourville JA, Guenther FH2008. A neuroimaging study of premotor lateralization and cerebellar involvement in the production of phonemes and syllables. J Speech Lang Hear Res51:1183-202.
16.
Greenlee JD, Oya H., Kawasaki H., Volkov IO, Kaufman OP, Kovach C., and others.2004. A functional connection between inferior frontal gyrus and orofacial motor cortex in human. J Neurophysiol92:1153-64.
17.
Guenther FH2006. Cortical interactions underlying the production of speech sounds. J Commun Disord39:350-65.
18.
Hage SR, Jurgens U.2006. On the role of the pontine brainstem in vocal pattern generation: a telemetric single-unit recording study in the squirrel monkey . J Neurosci26:7105-15.
19.
Hannig S., Jurgens U.2006. Projections of the ventrolateral pontine vocalization area in the squirrel monkey. Exp Brain Res169:92-105.
20.
Hast MH, Fischer JM, Wetzel AB, Thompson VE1974. Cortical motor representation of the laryngeal muscles in Macaca mulatta. Brain Res73:229-40.
21.
Hirano M.1981. Clinical examination of voice. Springer-Verlag in Wien, New York.
22.
Hocking J., McMahon KL, de Zubicaray GI2009. Semantic context and visual feature effects in object naming: an fMRI study using arterial spin labeling. J Cogn Neurosci21:1571-83.
23.
Horwitz B., Amunts K., Bhattacharyya R., Patkin D., Jeffries K., Zilles K., and others.2003. Activation of Broca’s area during the production of spoken and signed language: a combined cytoarchitectonic mapping and PET analysis. Neuropsychologia41:1868-76.
24.
Iwatsubo T., Kuzuhara S., Kanemitsu A., Shimada H., Toyokura Y.1990. Corticofugal projections to the motor nuclei of the brainstem and spinal cord in humans. Neurology40: 309-12.
25.
Jurgens U.1974. On the elicitability of vocalization from the cortical larynx area. Brain Res81:564-66.
26.
Jurgens U.1976. Projections from the cortical larynx area in the squirrel monkey. Exp Brain Res25:401-11.
Jurgens U., Ehrenreich L.2007. The descending motorcortical pathway to the laryngeal motoneurons in the squirrel monkey. Brain Res1148:90-5.
29.
Kelly RM, Strick PL2000. Rabies as a transneuronal tracer of circuits in the central nervous system. J Neurosci Methods103:63-71.
30.
Khedr EM, Aref EE2002. Electrophysiological study of vocal-fold mobility disorders using a magnetic stimulator. Eur J Neurol9:259-67.
31.
Kirzinger A., Jurgens U.1991. Vocalization-correlated single-unit activity in the brain stem of the squirrel monkey. Exp Brain Res84:545-60.
32.
Kunzle H.1975. Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia: an autoradiographic study in Macaca fascicularis. Brain Res88:195-209.
33.
Kuypers HG1958. Corticobular connexions to the pons and lower brain-stem in man: an anatomical study. Brain81: 364-88.
34.
Loucks TM, Poletto CJ, Simonyan K., Reynolds CL, Ludlow CL2007. Human brain activation during phonation and exhalation: common volitional control for two upper airway functions. Neuroimage36:131-43.
35.
Luria AR1964. Factors and forms of aphasia. In: de Reuck AVS, O’Connor M, editors. Disorders of language. London: Churchill. p 143-67.
36.
Luthe L., Hausler U., Jurgens U.2000. Neuronal activity in the medulla oblongata during vocalization: a single-unit recording study in the squirrel monkey. Behav Brain Res116: 197-210.
37.
Matsuzaka Y., Aizawa H., Tanji J.1992. A motor area rostral to the supplementary motor area (presupplementary motor area) in the monkey: neuronal activity during a learned motor task. J Neurophysiol68:653-62.
38.
McClean MD, Dostrovsky JO, Lee L., Tasker RR1990. Somatosensory neurons in human thalamus respond to speech-induced orofacial movements. Brain Res513:343-7.
39.
Milojevic B., Hast MH1964. Cortical motor centers of the laryngeal muscles in the cat and dog. Ann Otol Rhinol Laryngol73:979-88.
40.
Monnier M., Willi H.1953. [The integrative activity of the nervous system of a meso-rhombencephalic anencephalus. II. Anatomical part]. Monatsschr Psychiatr Neurol126:259-73.
41.
Olthoff A., Baudewig J., Kruse E., Dechent P.2008. Cortical sensorimotor control in vocalization: a functional magnetic resonance imaging study. Laryngoscope118:2091-6.
42.
Ozdemir E., Norton A., Schlaug G.2006. Shared and distinct neural correlates of singing and speaking . Neuroimage33:628-35.
43.
Papoutsi M., de Zwart JA, Jansma JM, Pickering MJ, Bednar JA, Horwitz B.2009. From phonemes to articulatory codes: an fMRI study of the role of Broca’s area in speech production. Cereb Cortex19:2156-65.
44.
Peeva MG, Guenther FH, Tourville JA, Nieto-Castanon A., Anton JL, Nazarian B., and others.Distinct representations of phonemes, syllables, and supra-syllabic sequences in the speech production network. Neuroimage50:626-38.
45.
Penfield W., Bordley E.1937. Somatic motor and sensory representation in the cortex as studied by electrical stimulation. Brain60:389-443.
46.
Penfield W., Roberts L.1959. Speech and brain mechanisms. Princeton (NJ): Princeton University Press.
47.
Penfield W., Welch K.1951. The supplementary motor area of the cerebral cortex: a clinical and experimental study. AMA Arch Neurol Psychiatry66:289-317.
48.
Peschke C., Ziegler W., Kappes J., Baumgaertner A.2009. Auditory-motor integration during fast repetition: the neuronal correlates of shadowing. Neuroimage47:392-402.
49.
Price JL1996. Vocalization and the orbital and medial prefrontal cortex . In: Davis PJ, Fletcher NH, editors. Vocal fold physiology: controlling complexity and chaos. San Diego (CA): Singular Publishing Group. p 171-85.
50.
Ramsay SC, Adams L., Murphy K., Corfield DR, Grootoonk S., Bailey DL, and others.1993. Regional cerebral blood flow during volitional expiration in man: a comparison with volitional inspiration. J Physiol461:85-101.
51.
Riecker A., Ackermann H., Wildgruber D., Dogil G., Grodd W.2000. Opposite hemispheric lateralization effects during speaking and singing at motor cortex, insula and cerebellum. Neuroreport11:1997-2000.
52.
Riecker A., Brendel B., Ziegler W., Erb M., Ackermann H.2008. The influence of syllable onset complexity and syllable frequency on speech motor control. Brain Lang107: 102-13.
53.
Rodel RM, Olthoff A., Tergau F., Simonyan K., Kraemer D., Markus H., and others.2004. Human cortical motor representation of the larynx as assessed by transcranial magnetic stimulation (TMS). Laryngoscope114:918-22.
54.
Scheiner E., Hammerschmidt K., Jurgens U., Zwirner P.2004. The influence of hearing impairment on preverbal emotional vocalizations of infants. Folia Phoniatr Logop56:27-40.
55.
Shiba K., Umezaki T., Zheng Y., Miller AD1997. The nucleus retroambigualis controls laryngeal muscle activity during vocalization in the cat. Exp Brain Res115:513-9.
56.
Shima K., Tanji J.1998. Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements. J Neurophysiol80:3247-60.
57.
Simonyan K., Jurgens U.2002. Cortico-cortical projections of the motorcortical larynx area in the rhesus monkey. Brain Res949:23-31.
58.
Simonyan K., Jurgens U.2003. Efferent subcortical projections of the laryngeal motorcortex in the rhesus monkey. Brain Res974:43-59.
59.
Simonyan K., Jurgens U.2005a. Afferent cortical connections of the motor cortical larynx area in the rhesus monkey. Neuroscience130:133-49.
60.
Simonyan K., Jurgens U.2005b. Afferent subcortical connections into the motor cortical larynx area in the rhesus monkey. Neuroscience130:119-31.
61.
Simonyan K., Ostuni J., Ludlow CL, Horwitz B.2009. Functional but not structural networks of the human laryngeal motor cortex show left hemispheric lateralization during syllable but not breathing production. J Neurosci29:14912-23.
62.
Simonyan K., Saad ZS, Loucks TM, Poletto CJ, Ludlow CL2007. Functional neuroanatomy of human voluntary cough and sniff production. Neuroimage37:401-9.
63.
Tanji J., Shima K.1996. Supplementary motor cortex in organization of movement . Eur Neurol36 Suppl 1:13-9.
64.
Terumitsu M., Fujii Y., Suzuki K., Kwee IL, Nakada T.2006. Human primary motor cortex shows hemispheric specialization for speech. Neuroreport17:1091-5.
65.
Tettamanti M., Rotondi I., Perani D., Scotti G., Fazio F., Cappa SF, and others.2009. Syntax without language: neurobiological evidence for cross-domain syntactic computations. Cortex45:825-38.
66.
Thoms G., Jurgens U.1987. Common input of the cranial motor nuclei involved in phonation in squirrel monkey. Exp Neurol95:85-99.
67.
Tyler LK, Shafto MA, Randall B., Wright P., Marslen-Wilson WD, Stamatakis EA2010. Preserving syntactic processing across the adult life span: the modulation of the frontotemporal language system in the context of age-related atrophy. Cereb Cortex20:352-64.
68.
Urban PP, Hopf HC, Connemann B., Hundemer HP, Koehler J.1996. The course of cortico-hypoglossal projections in the human brainstem: functional testing using transcranial magnetic stimulation. Brain119(pt 3):1031-8.
69.
VanderHorst VG, Terasawa E., Ralston HJ III.2001. Monosynaptic projections from the nucleus retroambiguus region to laryngeal motoneurons in the rhesus monkey. Neuroscience107:117-25.
70.
van de Ven V., Esposito F., Christoffels IK2009. Neural network of speech monitoring overlaps with overt speech production and comprehension networks: a sequential spatial and temporal ICA study. Neuroimage47:1982-91.
71.
Willems RM, Ozyurek A., Hagoort P.2009. Differential roles for left inferior frontal and superior temporal cortex in multimodal integration of action and language. Neuroimage47: 1992-2004.
72.
Wilson SM, Saygin AP, Sereno MI, Iacoboni M.2004. Listening to speech activates motor areas involved in speech production. Nat Neurosci7:701-2.
73.
Wise RJ, Greene J., Buchel C., Scott SK1999. Brain regions involved in articulation. Lancet353:1057-61.
74.
Woolsey CN, Settlage PH, Meyer DR, Sencer W., Pinto Hamuy T., Travis AM1952. Patterns of localization in precentral and "supplementary" motor areas and their relation to the concept of a premotor area. Res Publ Assoc Res Nerv Ment Dis30:238-64.
75.
Zheng ZZ, Munhall KG, Johnsrude IS2010. Functional overlap between regions involved in speech perception and in monitoring one’s own voice during speech production . J Cogn Neurosci22:1770-81.
