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Brain mechanisms of acoustic communication in humans and nonhuman primates: An evolutionary perspective

Published online by Cambridge University Press:  15 May 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]/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]
Wolfram Ziegler
Affiliation:
Clinical Neuropsychology Research Group, City Hospital Munich-Bogenhausen, D-80992 Munich, and Institute of Phonetics and Speech Processing, Ludwig-Maximilians-University, D-80799 Munich, Germany. [email protected]
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Abstract

Any account of “what is special about the human brain” (Passingham 2008) must specify the neural basis of our unique ability to produce speech and delineate how these remarkable motor capabilities could have emerged in our hominin ancestors. Clinical data suggest that the basal ganglia provide a platform for the integration of primate-general mechanisms of acoustic communication with the faculty of articulate speech in humans. Furthermore, neurobiological and paleoanthropological data point at a two-stage model of the phylogenetic evolution of this crucial prerequisite of spoken language: (i) monosynaptic refinement of the projections of motor cortex to the brainstem nuclei that steer laryngeal muscles, presumably, as part of a “phylogenetic trend” associated with increasing brain size during hominin evolution; (ii) subsequent vocal-laryngeal elaboration of cortico-basal ganglia circuitries, driven by human-specific FOXP2 mutations.;>This concept implies vocal continuity of spoken language evolution at the motor level, elucidating the deep entrenchment of articulate speech into a “nonverbal matrix” (Ingold 1994), which is not accounted for by gestural-origin theories. Moreover, it provides a solution to the question for the adaptive value of the “first word” (Bickerton 2009) since even the earliest and most simple verbal utterances must have increased the versatility of vocal displays afforded by the preceding elaboration of monosynaptic corticobulbar tracts, giving rise to enhanced social cooperation and prestige. At the ontogenetic level, the proposed model assumes age-dependent interactions between the basal ganglia and their cortical targets, similar to vocal learning in some songbirds. In this view, the emergence of articulate speech builds on the “renaissance” of an ancient organizational principle and, hence, may represent an example of “evolutionary tinkering” (Jacob 1977).

Keywords

articulate speechbasal gangliaFOXP2human evolutionspeech acquisitionspoken languagestriatumvocal behaviorvocal learning
Type
Target Article
Information
Behavioral and Brain Sciences , Volume 37 , Issue 6 , December 2014 , pp. 529 - 546
Copyright
Copyright © Cambridge University Press 2014 

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