Trends in Neurosciences
Volume 39, Issue 12, December 2016, Pages 813-829
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Feature Review
Dual Neural Network Model for the Evolution of Speech and Language

https://doi.org/10.1016/j.tins.2016.10.006Get rights and content

Trends

A dual-network model for the evolution of language is proposed that consists of two interacting brain networks.

A phylogenetically conserved PVMN produces genetically predetermined vocalizations in nonhuman primates and non-verbal vocalizations in humans.

During the course of primate evolution, an additional VAMN in the lateral frontal lobe (including Broca's area) emerges that cognitively controls vocal output.

In humans, the VAMN gains control over articulation by modulating the output of the PVMN.

The new VAMN also plays a vital role in establishing semantics and syntax, two hallmark characteristics of symbol systems in humans.

Explaining the evolution of speech and language poses one of the biggest challenges in biology. We propose a dual network model that posits a volitional articulatory motor network (VAMN) originating in the prefrontal cortex (PFC; including Broca's area) that cognitively controls vocal output of a phylogenetically conserved primary vocal motor network (PVMN) situated in subcortical structures. By comparing the connections between these two systems in human and nonhuman primate brains, we identify crucial biological preadaptations in monkeys for the emergence of a language system in humans. This model of language evolution explains the exclusiveness of non-verbal communication sounds (e.g., cries) in infants with an immature PFC, as well as the observed emergence of non-linguistic vocalizations in adults after frontal lobe pathologies.

Section snippets

The Apparent Discrepancy

Few questions in biology are as difficult and controversial as the evolution of human speech and language, and the emergence of essential speech and language brain structures such as Broca's area in the lateral frontal lobe. This is because human language vastly outperforms any primate communication system in scope and flexibility 1, 2, 3, with seemingly no counterpart in the animal kingdom, even among hominids. The vocalizations of nonhuman primates are largely innate, stereotypic, and were

The PVMN for Innate Primate Vocalizations

All primates possess a PVMN that produces genetically predetermined vocalizations in nonhuman primates and non-verbal vocalizations in humans. This PVMN consists of two structurally and functionally distinct parts: a vocal pattern-generating system in the brainstem, and an upstream limbic vocal-initiating network driving the pattern generator based on affective states (Figure 1A,B) 4, 5, 10.

The core of the PVMN, the brainstem vocal pattern-generating system is highly conserved in all vertebrate

The Role of the PVMN in Human Non-Verbal Vocalizations and Speech

It is important to realize that the phylogenetically conserved PVMN is still involved in vocalization in humans. One of its functions is to produce non-verbal vocal utterances such as crying, laughing, or moaning, all of which are innately predetermined and affective vocalizations considered to be directly homologous to monkey vocalizations 4, 5. Although brainstem lesions are often fatal, a clinical study revealed pathological laughter and crying due to a tumor beneath the brainstem that most

Volitional Articulatory Motor Network

Humans possess an additional VAMN consisting of cortical structures crucial for human speech control, and which is already present, although being anatomically and functionally underdeveloped, in the monkey brain. The VAMN comprises the inferior frontal gyrus (IFG), the caudally bordering ventral premotor cortex (area 6, PMv), and ventrolateral primary motor cortex (area 4, M1) including the facial and laryngeal motor cortex (Figure 1A,B). The central executive of this network is Broca's area,

The PFC Receives and Classifies Communicative Signals

For a cortical network to control vocal output during reciprocal communication acts, sensory input from a sender is required. The vlPFC as the core of the VAMN receives highly processed information from higher-order sensory areas of all modalities (Figure 4). Neurons in the vlPFC categorize and maintain communicative signals in working memory to guide goal-directed output.

Auditory information reaches the lateral PFC via two largely anatomically and functionally segregated cortical streams: the

PFC Precursors of Semantics in Primate Referential Systems

The VAMN is much more than merely a high-order motor network. It also plays a vital role in establishing semantics and syntax, two hallmark characteristics of the two symbol systems – language and number theory. In symbolic reference, relations are established between spoken/written words or numbers, respectively, on the basis of compositional rules (i.e., syntax) 138, 139. However, simpler and both phylogenetically and ontogenetically earlier referential associations are ‘indices’ – signs that

PFC Precursors of Grammar in Primate Referential Systems

To establish a fully fledged symbol/language system, meaningful associations (semantics) are not sufficient. Sign sequences must be hierarchically structured according to action plans or rules guiding the structuring of signs – ‘syntax’. Syntax refers to the rules governing structure in natural language sentences or mathematical systems. Syntax establishes relations between signs that determine the meaning of an expression. Therefore, syntax and semantics are inextricably linked in symbolic

Conclusions and Future Directions

In this review we suggest that the incipient linking of the prefrontal central executive of the brain with the vocalization system is a key neurobiological event and pre-adaptation for the evolution of speech and language. Crucial evidence for this hypothesis stems from comparative investigations of the cytoarchitecture of the human and the monkey vlPFC. These studies demonstrated that the basic architectonic plans are similar in these two primate brains, despite considerable development of the

Acknowledgements

We thank Barbara Peysakhovich for proofreading. This work was supported by the Werner Reichardt Centre for Integrative Neuroscience (CIN) at the Eberhard Karls University of Tübingen (CIN is an Excellence Cluster funded by the Deutsche Forschungsgemeinschaft within the frame-work of the Excellence Initiative EXC 307).

Glossary

Articulation
complex movements of the cranial muscles (facial, lip, tongue, jaw) to alter a basic tone, which is produced by the vocal folds, into decodable sounds.
Grammar
rules that govern how words can be combined to form sentences.
Language
a generative symbol-system to generate infinite meanings (semantics) based on a finite set of rules (syntax) (and usually is used to communicate).
Limbic network
complex network of brain structures including ACC, hypothalamus, amygdala and several other

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