Gestures, vocalizations, and memory in language origins

Abstract

THIS ARTICLE DISCUSSES THE POSSIBLE HOMOLOGIES BETWEEN THE HUMAN LANGUAGE NETWORKS AND COMPARABLE AUDITORY PROJECTION SYSTEMS IN THE MACAQUE BRAIN, IN AN ATTEMPT TO RECONCILE TWO EXISTING VIEWS ON LANGUAGE EVOLUTION: one that emphasizes hand control and gestures, and the other that emphasizes auditory-vocal mechanisms. The capacity for language is based on relatively well defined neural substrates whose rudiments have been traced in the non-human primate brain. At its core, this circuit constitutes an auditory-vocal sensorimotor circuit with two main components, a "ventral pathway" connecting anterior auditory regions with anterior ventrolateral prefrontal areas, and a "dorsal pathway" connecting auditory areas with parietal areas and with posterior ventrolateral prefrontal areas via the arcuate fasciculus and the superior longitudinal fasciculus. In humans, the dorsal circuit is especially important for phonological processing and phonological working memory, capacities that are critical for language acquisition and for complex syntax processing. In the macaque, the homolog of the dorsal circuit overlaps with an inferior parietal-premotor network for hand and gesture selection that is under voluntary control, while vocalizations are largely fixed and involuntary. The recruitment of the dorsal component for vocalization behavior in the human lineage, together with a direct cortical control of the subcortical vocalizing system, are proposed to represent a fundamental innovation in human evolution, generating an inflection point that permitted the explosion of vocal language and human communication. In this context, vocal communication and gesturing have a common history in primate communication.

Keywords: arcuate fasciculus; broca’s area; inferior parietal lobe; mirror neurons; phonological loop; superior longitudinal fasciculus; working memory.

Figure 1

Diagram depicting the language-related circuit in humans, as proposed by Frey et al. (2008). The superior longitudinal fasciculus (SLF) connects inferior parietal areas PF with the ventral premotor cortex (area 6; green), while areas PFG and PG are connected with areas 44 and 45 (red). The arcuate fasciculus (AF) connects posterior superior temporal regions with areas 44 and 45 as well (red), but is difficult to separate from the inferior branch of the SLF. The middle longitudinal fasciculus (MLF, blue) connects the posterior superior temporal gyrus and sulcus (STG, STS) with inferoparietal regions PFG and PG. Finally, a ventral route running via the extreme capsule (ECF, yellow) connects the middle and anterior temporal lobe with areas 44 and 45. A similar circuit has been described for the monkey (Petrides and Pandya, 2009). Ang, angular gyrus; aSMG, anterior supramarginal gyrus; CS, central sulcus; IPS, intraparietal sulcus; MI, primary motor area; MTG, middle temporal gyrus; pSMG, posterior supramarginal gyrus; SI, primary somatosensory area. Based on Kelly et al. (2010), with permission.

Figure 2

(A) Diagram depicting the location of the inferior arcuate sulcus (IAS), the intraparietal sulcus and inferior parietal lobe (IPS and IPS/IPL), and the superior temporal sulcus (STS) in the macaque brain. (B) Pathways involved in action understanding, according to Nelissen et al. (2011). In red, an intention-processing pathway connecting the upper (STS) with area PFG and mainly frontal area F5c; and in blue, an object-related pathway connecting the lower STS with area AIP and areas F5p and F5a. There are also connections to area 45B from area lateral intraparietal area a (LIPa) and the anterior STS (green). No projections are shown here from areas PFG and PF, but related studies have described projections from area PFG into F5a and F5p; and from PG to F5p (Gerbella et al., 2011). Modified from Nelissen et al. (2011), with permission.

Figure 3

Parcellation of the inferior arcuate sulcus (IAS) of the monkey according to (A) Petrides et al. (2005), and (B) Belmalih et al. (2009). In both cases, area 44 is shown in the depth of the sulcus, bordered anteriorly by area 45, and posteriorly by the premotor area (6v or F5a depending on the nomenclature). IAS, inferior arcuate sulcus; IPS/IPL, intraparietal sulcus and inferior parietal lobe, respectively; STS, superior temporal sulcus. From Belmalih et al. (2009), with permission.