Hostname: page-component-77f85d65b8-2tv5m Total loading time: 0 Render date: 2026-03-27T09:27:48.889Z Has data issue: false hasContentIssue false
  • English
  • Français

Phylogenetic reorganization of the basal ganglia: A necessary, but not the only, bridge over a primate Rubicon of acoustic communication

Published online by Cambridge University Press:  17 December 2014

Hermann Ackermann ,
Steffen R. Hage  and
Wolfram Ziegler
Hermann Ackermann
Affiliation:
Neurophonetics Group, Centre for Neurology – General Neurology, Hertie Institute for Clinical Brain Research, University of Tuebingen, D-72076 Tuebingen, Germany. hermann.ackermann@uni-tuebingen.de http://www.hih-tuebingen.de/neurophonetik/
Steffen R. Hage
Affiliation:
Neurobiology of Vocal Communication Research Group, Werner Reichardt Centre for Integrative Neuroscience, and Institute for Neurobiology, Department of Biology, University of Tuebingen, D-72076 Tuebingen, Germany. steffen.hage@uni-tuebingen.de http://www.vocalcommunication.de
Wolfram Ziegler
Affiliation:
Clinical Neuropsychology Research Group, Municipal Hospital Munich-Bogenhausen, D-80992 Munich, and Institute of Phonetics and Speech Processing, Ludwig-Maximilians-University, D-80799 Munich, Germany. wolfram.ziegler@extern.lrz-muenchen.de http://www.ekn.mwn.de
Get access Rights & Permissions [Opens in a new window]

Abstract

In this response to commentaries, we revisit the two main arguments of our target article. Based on data drawn from a variety of research areas – vocal behavior in nonhuman primates, speech physiology and pathology, neurobiology of basal ganglia functions, motor skill learning, paleoanthropological concepts – the target article, first, suggests a two-stage model of the evolution of the crucial motor prerequisites of spoken language within the hominin lineage: (1) monosynaptic refinement of the projections of motor cortex to brainstem nuclei steering laryngeal muscles, and (2) subsequent “vocal-laryngeal elaboration” of cortico-basal ganglia circuits, driven by human-specific FOXP2 mutations. Second, as concerns the ontogenetic development of verbal communication, age-dependent interactions between the basal ganglia and their cortical targets are assumed to contribute to the time course of the acquisition of articulate speech. Whereas such a phylogenetic reorganization of cortico-striatal circuits must be considered a necessary prerequisite for ontogenetic speech acquisition, the 30 commentaries – addressing the whole range of data sources referred to – point at several further aspects of acoustic communication which have to be added to or integrated with the presented model. For example, the relationships between vocal tract movement sequencing – the focus of the target article – and rhythmical structures of movement organization, the connections between speech motor control and the central-auditory and central-visual systems, the impact of social factors upon the development of vocal behavior (in nonhuman primates and in our species), and the interactions of ontogenetic speech acquisition – based upon FOXP2-driven structural changes at the level of the basal ganglia – with preceding subvocal stages of acoustic communication as well as higher-order (cognitive) dimensions of phonological development. Most importantly, thus, several promising future research directions unfold from these contributions – accessible to clinical studies and functional imaging in our species as well as experimental investigations in nonhuman primates.

Information

Type
Authors' Response
Information
Behavioral and Brain Sciences , Volume 37 , Issue 6 , December 2014 , pp. 577 - 604
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.)

Article purchase

Temporarily unavailable

References

Ackermann, H. & Brendel, B. (in press) Cerebellum. In: The neurobiology of language, ed. Hickok, G. & Small, S. L.. Elsevier.Google Scholar
Ackermann, H., Konczak, J. & Hertrich, J. (1997b) The temporal control of repetitive articulatory movements in Parkinson's disease. Brain and Language 56:312–19.Google Scholar
Ackermann, H., Mathiak, K. & Riecker, A. (2007) The contribution of the cerebellum to speech production and speech perception: Clinical and functional imaging data. Cerebellum 6:202–13.Google Scholar
Ackermann, H. & Ziegler, W. (1994) Acoustic analysis of vocal instability in cerebellar dysfunctions. Annals of Otology, Rhinology and Laryngology 103:98–104.CrossRefGoogle ScholarPubMed
Alpert, M., Pouget, E. R. & Silva, R. R. (2001) Reflections of depression in acoustic measures of the patient's speech. Journal of Affective Disorders 66:59–69.Google Scholar
Breitenstein, C., Daum, I. & Ackermann, H. (1998) Emotional processing following cortical and subcortical brain damage: Contribution of the fronto-striatal circuitry. Behavioural Neurology 11:29–42.Google Scholar
Brendel, B. & Ziegler, W. (2008) Effectiveness of metrical pacing in the treatment of apraxia of speech. Aphasiology 22:77–102.Google Scholar
Brumm, H. & Slabbekoorn, H. (2005) Acoustic communication in noise. Advances in the Study of Behavior 35:151–209.CrossRefGoogle Scholar
Brumm, H. & Zollinger, S. A. (2011) The evolution of the Lombard effect: 100 years of psychoacoustic research. Behaviour 148:1173–98.Google Scholar
Cardona, J. F., Gershanik, O., Gelormini-Lezama, C., Houck, A. L., Cardona, S., Kargieman, L., Trujillo, N., Arévalo, A., Amoruso, L., Manes, F. & Ibánez, A. (2013) Action-verb processing in Parkinson's disease: New pathways for motor-language learning. Brain Structure and Function 218:1355–73.CrossRefGoogle Scholar
Cohn, J. F., Kruez, T. S., Matthews, I., Yang, Y., Nguyen, M. H., Padilla, M. T., Zhou, F. & De la Torre, F. (2009) Detecting depression from facial actions and vocal prosody. In: Proceedings of the Third International Conference on Affective Computing and Intelligent Interaction (ACII-09), 10-12 September 2009, Amsterdam, The Netherlands, pp. 1–7. IEEE Xplore Digital Library.Google Scholar
Cummins, F. (2009) Rhythm as entrainment: The case of synchronous speech. Journal of Phonetics 37:16–28.Google Scholar
Ellgring, H. & Scherer, K. R. (1996) Vocal indicators of mood change in depression. Journal of Nonverbal Behavior 20:83–110.Google Scholar
Fagan, B. (2010) Cro-Magnon: How the Ice Age gave birth to the first modern humans. Bloomsbury.Google Scholar
Fichtel, C., Hammerschmidt, K. & Jürgens, U. (2001) On the vocal expression of emotion: A multi-parametric analysis of different states of aversion in the squirrel monkey. Behaviour 138:97–116.Google Scholar
Goldstein, L. M., Byrd, D. & Saltzman, E. (2006) The role of vocal tract gestural action units in understanding the evolution of phonology. In: Action to language via the mirror neuron system, ed. Arbib, M. A., pp. 215–49. Cambridge University Press.Google Scholar
Hage, S. R., Jiang, T., Berquist, S. W., Feng, J. & Metzner, W. (2013) Ambient noise induces independent shifts in call frequency and amplitude within the Lombard effect in echolocating bats. Proceedings of the National Academy of Sciences USA 110(10):4063–68.CrossRefGoogle ScholarPubMed
Hage, S. R. & Nieder, A. (2013) Single neurons in monkey prefrontal cortex encode volitional initiation of vocalizations. Nature Communications 4:2409.Google Scholar
Hosoda, C., Tanaka, K., Nariai, T., Honda, M. & Hanakawa, T. (2013) Dynamic neural network reorganization associated with second language vocabulary acquisition: A multimodal imaging study. The Journal of Neuroscience 33:13663–72.Google Scholar
Hurford, J. R. (2007) The origins of meaning: Language in the light of evolution. Oxford University Press.Google Scholar
Jankovic, J. (2008) Parkinson's disease: Clinical features and diagnosis. Journal of Neurology, Neurosurgery, and Psychiatry 79:368–76.CrossRefGoogle ScholarPubMed
Johansson, S. (2005) Origins of language: Constraints on hypotheses. John Benjamins.Google Scholar
Kirzinger, A. (1985) Cerebellar lesion effects on vocalization of the squirrel monkey. Behavioural Brain Research 16:177–81.CrossRefGoogle ScholarPubMed
Konczak, J., Ackermann, H., Hertrich, I., Spieker, S. & Dichgans, J. (1997) Control of repetitive lip and finger movements in Parkinson's disease: Influence of external timing signals and simultaneous execution on motor performance. Movement Disorders 12:665–76.CrossRefGoogle ScholarPubMed
Larson, C. R. & Kistler, M. K. (1984) Periaqueductal gray neuronal activity associated with laryngeal EMG and vocalization in the awake monkey. Neuroscience Letters 46:261–66.CrossRefGoogle ScholarPubMed
MacNeilage, P. F. (1998) The frame/content theory of evolution of speech production. Behavioral and Brain Sciences 21(4):499–511.Google Scholar
MacNeilage, P. F. (2008) The origin of speech. Oxford University Press.Google Scholar
MacNeilage, P. F. & Davis, B. L. (2001) Motor mechanisms in speech ontogeny: Phylogenetic, neurobiological and linguistic implications. Current Opinion in Neurobiology 11:696–700.Google Scholar
Massart, R., Mongeau, R. & Lanfumey, L. (2012) Beyond the monoaminergic hypothesis: Neuroplasticity and epigenetic changes in a transgenic mouse model of depression. Philosophical Transactions of the Royal Society B 367:2485–94.Google Scholar
Mithen, S. J. (2006) The singing Neanderthals: The origins of music, language, mind and body. Harvard University Press. (Original work published in 2005).Google Scholar
Peelle, J. E. & Davis, M. H. (2012) Neural oscillations carry speech rhythm through to comprehension. Frontiers in Psychology 3:320.Google Scholar
Riecker, A., Wildgruber, D., Dogil, G., Grodd, W. & Ackermann, H. (2002) Hemispheric lateralization effects of rhythm implementation during syllable repetitions: An fMRI study. NeuroImage 16:169–76.Google Scholar
Rothermich, K., Schmidt-Kassow, M. & Kotz, S. A. (2012) Rhythm's gonna get you: Regular meter facilitates semantic sentence processing. Neuropsychologia 50:232–44.Google Scholar
Schmahmann, J. D. & Sherman, J. C. (1998) The cerebellar cognitive affective syndrome. Brain 121 (Pt. 4):561–79.Google Scholar
Sidtis, J. J. & Van Lancker Sidtis, D. (2003) A neurobehavioral approach to dysprosody. Seminars in Speech and Language 24:93–105.Google Scholar
Sterelny, K. (2012) The evolved apprentice: How evolution made humans unique. MIT Press.Google Scholar
Teichmann, M., Dupoux, E., Kouider, S., Brugières, P., Boissé, M. F., Baudic, S., Cesaro, P., Peschanski, M. & Bachoud-Lévi, A. C. (2005) The role of the striatum in rule application: The model of Huntington's disease at early stage. Brain 128:1155–67.Google Scholar
Ullman, M. T. (2001) A neurocognitive perspective on language: The declarative/procedural model. Nature Reviews Neuroscience 2:717–26.CrossRefGoogle ScholarPubMed
Weiller, C., Willmes, K., Reiche, W., Thron, A., Isensee, C., Buell, U. & Ringelstein, E. B. (1993) The case of aphasia or neglect after striatocapsular infarction. Brain 116:1509–25.Google Scholar
Wilson, M. & Wilson, T. P. (2005) An oscillator model of the timing of turn-taking. Psychonomic Bulletin and Review 12:957–68.Google Scholar
Wittforth, M., Schröder, C., Schardt, D. M., Dengler, R., Heinze, H. J. & Kotz, S. A. (2010) On emotional conflict: Interference resolution of happy and angry prosody reveals valence-specific effects. Cerebral Cortex 20(2):383–92.Google Scholar