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Morphological evolution of language-relevant brain areas [1]

['Guillermo Gallardo', 'Department Of Neuropsychology', 'Max Planck Institute For Human Cognitive', 'Brain Sciences', 'Leipzig', 'Cornelius Eichner', 'Chet C. Sherwood', 'Department Of Anthropology', 'The George Washington University', 'Washington']

Date: 2023-09

Human language is supported by a cortical network involving Broca’s area, which comprises Brodmann Areas 44 and 45 (BA44 and BA45). While cytoarchitectonic homolog areas have been identified in nonhuman primates, it remains unknown how these regions evolved to support human language. Here, we use histological data and advanced cortical registration methods to precisely compare the morphology of BA44 and BA45 in humans and chimpanzees. We found a general expansion of Broca’s areas in humans, with the left BA44 enlarging the most, growing anteriorly into a region known to process syntax. Together with recent functional and receptorarchitectural studies, our findings support the conclusion that BA44 evolved from an action-related region to a bipartite system, with a posterior portion supporting action and an anterior portion supporting syntactic processes. Our findings add novel insights to the longstanding debate on the relationship between language and action, and the evolution of Broca’s area.

Funding: This study was funded by the Max Planck Society under the inter-institutional funds of the president for the project “Evolution of Brain Connectivity (EBC)” to AF. This work was supported, in part, by NIH grants AG-067419, NS-092988, and NS- 42867 to WDH and CCS. All aspects of this research conformed to existing US and NIH federal policies on the ethical use of chimpanzees in research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Introduction

Language processing is a human trait that recruits Broca’s area in the inferior frontal gyrus [1–3]. Previous studies suggest an involvement of this area in the understanding and imitation of actions [4]. Moreover, homologous areas in nonhuman primates have similarly been shown to support actions of the orofacial muscles and upper limbs [5]. Despite extensive research, our knowledge about the relationship between action and language, and how Broca’s area evolved to support them, remains incomplete. A longstanding debate persists regarding whether language and action share the same neural basis, with 2 opposing views. One view proposes that language emerged from action expressed in communicative gestures, and thus they share a common basis [5–7]. The other view sees language as a cognitive ability independent of action [8,9].

Both views—favoring and opposing a shared basis for language and action—built their arguments on theoretical and empirical grounds [5–7]. At the theoretical level, the debate focuses on the (di)similarity between the structure of goal-directed sequential actions and syntax (i.e., the rules that govern how words are arranged in a sentence). While some argue that actions rely on a hierarchical structure of subgoals similar to that of linguistic syntax [10,11], others claim that such a description does not meet the definition of syntactic hierarchy in human language [8]. Meanwhile, at the empirical level, several studies in humans have found action to recruit Broca’s area [12,13], an area primarily related to language, thus suggesting a functional codependence between action and language [5,14,15]. However, these studies did not directly compare action against syntactic aspects of language, thus making it hard to understand if the same regions activate for both processes. In this way, the debate concerning action and language is, at its center, about the relationship between action and the core aspect of language, syntax. Other aspects of language (e.g., semantics, phonology) rely on more widely distributed neural networks [16].

To date, only 3 studies directly compared the neural underpinning of action and syntactic aspects of language in humans. Two are meta-analyses, comparing peak activations of syntactic tasks against motor-related ones [17], and syntactic processing with tool use [18]. The third study uses functional imaging to compare syntactic processing with tool use in a within-subject design [19]. All these studies found that language and action recruit largely nonoverlapping areas of Broca’s area, with language being processed more anterior than action. In addition, meta-analysis showed that Brodmann Area 44 (BA44), the cytoarchitectonic defined posterior division of Broca’s area [20,21], is functionally divided in 2 regions, with language recruiting its anterior part and action recruiting its posterior part [17]. Importantly, this functional subdivision mirrors the underlying distribution of neurotransmitter receptors in BA44, which are a powerful indicator of functional diversity [22].

To help settle the debate on the language/action relationship, we can turn to our close evolutionary relatives [23]. Anthropoid primates, such as chimpanzees and macaques, possess a cytoarchitectonically similar Broca’s area homolog that, as in humans, functionally responds to action [4]. Moreover, there is evidence that great apes can master some aspects of language using augmentative or alternative communication systems such as gestures or visual graphic symbols [24]. However, only humans possess the faculty of creating complex multiword utterances following a syntactic hierarchy [25]. Hence, a cross-species comparison between the human linguistic brain and that of one of our close living relatives, the chimpanzees, may shed light on the neural basis of action and language.

Earlier cross-species comparisons have shown that the prefrontal cortex is a region that allometrically scales to increase at a disproportionate rate across primates [23], leading to a relatively large size in the human brain [26,27]. A comparison of the cytoarchitectonic structure of Broca’s area in human and macaque brains revealed an enlargement of BA44 and BA45, in particular for the posterior part of BA45 [28]. Although the comparison with macaques is of interest, it has been argued that research focused on our nearest extant relatives, bonobos and chimpanzees, is most relevant to determine which unique features have coevolved with language abilities [23]. Comparing humans and chimpanzees, it was found that the cytoarchitectural regions BA44 and BA45 were up to 6.6-fold larger in humans than in chimpanzees (1.3-fold and 1.4-fold larger than expected, respectively, after correcting for overall cortical enlargement) [29]. Furthermore, based on histological studies, it has been shown that Broca’s subregions BA44 and BA45 differ between humans and chimpanzees in terms of their asymmetry. Human BA45 reaches its leftward volumetric asymmetry by the age of 5 years during development. Human BA44 only reaches its asymmetry by the age of 11 years [21] when children acquire full proficiency in semantic and syntactic knowledge [30]. In contrast, in chimpanzees, neither BA44 nor BA45 develops volumetric asymmetry [29].

In the present study, we examined the phylogenetic changes of Broca’s area by comparing cytoarchitectural segmentations of BA44 and BA45 in humans and chimpanzees, derived from published histological data [21,29]. Leveraging advanced cortical registration methods [31–33], we aligned the brains of chimpanzee and human, enabling us to perform a direct comparison of the segmentations across species. Our analysis confirms that Broca’s area expanded in humans, with left BA44 being the subregion that enlarged the most. Furthermore, we show that the chimpanzee left BA44 maps to the posterior section of human BA44, a region functionally related to action, having virtually no overlap with the anterior syntax regions. Our results suggest that BA44 evolved from an action region, as found in our close living ape relatives, to a bipartite system with a posterior section recruiting action, and an independent anterior section for syntax. These findings contribute important insights regarding the longstanding debate on the (in)dependence of language and action and the evolution of Broca’s area.

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[1] Url: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3002266

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