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      From where to what: a neuroanatomically based evolutionary model of the emergence of speech in humans

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      a , 1
      F1000Research
      F1000Research
      Speech, Evolution, Auditory dorsal stream, Contact calls, Auditory cortex, Vocal production

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          Abstract

          In the brain of primates, the auditory cortex connects with the frontal lobe via the temporal pole (auditory ventral stream; AVS) and via the inferior parietal lobe (auditory dorsal stream; ADS). The AVS is responsible for sound recognition, and the ADS for sound-localization, voice detection and integration of calls with faces. I propose that the primary role of the ADS in non-human primates is the detection and response to contact calls. These calls are exchanged between tribe members (e.g., mother-offspring) and are used for monitoring location. Detection of contact calls occurs by the ADS identifying a voice, localizing it, and verifying that the corresponding face is out of sight. Once a contact call is detected, the primate produces a contact call in return via descending connections from the frontal lobe to a network of limbic and brainstem regions.

          Because the ADS of present day humans also performs speech production, I further propose an evolutionary course for the transition from contact call exchange to an early form of speech. In accordance with this model, structural changes to the ADS endowed early members of the genus Homo with partial vocal control. This development was beneficial as it enabled offspring to modify their contact calls with intonations for signaling high or low levels of distress to their mother. Eventually, individuals were capable of participating in yes-no question-answer conversations. In these conversations the offspring emitted a low-level distress call for inquiring about the safety of objects (e.g., food), and his/her mother responded with a high- or low-level distress call to signal approval or disapproval of the interaction. Gradually, the ADS and its connections with brainstem motor regions became more robust and vocal control became more volitional. Speech emerged once vocal control was sufficient for inventing novel calls.

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          Perisylvian language networks of the human brain.

          Early anatomically based models of language consisted of an arcuate tract connecting Broca's speech and Wernicke's comprehension centers; a lesion of the tract resulted in conduction aphasia. However, the heterogeneous clinical presentations of conduction aphasia suggest a greater complexity of perisylvian anatomical connections than allowed for in the classical anatomical model. This article re-explores perisylvian language connectivity using in vivo diffusion tensor magnetic resonance imaging tractography. Diffusion tensor magnetic resonance imaging data from 11 right-handed healthy male subjects were averaged, and the arcuate fasciculus of the left hemisphere reconstructed from this data using an interactive dissection technique. Beyond the classical arcuate pathway connecting Broca's and Wernicke's areas directly, we show a previously undescribed, indirect pathway passing through inferior parietal cortex. The indirect pathway runs parallel and lateral to the classical arcuate fasciculus and is composed of an anterior segment connecting Broca's territory with the inferior parietal lobe and a posterior segment connecting the inferior parietal lobe to Wernicke's territory. This model of two parallel pathways helps explain the diverse clinical presentations of conduction aphasia. The anatomical findings are also relevant to the evolution of language, provide a framework for Lichtheim's symptom-based neurological model of aphasia, and constrain, anatomically, contemporary connectionist accounts of language.
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            Ventral and dorsal pathways for language.

            Built on an analogy between the visual and auditory systems, the following dual stream model for language processing was suggested recently: a dorsal stream is involved in mapping sound to articulation, and a ventral stream in mapping sound to meaning. The goal of the study presented here was to test the neuroanatomical basis of this model. Combining functional magnetic resonance imaging (fMRI) with a novel diffusion tensor imaging (DTI)-based tractography method we were able to identify the most probable anatomical pathways connecting brain regions activated during two prototypical language tasks. Sublexical repetition of speech is subserved by a dorsal pathway, connecting the superior temporal lobe and premotor cortices in the frontal lobe via the arcuate and superior longitudinal fascicle. In contrast, higher-level language comprehension is mediated by a ventral pathway connecting the middle temporal lobe and the ventrolateral prefrontal cortex via the extreme capsule. Thus, according to our findings, the function of the dorsal route, traditionally considered to be the major language pathway, is mainly restricted to sensory-motor mapping of sound to articulation, whereas linguistic processing of sound to meaning requires temporofrontal interaction transmitted via the ventral route.
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              Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing.

              The advent of functional neuroimaging has allowed tremendous advances in our understanding of brain-language relationships, in addition to generating substantial empirical data on this subject in the form of thousands of activation peak coordinates reported in a decade of language studies. We performed a large-scale meta-analysis of this literature, aimed at defining the composition of the phonological, semantic, and sentence processing networks in the frontal, temporal, and inferior parietal regions of the left cerebral hemisphere. For each of these language components, activation peaks issued from relevant component-specific contrasts were submitted to a spatial clustering algorithm, which gathered activation peaks on the basis of their relative distance in the MNI space. From a sample of 730 activation peaks extracted from 129 scientific reports selected among 260, we isolated 30 activation clusters, defining the functional fields constituting three distributed networks of frontal and temporal areas and revealing the functional organization of the left hemisphere for language. The functional role of each activation cluster is discussed based on the nature of the tasks in which it was involved. This meta-analysis sheds light on several contemporary issues, notably on the fine-scale functional architecture of the inferior frontal gyrus for phonological and semantic processing, the evidence for an elementary audio-motor loop involved in both comprehension and production of syllables including the primary auditory areas and the motor mouth area, evidence of areas of overlap between phonological and semantic processing, in particular at the location of the selective human voice area that was the seat of partial overlap of the three language components, the evidence of a cortical area in the pars opercularis of the inferior frontal gyrus dedicated to syntactic processing and in the posterior part of the superior temporal gyrus a region selectively activated by sentence and text processing, and the hypothesis that different working memory perception-actions loops are identifiable for the different language components. These results argue for large-scale architecture networks rather than modular organization of language in the left hemisphere.
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                Author and article information

                Journal
                F1000Res
                F1000Res
                F1000Research
                F1000Research
                F1000Research (London, UK )
                2046-1402
                21 January 2016
                2015
                : 4
                : 67
                Affiliations
                [1 ]Bangor University, Bangor, UK
                [1 ]Laboratory of Integrative Neuroscience and Cognition, Georgetown University, Washington DC, USA
                [1 ]Computer Science Department, University of Southern California, Los Angeles, CA, USA
                [1 ]Laboratory of Integrative Neuroscience and Cognition, Georgetown University, Washington DC, USA
                Bangor University, UK
                [1 ]Department of Psychology, University of Iowa, Iowa City, IA, USA
                Bangor University, UK
                Author notes

                Competing interests: No competing interests were disclosed.

                Competing interests: No competing interests were disclosed.

                Competing interests: No competing interests were disclosed.

                Competing interests: No competing interests were disclosed.

                Competing interests: No competing interests were disclosed.

                Competing interests: No competing interests were disclosed.

                Competing interests: No competing interests were disclosed.

                Article
                10.12688/f1000research.6175.2
                5600004
                d14b3b0d-10bb-422b-b325-a9a8d9e41890
                Copyright: © 2016 Poliva O

                This is an open access article distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 12 January 2016
                Funding
                The author(s) declared that no grants were involved in supporting this work.
                Categories
                Opinion Article
                Articles
                Cognitive Neuroscience
                Developmental Evolution
                Motor Systems
                Sensory Systems

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