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

Oren Poliva

doi:10.12688/f1000research.6175.1

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 lobule (auditory dorsal stream; ADS). The AVS is responsible for sound recognition, and the ADS for sound-localization, voice detection and audio-visual integration. I propose that the primary role of the ADS in monkeys/apes is the perception and response to contact calls. These calls are exchanged between tribe members (e.g., mother-offspring) and are used for monitoring location. Perception of contact calls occurs by the ADS detecting a voice, localizing it, and verifying that the corresponding face is out of sight. The auditory cortex then projects to parieto-frontal visuospatial regions (visual dorsal stream) for searching the caller, and via a series of frontal lobe-brainstem connections, a contact call is produced in return. Because the human ADS processes also speech production and repetition, I further describe a course for the development of speech in humans. I propose that, due to duplication of a parietal region and its frontal projections, and strengthening of direct frontal-brainstem connections, the ADS converted auditory input directly to vocal regions in the frontal lobe, which endowed early Hominans with partial vocal control. This enabled offspring to modify their contact calls with intonations for signaling different distress levels to their mother. Vocal control could then enable question-answer conversations, by offspring emitting a low-level distress call for inquiring about the safety of objects, and mothers responding with high- or low-level distress calls. Gradually, the ADS and the direct frontal-brainstem connections became more robust and vocal control became more volitional. Eventually, individuals were capable of inventing new words and offspring were capable of inquiring about objects in their environment and learning their names via mimicry.

Highlights

In the past five decades, gorillas, orangutans, chimpanzees and bonobos were shown capable of learning sign language (Blake, 2004; Gibson, 2011)
Jordania (2006), in his review of the literature, noted that other signing apes did not utilize questions and that their initiation of conversations was limited to commands (e.g., “me more eat”) and observational statements (e.g., “bird there”). This absence of a questioning mind is in direct contrast to human toddlers and children, who are renown for their incessant use of questions. My interpretation of this human-ape distinction is that during human evolution, we transitioned from the display of curiosity toward items that are present in our environment to curiosity toward items that are absent in our environment (i.e., WH questions)
Evidence for the role of the auditory dorsal stream (ADS) in encoding sounds into working memory is provided via studies that trained monkeys in a delayed matching to sample task, and reported of activation in areas CM-CL (Gottlieb et al, 1989) and intra-parietal sulcus (IPS) (Linden et al, 1999; Mazzoni et al, 1996) during the delay phase