Neurocomputational Consequences of Evolutionary Connectivity Changes in Perisylvian Language Cortex

Abstract

The human brain sets itself apart from that of its primate relatives by specific neuroanatomical features, especially the strong linkage of left perisylvian language areas (frontal and temporal cortex) by way of the arcuate fasciculus (AF). AF connectivity has been shown to correlate with verbal working memory—a specifically human trait providing the foundation for language abilities—but a mechanistic explanation of any related causal link between anatomical structure and cognitive function is still missing. Here, we provide a possible explanation and link, by using neurocomputational simulations in neuroanatomically structured models of the perisylvian language cortex. We compare networks mimicking key features of cortical connectivity in monkeys and humans, specifically the presence of relatively stronger higher-order “jumping links” between nonadjacent perisylvian cortical areas in the latter, and demonstrate that the emergence of working memory for syllables and word forms is a functional consequence of this structural evolutionary change. We also show that a mere increase of learning time is not sufficient, but that this specific structural feature, which entails higher connectivity degree of relevant areas and shorter sensorimotor path length, is crucial. These results offer a better understanding of specifically human anatomical features underlying the language faculty and their evolutionary selection advantage.SIGNIFICANCE STATEMENT Why do humans have superior language abilities compared to primates? Recently, a uniquely human neuroanatomical feature has been demonstrated in the strength of the arcuate fasciculus (AF), a fiber pathway interlinking the left-hemispheric language areas. Although AF anatomy has been related to linguistic skills, an explanation of how this fiber bundle may support language abilities is still missing. We use neuroanatomically structured computational models to investigate the consequences of evolutionary changes in language area connectivity and demonstrate that the human-specific higher connectivity degree and comparatively shorter sensorimotor path length implicated by the AF entail emergence of verbal working memory, a prerequisite for language learning. These results offer a better understanding of specifically human anatomical features for language and their evolutionary selection advantage.

Development of information sharing in language neocortex in childhood‐onset drug‐resistant epilepsy

“…The thickness of the arrows corresponds with mean mutual information in the age group, whereas color indicates statistical significance (red, P ≤ 0.0032, Šidák-corrected P value for 16 independent regression models; orange, 0.05 ≤ P ≤ 0.0032, suggesting a trend but not meeting criteria for statistical significance; blue, P > 0.05) observations in children and showed that HGM during story listening has higher specificity and accuracy to determine ESM language sites in the posterior compared to frontal ROIs. 32 Clinically, our findings also agree with a study including 18 adults with brain tumors who had repeat craniotomies after a mean interval of 4.1 years, where intraoperative ESM at the same locations showed a loss or gain of function at 8.5% of 117 cortical sites. Similarly, increasing MI with age in the Broca's area-Wernicke's area pair during the listening task probably indicates more efficient decoding of expressive representations in the heard speech.…”

“…6 Recently, we confirmed these Mean mutual information for patients in these age groups is shown between pairs of language regions of interest (red, Broca's area; pink, inferior precentral gyrus; brown, frontal association cortex; blue, Wernicke's area; turquoise, posterior association cortex), for picture naming (A-D) and story listening (E-H). 32 Additionally, in humans, other perisylvian corticocortical connections were shown to decrease the effective path length, contributing to better information sharing within the audioarticulatory loop, which further supports our hypothesis of spatial redundancy in these F I G U R E 3 Mutual information between pairs of language regions during story listening. 7 Hence, increasing MI with age between Wernicke's area and FAC/PAC likely represents an important role of Wernicke's area in transferring information contained in auditory speech representations to association cortices.…”

“…A recent computer simulation study showed that arcuate fasciculus has a critical role in word learning because its rich connectivity in humans (compared to other primates) allows more efficient binding of auditory and articulatory information about speech due to reverberating perisylvian neuronal circuits. 32 Additionally, in humans, other perisylvian corticocortical connections were shown to decrease the effective path length, contributing to better information sharing within the audioarticulatory loop, which further supports our hypothesis of spatial redundancy in these F I G U R E 3 Mutual information between pairs of language regions during story listening. Linear regression models for mutual information (y-axis) between pairs of language cortical regions during story listening are shown as functions of age (x-axis).…”

What can autism teach us about the role of sensorimotor systems in higher cognition? New clues from studies on language, action semantics, and abstract emotional concept processing

“…These may be made possible via the neuroanatomical longdistance connections between motor (frontal) and sensory (temporoparietal) regions, which are particularly richly developed in humans (Pulvermü ller & Fadiga, 2010). These may indeed contribute to an explanation why human language and sociocommunicative interaction is much more complex than that seen in primates (Schomers et al, 2017).…”

“…The impaired integration of motor and perceptual information shown here in the language domain most particularly implies deficits in the long-distance fibre bundles that are especially important in the sensorimotor 'information mixing' process for language. The arcuate fasciculus (AF) has been purported to play a particular role in channelling sensory activity in temporal and parietal regions to the frontal lobe and motor cortex (Pulvermü ller & Fadiga, 2010;Schomers et al, 2017). We thus conducted probabilistic tractography (diffusion-weighted imaging) of the long frontotemporal segment of the arcuate in 18 adults with AS and 14 .…”