A model for Social Communication And Language Evolution and Development (SCALED)
Introduction
Classical neurological models of language consist of the arcuate fasciculus connecting Broca's and Wernicke's regions dedicated to speech production and comprehension, respectively. This dorsal network is considered pivotal in syntactic analysis and auditory–motor transcoding. In addition to classical language areas, several studies have suggested that the anterior temporal lobe is crucial for lexical and semantic processing. Hence, the majority of language models are based on a dual stream, a dorsal phonological route for mapping sound into words and a ventral semantic route for mapping sound into meaning [1, 2, 3].
The dual stream model may represent an oversimplification as recent evidence based on tractography suggests that language relies on a more extended network encompassing additional connections to the inferior parietal lobule [4, 5] and the dorsomedial frontal cortex [6, 7•]. These connections seem to underlie other aspects of communication, at the interface between language and social cognition, in the domain of pragmatics [8, 9, 10•, 11••].
In this article we review and integrate these recent developments in a five-tiered anatomical model of social communication and language (Figure 1). The model includes different aspects of language knowledge and use, from basic recognition of pre-linguistic informative actions to complex pragmatic interpretation. The model is primarily based on imaging studies in humans and finds support from developmental studies, comparative anatomy, and observation of animal behaviour. A key feature of the model is the hierarchical organization of the five levels according to developmental and evolutionary aspects of social communication.
Section snippets
Level 1. A fronto-parietal network for informative actions
Within the arcuate fasciculus, a subset of fibres (anterior segment) links Broca's region to Geschwind's region in the inferior parietal lobule (Figure 1, green colour) [4]. This fronto-parietal network connects the so-called mirror neurons that activate not only during motor execution, but also when observing movements performed by others. By mapping the sensory representation of actions and sounds made by others onto internal motor representations, the mirror neuron network may implement a
Level 2. A frontal aslant network for communicative intentions
Broca's region is also connected to the dorsomedial frontal cortex via a newly described fascicle we termed the ‘frontal aslant tract’ (Figure 1, purple colour) [6, 18, 19]. A number of studies identified the posterior portions of the dorsomedial frontal cortex (pre-supplementary motor area) as involved in distinguishing self from others’ actions [20], action monitoring [21] and low-level aspects of mentalizing [22]. More anterior areas (the medial pre-frontal cortex) are involved in higher
Level 3. Anterior temporal networks for lexical and semantic processing
Wernicke's region is connected to the anterior temporal lobe via the middle and inferior longitudinal fasciculus (Figure 1, dark and light blue colours, respectively). Furthermore, connections from the anterior temporal lobe to anterior Broca's region run through the uncinate fasciculus (Figure 1, azure colour) [7•, 31, 32]. In addition, other authors describe direct connections between Wernicke's and Broca's region through the inferior fronto-occipital fasciculus (Figure 1, cyan colour) [2].
Level 4. A fronto-temporal network for syntactic analysis
The long segment of the arcuate fasciculus connects directly Broca's and Wernicke's regions (Figure 1, red colour) [4, 39•]. A significant portion of this dorsal network (especially projections to the middle temporal gyrus) is involved in syntactic production and comprehension. Broca's region activates in tasks involving processing of syntactically complex sentences and acquisition of grammatical rules [40••, 41•] while the middle temporal gyrus in Wernicke's region participates in syntactic
Level 5. A temporo-parietal network for pragmatic integration
The posterior segment of the arcuate fasciculus is a short vertical tract connecting Wernicke's region to the Geschwind's region (especially the angular gyrus) (Figure 1, yellow colour) [4, 39•]. This temporo-parietal network is involved in semantic aspects of language processing [46] and high-level social cognition [22, 23, 24••]. This connection has also a key role in stimulus-driven control of attention and diverting self-reflective thinking to salient external stimuli [47]. In addition, the
General features of the model
In this paper we reviewed the recent literature on language networks, in particular evidence of a dorsal and a ventral stream, and we incorporated newly described connections involving the inferior parietal lobule and the dorsomedial frontal cortex. Our proposal consists of a hierarchical neuroanatomical model that integrates aspects of language and social cognition for communication. Each level of the model lays out the ground for the acquisition of higher social, linguistic and pragmatic
Limitations and future directions
We hope that the SCALED model will help to integrate anatomical and neurolinguistic approaches to communicative behaviour. Yet multiple features of the model remain to be clarified. A crucial difficulty for our proposal is its reliance on anatomical evidence derived primarily from axonal tracing in macaque monkeys and diffusion tractography in humans. Both methods have several advantages but their current limitations hinder our detailed knowledge of comparative anatomy [65]. Considering the
Conflict of interest statement
Nothing declared.
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
The authors wish to thank Michel Thiebaut de Schotten for providing the human diffusion dataset, Alex de Crespigny and Helen D’Arceuil for the macaque brain dataset used in Figure 1, Stefano Cappa, Stephanie Forkel, and Andrea Moro for useful comments. Marco Catani is recipient of a New Investigator Award from the Wellcome Trust (103759/Z/14/Z). Valentina Bambini is partially supported by the Italian PRIN project ‘I meccanismi neurocognitivi alla base delle interazioni sociali’ (MIUR
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