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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. [email protected]://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. [email protected]://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. [email protected]://www.ekn.mwn.de
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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.

Type
Authors' Response
Information
Behavioral and Brain Sciences , Volume 37 , Issue 6 , December 2014 , pp. 577 - 604
Copyright
Copyright © Cambridge University Press 2014 

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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