Birds, primates, and spoken language origins: Behavioral phenotypes and neurobiological substrates

Institute of Neuroscience, Newcastle University Newcastle upon Tyne, UK.
Frontiers in Evolutionary Neuroscience 08/2012; 4:12. DOI: 10.3389/fnevo.2012.00012
Source: PubMed


Vocal learners such as humans and songbirds can learn to produce elaborate patterns of structurally organized vocalizations, whereas many other vertebrates such as non-human primates and most other bird groups either cannot or do so to a very limited degree. To explain the similarities among humans and vocal-learning birds and the differences with other species, various theories have been proposed. One set of theories are motor theories, which underscore the role of the motor system as an evolutionary substrate for vocal production learning. For instance, the motor theory of speech and song perception proposes enhanced auditory perceptual learning of speech in humans and song in birds, which suggests a considerable level of neurobiological specialization. Another, a motor theory of vocal learning origin, proposes that the brain pathways that control the learning and production of song and speech were derived from adjacent motor brain pathways. Another set of theories are cognitive theories, which address the interface between cognition and the auditory-vocal domains to support language learning in humans. Here we critically review the behavioral and neurobiological evidence for parallels and differences between the so-called vocal learners and vocal non-learners in the context of motor and cognitive theories. In doing so, we note that behaviorally vocal-production learning abilities are more distributed than categorical, as are the auditory-learning abilities of animals. We propose testable hypotheses on the extent of the specializations and cross-species correspondences suggested by motor and cognitive theories. We believe that determining how spoken language evolved is likely to become clearer with concerted efforts in testing comparative data from many non-human animal species.

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    • "First, we can voluntarily and independently control the source and filter properties of our vocalizations, and second we can perform these modulations in the complete absence of an associated inducing experience or state333435. It is important to note that vocal control as defined above is a phenomenon distinct from vocal learning, which does not necessarily involve flexible manipulation of the vocal anatomy but rather entails the capacity to acquire or converge call types or entire vocal repertoires through imitation or learning [36,37]. The use of specific[ 5 1 _ T D $ D I F F ] and pre-existing vocalizations in different or novel contexts, and the ability to respond differentially to the vocalizations of others through experience, is considered distinct from vocal production learning, namely because these behaviors are present in a broader range of animals and are likely to require comparatively less complex neural control [38]. "
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    ABSTRACT: An unresolved issue in comparative approaches to speech evolution is the apparent absence of an intermediate vocal communication system betweenhuman speech and the lessflexible vocal repertoires of other primates. We argue that humans’ ability to modulate nonverbal vocal features evolutionarily linked to expression of body size and sex (fundamental and formant frequencies) provides a largely overlooked window into the nature of this intermediate system. Recent behavioral and neural evidence indicates that humans’ vocal control abilities, commonly assumed to subserve speech, extend to these nonverbal dimensions. This capacity appears in continuity with context-dependent frequency modulations recently identified in other mammals, including primates, and may represent a living relic of early vocal control abilities that led to articulated human speech.
    Full-text · Article · Feb 2016 · Trends in Cognitive Sciences
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    • "The robust nucleus of the arcopallium (RA) is a premotor nucleus in the VMP. RA receives inputs from HVC (used as a proper name) of the VMP and also receives inputs from the lateral magnocellular nucleus of anterior nidopallium (LMAN) of the anterior forebrain pathway (AFP) that is necessary for song learning and adult song variability [3]. RA projection neurons project to brainstem respiratory and vocal control nuclei to form a part of song premotor pathway [4]. "
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    ABSTRACT: Cholinergic mechanism is involved in motor behavior. In songbirds, the robust nucleus of the arcopallium (RA) is a song premotor nucleus in the pallium and receives cholinergic inputs from the basal forebrain. The activity of projection neurons in RA determines song motor behavior. Although many evidences suggest that cholinergic system is implicated in song production, the cholinergic modulation of RA is not clear until now. In the present study, the electrophysiological effects of carbachol, a nonselective cholinergic receptor agonist, were investigated on the RA projection neurons of adult male zebra finches through whole-cell patch-clamp techniques in vitro. Our results show that carbachol produced a significant decrease in the spontaneous and evoked action potential (AP) firing frequency of RA projection neurons, accompanying a hyperpolarization of the membrane potential, an increase in the evoked AP latency, afterhyperpolarization (AHP) peak amplitude, and AHP time to peak, and a decrease in the membrane input resistance, membrane time constant, and membrane capacitance. These results indicate that carbachol reduces the activity of RA projection neurons by hyperpolarizing the resting membrane potential and increasing the AHP and the membrane conductance, suggesting that the cholinergic modulation of RA may play an important role in song production.
    Full-text · Article · Dec 2015 · Neural Plasticity
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    • ", 2014 ) . The songbird HVC is similar to layers 2 and 3 neurons of primary motor cortex , and thereby possibly also to LMC ; songbird LMAN has a weak similarity to Broca ' s area that requires further investigation for confirmation ; DLM ( dorsolateral nucleus of the medial thalamus ) is most similar to the human anterior thalamus necessary for speech learning and production ( Jarvis , 2004 ; Petkov and Jarvis , 2012 ) . In this article I present a hypothesis on how foreign accents could be improved by optimizing variability in vocal learning brain circuits , followed by support for the hypothesis , drawing on the literature on variability in songbird vocal learning and variability in motor learning . "
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    ABSTRACT: Rapid vocal motor learning is observed when acquiring a language in early childhood, or learning to speak another language later in life. Accurate pronunciation is one of the hardest things for late learners to master and they are almost always left with a non-native accent. Here, I propose a novel hypothesis that this accent could be improved by optimizing variability in vocal learning brain circuits during learning. Much of the neurobiology of human vocal motor learning has been inferred from studies on songbirds. Jarvis (2004) proposed the hypothesis that as in songbirds there are two pathways in humans: one for learning speech (the striatal vocal learning pathway), and one for production of previously learnt speech (the motor pathway). Learning new motor sequences necessary for accurate non-native pronunciation is challenging and I argue that in late learners of a foreign language the vocal learning pathway becomes inactive prematurely. The motor pathway is engaged once again and learners maintain their original native motor patterns for producing speech, resulting in speaking with a foreign accent. Further, I argue that variability in neural activity within vocal motor circuitry generates vocal variability that supports accurate non-native pronunciation. Recent theoretical and experimental work on motor learning suggests that variability in the motor movement is necessary for the development of expertise. I propose that there is little trial-by-trial variability when using the motor pathway. When using the vocal learning pathway variability gradually increases, reflecting an exploratory phase in which learners try out different ways of pronouncing words, before decreasing and stabilizing once the “best” performance has been identified. The hypothesis proposed here could be tested using behavioral interventions that optimize variability and engage the vocal learning pathway for longer, with the prediction that this would allow learners to develop new motor patterns that result in more native-like pronunciation.
    Full-text · Article · Nov 2015 · Frontiers in Human Neuroscience
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