Morphological evolution of language-relevant brain areas

Guillermo Gallardo; Cornelius Eichner; Chet C Sherwood; William D Hopkins; Alfred Anwander; Angela D Friederici

doi:10.1371/journal.pbio.3002266

. 2023 Sep 1;21(9):e3002266. doi: 10.1371/journal.pbio.3002266

Morphological evolution of language-relevant brain areas

Guillermo Gallardo ^1,^*,^#, Cornelius Eichner ^1,^#, Chet C Sherwood ², William D Hopkins ³, Alfred Anwander ¹, Angela D Friederici ¹

Editor: Simon W Townsend⁴

PMCID: PMC10501646 PMID: 37656748

Abstract

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.

What is the relationship between language and action, and do they share a common neural basis? Comparison of the cytoarchitectural subdivisions of Broca’s area in humans and chimpanzees reveals that BA44 expanded from a purely action region to a bipartite system, with an action-related posterior section and a syntax-related anterior section.

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.

Results

Symmetry of Broca’s area homolog in chimpanzee and a surface probabilistic atlas

Through a semisupervised pipeline (summarized in Fig 1A), we precisely reconstructed the cortical surface of 9 chimpanzee brains from their structural MRI data. Having their surface representation, we projected both BA44 and BA45 volumetric histological segmentations [29] to each individual surface. We examined all individuals for evidence of surface area asymmetry of both histologically defined regions (BA44 and BA45) using a Wilcoxon signed-ranks test. Although there was considerable asymmetry in some individuals (see Fig 1B), both BA44 and BA45 showed no asymmetry at the population level (BA44 T = 16, p = 0.49; BA45 T = 10, p = 0.16).

To enable comparison across subjects, we coregistered the individual brain surfaces to the surface reconstruction of the JUNA [34] chimpanzee template (see Fig 1A). On the JUNA surface, we averaged all the individual segmentations, deriving a high-quality probabilistic atlas of BA44 and BA45 homologs in the chimpanzee brain (Fig 1B). The resulting atlas is open access and available for direct download (see Data and Code Availability Statement).

Comparison between human Broca’s area and its chimpanzee homolog

Leveraging advanced surface registration [31,33], we coregistered the JUNA surface to the surface reconstruction of the MNI-2009c human template (Fig 2A) [35]. This enabled us to compare the human BA44 and BA45 histological atlases derived by Amunts and colleagues [21], with our probabilistic atlas of the chimpanzee homolog (Fig 2B).

After projecting the chimpanzee segmentations to the human brain, we computed their volumes using the MNI template’s cortical thickness. We found the projected chimpanzee BA44 to have an average size of 2,331 mm³ (SD: 789) in the left hemisphere, and 1,955 mm³ (SD: 935) in the right hemisphere. In contrast, Amunts and colleagues [21] reported the human BA44 to have an average size of 3,839 mm³ (SD: 2,277) in the left hemisphere, and 2,527 mm³ (SD: 1,597) in the right hemisphere. This means that, when scaled and projected to the same surface template, the human BA44 is 1.64 times larger in the left hemisphere than in the chimpanzee, and 1.29 times larger in the right hemisphere. Moreover, Fig 2B shows that such enlargement is likely the result of a substantial anterior expansion, not present in the right BA44.

For the chimpanzee BA45, the average size after projecting to the human brain (Fig 2B) was 3,187 mm³ (SD: 1,002) and 2,329 mm³ (SD: 1,308) for the left and right hemispheres, respectively. For the same region in humans, Amunts and colleagues [21] reported an average size of 3,242 mm³ (SD: 1,149) and 3,173 mm³ (SD: 1,637) for the left and right hemispheres, respectively. The human BA45 was only 1.02 times larger in the left hemisphere than the chimpanzee’s homolog area, while being 1.36 times larger in the right hemisphere.

Comparing the projection of chimpanzee BA44 with human functional maps

To better understand the behavioral role of the observed expansion, we computed the overlap of the projected chimpanzee BA44 with functional subdivisions of human BA44 related to action and syntax [17,36–38]. To compare only with the core chimpanzee BA44, we thresholded the projected atlas at the 0.5 level. We found that the chimpanzee BA44 overlapped most with the regions involved in action [17,36] (Figs 3, left, and S1 and Table 1). The highest overlap was found with the area Clos 4, associated with action imagination [36], of which 34% was contained by the chimpanzee’s BA44. Following this were the regions Clos 1 (26% contained, associated with phonology and overt speech tasks [36]), Clos 5 (20%, associated with phonology and semantics [36]), Papitto’s region (18%, associated with action execution/imitation [17]), and Clos 2 (7%, associated with semantics, orthography, and covert speech [36]). In contrast, the region Clos 3, associated with basic syntactic operations [36–38], had only a 3% overlap with the chimpanzee BA44. Similar results were obtained when comparing across different levels of thresholding (see S1 Fig). Finally, when visually compared, the projected chimpanzee BA44 shared spatial location and extension with the receptorarchitectural division of the human BA44 [22,23] (see S2 Fig).

Fig 3 — Action-related regions present the highest overlap with action-related areas and virtually no overlap with the syntax area. The chimpanzee BA44 atlas was thresholded at 0.5 to maintain only its core area. The functions being reported are those with the highest P (Activation | Domain) as reported by Clos and colleagues [36] and Papitto and colleagues [17], except Clos 1, which was originally reported to be a syntax area, but further studies did not find to be involved in basic syntactic operations [36,37]. The underlying data and scripts used can be found in the GitHub/Zotero repository, under the scripts/ and results/human-comparison folders.

Table 1. Anatomical overlap between functional areas [17,36] with the projected BA44 chimpanzee thresholded at 0.5.

The functional role of each area, as reported by their authors, is stated in the third column. For Clos regions, we report the functions with the highest P (Activation | Domain).

Region	Area Contained by BA44	Associated Functions
Clos 4	34%	Action Imagination
Clos 1	26%	Phonology, Syntax^*
Clos 5	20%	Phonology, Semantics
Papitto	18%	Action Execution / Imitation
Clos 2	7%	Orthography, Working Memory
Clos 3	3%	Syntax, Phonology

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*It is important to notice that, even though Clos was originally reported to be a syntax area, further studies did not find it to be involved in basic syntactic operations [37,38].

Discussion

A longstanding debate persists concerning the relationship between language and action and whether they share a common neural basis. At the center of the debate is the relationship between action and a core aspect of language, syntax. Arguments favoring and opposing their (in)dependence exist based on the structure of action and syntactic processes and the involvement of Broca’s area in both abilities. To shed light on the debate, we turned to one of our closest relatives, the chimpanzee, who have a Broca’s area homolog involved in action [4] but lack a complex syntactic language. Using robust algorithms [31,33], we aligned human and chimpanzee brains, facilitating a direct comparison of Broca’s area cytoarchitectonic subdivisions (BA44 and BA45) [21,29]. We assessed between-species differences in terms of size, symmetry, and spatial location. Furthermore, we leveraged human studies focused on action and syntactic processing to better understand the functional impact of these differences.

BA44 became increasingly left lateralized in evolution

We tested for asymmetry in surface area for both BA44 and BA45 in chimpanzee brains. Consistent with Schenker and colleagues’ [29] volumetric analysis, we found both regions to show no statistical difference in size, thus being symmetric at the population level. This result is in clear contrast with the strongly left lateralized BA44 in humans [21]. Since both chimpanzee and human segmentation were obtained through similar histological procedures, the results support the conclusion that the asymmetry of BA44 developed after humans diverged from our last common ancestor with chimpanzees.

BA44 expanded the most in humans relative to chimpanzees, extending anteriorly

We projected the BA44 and BA45 of each chimpanzee to the surface of a human cortical template and computed an average volume using the template’s cortical thickness. Assuming the MNI template is representative of the Amunts and colleagues [21] population, their reported volumes for humans are directly comparable with our scaled-up volumes for chimpanzee. Our comparison revealed that BA44 enlarged by a factor of 1.64 and 1.29 in the left and right hemispheres beyond the amount of overall cortical expansion, respectively, in this cross-species comparison. Meanwhile, BA45 enlarged only in the right hemisphere, by a factor of 1.36. Our results show that Broca’s area enlargement is remarkable in context of the evolution of human prefrontal cortex size [26,29]. Moreover, our findings suggest that BA44 became left lateralized thanks to a large anterior expansion in the left hemisphere.

The chimpanzee BA44 projects to human areas related to action, and not syntax

We compared the projected chimpanzee atlas with functional subdivisions of human Broca’s area. Our results show that the core chimpanzee BA44 overlapped solely with action-related areas, with the greatest overlap found with regions functionally associated with (in descending order) action imagination, phonology, and action execution/imitation [17,36]. Indeed, we found almost no overlap between the core BA44 chimpanzee homolog and the Broca’s subdivision involved in basic syntax operations [36–38]. Our findings were consistent across multiple levels of thresholding for the chimpanzee BA44 probabilistic map. These results indicate that a simple anatomical scale and shift of the chimpanzee Broca’s area does not explain the existence of the syntax subregion of Broca’s area in the human brain.

Cross-species differences in BA44 support a segregation of action and syntax in humans

Recent functional imaging studies found that both language and action recruit nonoverlapping subdivisions of Broca’s area in the human brain, with language being processed more anteriorly than action [17–19,36–38]. Moreover, it has been found that left BA44 segregates action and syntactic processes of language in 2 distinct subregions, with syntax recruiting its anterior part and action the posterior one [17,36–38]. This functional subdivision of human BA 44 mirrors the underlying receptorarchitectonic organization, which is a powerful indicator of functional diversity [22].

In this study, we have provided further evidence for this action/language segregation, finding that it is likely the result of an evolutionary process involving Broca’s area. By coregistering chimpanzee and human brains, we found that BA44 underwent a large expansion and left lateralization. Moreover, we found the chimpanzee BA44 maps anatomically to the posterior section of human BA44, functionally associated to action. Indeed, virtually no overlap was found between the chimpanzee BA44 and the human syntax regions. Furthermore, when visually compared, the projected chimpanzee BA44 shared spatial location and extension with the receptorarchitectonic division of human BA44. Taken together, this suggests that the left human BA44 evolved to accommodate syntax through an anterior expansion in the inferior frontal cortex.

Along with contributing to the debate on the relationship between action and language, our findings add to the broader topic of language origins. Although there is an evolutionary continuity in auditory-vocal processing and their underlying neurobiological substrate in temporo-frontal networks [39–42], functional neuroanatomical changes appear to play a crucial role during the evolution of prefrontal cortex. Functional studies indicate that when macaques process simple grammatical sequences activation of both Broca’s area and the frontal operculum is observed [43]. In contrast, human brains solely recruit the frontal operculum for simple grammars, whereas BA44 comes into play when processing complex grammatical sequences that nonhuman primates cannot process [44,45]. Thus, despite the observed similarity in the organizational principles across primates, it may have been the expansion of cytoarchitectonically defined BA44 throughout evolution that paved the way for the representation of language in the human brain.

When comparing human and chimpanzee Broca’s area, an implicit assumption is that the chimpanzee homolog can serve as a referential model to that of our shared last common ancestor. It is important to acknowledge that this is not entirely accurate, as chimpanzee brains have also certainly changed along their evolutionary lineage. Nevertheless, the limited fossil evidence from endocranial morphology suggests similarities between extant great apes and early hominins in the region of the inferior frontal gyrus, until a more pronounced “Broca’s cap” in the left hemisphere becomes evident from certain crania of the genus Homo starting at approximately 1.8 million years ago [46]. Of additional note, the anatomical coregistration method we employed cannot offer a complete answer to the exact underlying evolutionary process that Broca’s area underwent (e.g., recycling, neural reuse or cultural reuse [47–49]); for a thorough discussion, please refer to Amunts and colleagues [22]. Finally, our sample size is relatively small, meaning further cross-species comparative studies will be needed on the cytoarchitectonic and receptorarchitectonic organization of BA44 to test our conclusions.

Through a cross-species comparison, our study contributes key insights to Broca’s area reorganization and the ongoing debate on the relationship between language and action. Our findings support the interpretation that BA44 was modified from an action area, as found in nonhuman primates, to a bipartite system serving syntax anteriorly and action posteriorly. In this way, our results underline distinct neural bases for action and syntactic processes in the human brain, and thus, an independence of both cognitive domains.

Materials and methods

Ethics statement

All subjects in this study were housed in accordance with federal and state laws governing the welfare and care of nonhuman primates in the United States. All procedures were approved by the Emory University Institutional Animal Care and Use Committee (protocol #YER2000673012513). We emphasize that the collection of postmortem brains used in this study were obtained opportunistically when individuals died from natural causes or were euthanized for quality-of-life reasons.

Cytoarchitecture segmentation of Broca’s area in human brains

We downloaded the publicly available data from Amunts and colleagues [21], in which the left and right BA44 and BA45 were manually segmented on 10 subjects following histological procedures. While the individual maps are not available, the Julich institute has released the probabilistic cytoarchitectural map of both areas derived from the Amunts’ dataset.

Cytoarchitecture segmentation of Broca’s area homolog in chimpanzee brains

Our chimpanzee cytoarchitectural data come from a previous study [29], in which both BA44 and BA45 were bilaterally delineated and guided by the same cytoarchitectonic criteria used in the human maps [21]. Whole-brain MRI data were acquired ex vivo for all chimpanzees (see S1 Supplementary Methods). From the population of 12 chimpanzees, we discarded 3 based on inadequate corresponding MRI data quality, retaining 9 subjects (Pan troglodytes, 5/4 males/females, age = 32.8 ± 11.8 years, age range = 12 to 44.5 years). The demographics of the included chimpanzees are summarized in S1 Table. For additional information on the data acquisition, please refer to the original publication [29].

Broca’s homolog in chimpanzees: Deriving a probabilistic atlas and studying population symmetry

We derived a probabilistic atlas of Broca’s area homolog from the individual cytoarchitectonic segmentations of BA44 and BA45 and their associated ex vivo MRI scans. We performed all the analysis on the reconstructed cortical surfaces, as surface analysis better captures and aligns brains based on their gyrification, thus being more robust than volumetric analysis [50].

The procedure can be summarized in 5 steps: (I) reconstruct 3D brain surfaces from the ex vivo MRI scans using FreeSurfer; (II) project each chimpanzee’s BA44 and BA45 volumetric segmentation to their corresponding surfaces; (III) register all surfaces to a common template, namely, the JUNA chimpanzee brain template [34]; (IV) map the individual cytoarchitectural regions to the JUNA template; and (V) aggregate them to derive a high-quality probabilistic atlas. See Fig 1A for a graphical explanation and S1 Supplementary Methods for a detailed explanation of each step. The processing scripts for the computation of the open access atlas are readily available for download (see Data and Code Availability Statement).

We further leveraged the individual reconstructions to study the surface-area asymmetry of Broca’s homolog in chimpanzee brains. For this, we computed the areas of BA44 and BA45 on each individual chimpanzee and tested their bilateral symmetry through a Wilcoxon signed-ranks test.

Mapping chimpanzee cytoarchitectural maps to the human brain

To enable cross-species comparison, we aligned the cortical reconstruction of JUNA template [34] to that of the human MNI template (ICBM152 9c Asymmetric) [35]. Given the differences in brain shape and volume, we opted to use surface-based registration algorithms, which have been proven successful in aligning the brains of chimpanzees and humans [33].

Based on the work of Eichert and colleagues [33], we performed the surface-based registration in 2 stages. In the first stage, we performed a first alignment of the brain templates using gross anatomical regions. Specifically, we aligned the brains based on their inferior frontal gyrus, as defined by the Desikan atlas (Fig 2A) [51]. Starting from that rough alignment, we then carried a more granular registration based on the sulcal patterns. For a detailed explanation of each stage, please refer to S1 Supplementary Methods as well as the open access processing script (see Data and Code Availability Statement).

Expansion of BA44 and BA45 in humans relative to chimpanzees

In their histological study, Amunts and colleagues [21] report the average gray matter volume for human BA44 and BA45. Since our chimpanzee regions stem from similar histological procedures, we can study how much BA44 and BA45 expanded through evolution by mapping them to a common space and by comparing their size across species.

Having morphed chimpanzee BA44 and BA45 to the human template, we computed their individual volumes using the MNI template cortical thickness. In this way, we obtained volumes for chimpanzee Broca’s area subregions that are scaled up and projected onto the template human cortical surface. Assuming the MNI template is representative of the Amunts and colleagues [21] population, their reported volumes for humans are directly comparable with our scaled-up volumes for chimpanzee.

Functional aspects of the BA44 homolog in the human brain

We aimed to understand the relation between function and the location of the projected chimpanzee Broca’s area homolog—with a particular interest in language and action. For this, we projected the functional subdivisions of human BA44 defined by Papitto and colleagues [17] and Clos and colleagues [36] to the MNI cortical surfaces. There, we compared them to the core chimpanzee BA44, obtained by thresholding the atlas at the 0.5 level, i.e., the points in the surface where the majority of the chimpanzee population had their BA44 located. Particularly, for each functional region, we computed their overlap with the chimpanzee BA44, defined as how much of the functional area was contained by the chimpanzee BA44. We further visually compared our projected chimpanzee BA44 with an existing receptorarchitectonic division of BA44 [23]. The comparison had to be carried out visually since no volumetric nor surface data are publicly available.

Supporting information

S1 Table. Demographics of the included subjects.

(DOCX)

Click here for additional data file.^{(12.7KB, docx)}

S1 Fig. Comparing the overlap of Functional Subdivisions of the Human BA44 and the Chimpanzee BA44 Probabilistic Atlas at different levels of threshold.

Notice that only the probabilistic atlas is being thresholded. As expected, the overlap decreases as the area of BA44 shrinks (the threshold increases). For all threshold levels, the least overlapping region is the syntax-related area Clos 3. The data and plotting script can be found on the GitHub/Zotero repository, under the scripts/human-space folder.

(EPS)

Click here for additional data file.^{(98.4KB, eps)}

S2 Fig. Visual comparison between our derived atlases for BA44 and the receptorarchitectonic parcellation from Amunts and colleagues [22].

Left: Receptorarchitectonic areas projected to the lateral surface of an individual postmortem brain as depicted in Amunts and colleagues [22]. Right: Human and chimpanzee BA44 [21,29] projected into the human template surface. By visual comparison, 44v shares location and extension with the projected chimpanzee BA44. No volumetric or surface data are publicly available, for which only a visual comparison is possible. Please notice that the diagonal sulcus (ds) from the individual brain (Left) corresponds to the ascending branch of the Sylvian fissure in the MNI template (Right) as shown by Sprung-Much and Petrides [52]. The human and chimpanzee data can be found in the GitHub/Zotero repository, under the results/human-comparison folder.

(EPS)

Click here for additional data file.^{(1.3MB, eps)}

S1 Supplementary Methods. Chimpanzee data.

(DOCX)

Click here for additional data file.^{(43.9KB, docx)}

Acknowledgments

We thank Hannah Gerbeth for her help during the FreeSurfer white matter segmentation.

Data Availability

The probabilistic chimpanzee atlases of BA44 and 45, alongside the respective processing scripts used to generate them are publicly available for download in our repository: https://github.com/gagdiez/chimpanzee-broca. An archived version of this data can be found through Zenodo: https://zenodo.org/record/8154437.

Funding Statement

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.

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PLoS Biol. doi: 10.1371/journal.pbio.3002266.r001

Decision Letter 0

Kris Dickson, PhD

7 Feb 2023

Dear Dr Gallardo,

Thank you for submitting your manuscript entitled "Uncovering the Morphological Evolution of Language-Relevant Brain Areas" for consideration as a Short Reports by PLOS Biology.

Your manuscript has now been evaluated by the PLOS Biology editorial staff, as well two academic editors with relevant expertise. I am writing to let you know that we would like to send your submission out for external peer review, and apologize for the delay in getting this feedback to you. One of our academic editors came down with a cold which delayed our discussion a bit.

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PLoS Biol. doi: 10.1371/journal.pbio.3002266.r002

Decision Letter 1

Paula Jauregui, PhD

29 Mar 2023

Dear Dr. Gallardo,

Thank you for your patience while your manuscript "Uncovering the Morphological Evolution of Language-Relevant Brain Areas" was peer-reviewed at PLOS Biology. It has now been evaluated by the PLOS Biology editors, an Academic Editor with relevant expertise, and by several independent reviewers.

In light of the reviews, which you will find at the end of this email, we would like to invite you to revise the work to thoroughly address the reviewers' reports.

As you will see, all the reviewers agree that you should tone down the strength of your claims and better develop your arguments (also incorporating additional monkey data/findings). We think that it is important that you address the comments of reviewer #3 who highlights some key issues in your conclusions related to i) potentially secondary loss of the division of BA44 concerned with syntax (at least as an alternative evolutionary scenario to be discussed), but critically ii) the fact that, since chimpanzees do not have language-related areas to map (given they lack language per se) it is not really possible to find any other result than chimpanzee action-related brain areas mapping onto human brain areas. Specifically, as also noted by reviewer #3 we think it is also important to discuss what potential result could lead to the opposite conclusion than that you currently reached. Please also address the rest of the reviewers' issues.

Given the extent of revision needed, we cannot make a decision about publication until we have seen the revised manuscript and your response to the reviewers' comments. Your revised manuscript is likely to be sent for further evaluation by all or a subset of the reviewers.

We expect to receive your revised manuscript within 3 months. Please email us (plosbiology@plos.org) if you have any questions or concerns, or would like to request an extension.

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Thank you again for your submission to our journal. We hope that our editorial process has been constructive thus far, and we welcome your feedback at any time. Please don't hesitate to contact us if you have any questions or comments.

Sincerely,

Paula

---

Paula Jauregui, PhD,

Senior Editor

PLOS Biology

pjaureguionieva@plos.org

------------------------------------

REVIEWS:

Reviewer #1: This is very interesting Report, focusing on a key question in the evolution of (neurobiological bases of) language (the relationship between action and syntax), and on an area of the brain that is central to the language circuit ("Broca's region", and in particular BA44).

The authors rely on histological data and cortical registration methods to offer a close comparison of the morphology of BA44 and 45 between humans and chimpanzees

Their main result is that "the left human BA44 evolved to accommodate syntax through an anterior expansion of action-related regions in the inferior frontal cortex"

This is a claim that is sure to trigger a lot of discussion. The evidence provided will likely be closely examined by proponents of different scenarios for the evolution of syntax. It constitutes a genuine novel finding, in my opnion. I am therefore happy to recommend publication.

My only concern pertains to the rather generic use of the term "syntax" throughout the manuscript. As the authors are aware, "syntax" likely consists o multiple subcomponents/traits, and these are likely to be distributed across the brain. This, of course, does not diminish the role of BA44 is core aspects of syntax, but it may require a bit more qualification.

I also think that the results presented in this Report are unlikely to "provide a solution for the long- standing debate concerning the structural and functional evolution of Broca's area and its role in action and language". Proponents of the view that syntax evolved out of an Action Grammar capacity are likely to take these results to be evidence for a duplication-and-divergence model (evolutionary continuity as opposed to 'novelty'). I leave it to the authors to decide if their claim should be qualified. I don't feel I should insist on this modification. I think that the results are worthy of publicaion in PLoS Biology as they are, and whatever conceptual position the authors adopt will be adequate, as it sure will fuel discussion in the future.

Reviewer #2: In their work, Gallardo and colleagues examine the evolution of Broca's area by comparing the cytoarchitectonic segmentations of BA44 and BA45 in humans and chimpanzees.

They reconstructed the cortical surface of nine chimpanzee brains using MRI data and aligned brains from chimpanzees and humans to perform a direct comparison of segmentations between the species. They found no BA45 asymmetry at chimpanzee level unlike for humans. Furthermore, they showed an expansion of Broca's areas in humans, with the left BA44 being the most enlarged. The authors conclude that BA44 in humans has evolved from a purely action-related region to a more comprehensive region, with a posterior region that supports action and an anterior region that processes syntax.

The results are novel and will potentially advance our understanding of the evolution of Broca's area in the primate lineage. The study is methodologically sound, and the number of animals used is sufficient for a study with non-human primates. I have only one major concern regarding the overall approach that the authors should consider in their revision.

1. The authors strongly suggest that their data will help improve our understanding of the evolution of Broca's area in humans. Here, they argue that Broca's area may have evolved continuously from precursor structures in the primate lineage. However, to be truly convincing here, it would be essential to go back another step in evolution and look at the morphology of the monkey homolog of Broca's area. This is particularly suggested by the fact that there are a large number of studies present showing morphological and physiological similarities between the macaque monkey homolog and the human Broca's area (notably the extensive work by Pandya and Petrides, but also others). In addition, there are already several reviews addressing the evolution of Broca's area in the primate lineage. I strongly recommend that the authors consider the monkey data and incorporate and discuss the existing review articles accordingly.

Reviewer #3: This short report presents a comparative analysis of human BA44/45 and their chimpanzee homologues in which they probe a hypothetical allometric expansion of these areas in humans vs chimpanzees. The principal result is that the anterior division of the area referred to as "Broca's region" in humans shows a 'disproportionately' great expansion vis-a-vis the right homologue and the more posterior subregion. The methods appear solid, the data and methods are available. The statistical analyses are acceptable. The findings are novel but their importance currently seems over-stated. The rationale for the study is that there are two opposing views on the emergence of language, either from action or independently of it. A key reference is not cited: Zilles & Amunts (2018) discuss comparisons between human and non-human primate LIFG anatomy and this work should be considered, and possibly foregrounded (especially given that it explicitly calls for a comparison between human and chimpanzee neuroanatomy) in the introduction.

They authors make the bold claim that this:

i. Shows that BA44 "evolved from a purely action-related region"

ii. Solves a longstanding debate regarding the structural and functional evolution of Broca's area and its role in action and language

It is unclear how looking at anthropoid primates can "settle the debate". The neural basis of action and language in humans is already known (characterised to some extent, even if not completely described), it is not by examining non-human primates that these can be better elucidated.

The assertion that the manuscript provides "a complete picture of Broca's area evolution and … solution to the longstanding debate of BA44's role in language and action" is not well supported. The comparisons presented could not provide a full picture (but nor would they strictly need to), and moreover the function of human BA44 in language and action can only be established by studying humans. Mapping cytoarchitectonic homologues does not itself demonstrate any particular functional role and drawing inferences about the presumed functional drift of a region over evolution requires more convincing argumentation.

If I have understood the argumentation correctly, the authors suggest that because chimpanzee BA44 maps onto only a small, posterior portion of human BA44, human BA44 has undergone an anterior expansion since the LCA with chimpanzees. This seems to depend upon an assumption that the human BA44 is a cytoarchitectonically homogeneous region. Since anterior BA44 (loosely) tends to be found to process syntax, the assumption is that the "syntax part" is derived from the "action part". This result supposedly answers the question of whether the syntax processing region in anterior BA44 evolved from action processing, and not independently. This could be a relatively compelling argument, and certainly fits with a prevailing view (as described int he introduction), but it is need of additional support.

On the basis of the evidence presented it would be equally possible to claim (albeit perversely) that chimpanzee BA44 evolved from a region that supported both syntactic and action processing and lost the division concerned with syntax. It seems important to consider that chimpanzees are not the human/chimpanzee LCA - and that they have presumably also been undergoing evolutionary changes over the past 5-10million years.

Anderson (2010) proposes neural reuse as a mechanism whereby a cytoarchitectonically homologous region of human and non-human cortex could become functionally differentiated. Some kind of argumentation along these lines (or any theory the authors favour) is required to help lend credibility to the proposals.

I feel that there is a flaw in the current set-up of the study, but this may be a misunderstanding arising due to the density of the manuscript. Given the widely accepted assumption that chimpanzees have no language (as defined by the authors), it would be impossible for any result to arise other than one showing that chimpanzee action-related brain areas map onto human brain areas (as there are no chimpanzee language-related areas to map). It would therefore seem impossible for the authors to test the hypothesis that language arose independently of action using this method. Even if Chimpanzee BA44 mapped directly onto human BA44, this would provide evidence for or against - it would merely indicate that some functional modification of a previously homologous region must have taken place. In the present case it is hypothesised that there was an expansion, but if that expansion could only be found to have arisen from a region that is characterised in chimpanzees and therefore non-linguistic, it does not seem that the debate has been solved. If this is not the case, it would be very important to discuss which result would lead to the opposite conclusion. Mapping cytoarchitectonic probability maps from one atlas to another using the methods employed here could never lead to the discovery of an area in one species that does not map onto some region of the other.

Thus, the results regarding the extent of allometric expansion and the asymmetry are themselves compelling, but the interpretation is pushed too far.

To sum up - I am not opposed to the authors' position that language conceivably arises on the basis of action systems. However I do not believe that the present paper demonstrates this as conclusively as claimed. The pattern of allometric expansion from chimpanzee to human with a greater expansion in the left than right hemisphere and a greater expansion in BA44 than 45 is extremely intriguing and these analyses are of interest to the community of researchers concerned with the evolution of the neurobiological bases of language. However the argumentation is under-developed, limitations and fundamental assumptions relevant to the approach are not really discussed and there is no convincing control analysis that can help to support that the pattern of results is related to language specifically. My recommendation is therefore for substantial modification to the introduction and discussion to justify the approach and the strength of the claims.

PLoS Biol. 2023 Sep 1;21(9):e3002266. doi: 10.1371/journal.pbio.3002266.r003

Author response to Decision Letter 1

2 Jun 2023

Attachment

Submitted filename: Response to Reviewers.docx

Click here for additional data file.^{(31.4KB, docx)}

PLoS Biol. doi: 10.1371/journal.pbio.3002266.r004

Decision Letter 2

Paula Jauregui, PhD

5 Jul 2023

Dear Dr. Gallardo,

Thank you for your patience while we considered your revised manuscript "Uncovering the Morphological Evolution of Language-Relevant Brain Areas" for publication as a Short Reports at PLOS Biology. This revised version of your manuscript has been evaluated by the PLOS Biology editors, the Academic Editor, and the original reviewers.

Based on the reviews, we are likely to accept this manuscript for publication, provided you satisfactorily address the remaining points raised by the reviewers. Please also make sure to address the following data and other policy-related requests.

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3. We suggest a change in the title: "Part of the human language-relevant brain region Broca's area evolved from an action-related area in non-human primates".

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Reviewer remarks:

Reviewer #1: I am grateful to the authors for taking my comments into consideration. I am particularly pleased with the fact they decided to tone down their conclusions. I endorse publication.

Reviewer #2: The authors have done a good job revising their paper and toning down the impact of some of their findings. However, my major concern has not been adequately addressed.

I agree with the authors that additional studies on cytoarchitecture and connections in apes will help to learn more about the evolution of Broca's area. However, to fully understand the evolution, we also critically rely on neurophysiological data in our closest relatives, and for these invasive experiments we rely on monkeys. Although more distantly related to humans than apes, the similarities are striking, as demonstrated in the extensive work of Petrides and discussed in several reviews in recent years (e.g., Fröhlich et al. 2019 Biol Rev; Rauschecker 2018 Curr Opin Behav Sci; Aboitiz 2018 Front Neurosci; Hage & Nieder 2016 TINS). Moreover, several laboratories have recorded neural activity from ventrolateral prefrontal areas in monkeys showing similar activity patterns before and during vocal output as in human Broca's area before and during human speech signals. Therefore, I would like to emphasize again how important it would be to consider the abundant data on cortical control mechanisms available from the monkey studies, at least in the discussion. This inclusion would increase the impact of the manuscript, which is crucial, especially considering that the paper has lost impact due to the necessary toning down of the results.

Reviewer #3: I enjoyed reading the revised manuscript and feel that the authors' substantial and considered modifications have improved the work. They have addressed my preceding concerns and I wish to express my appreciation of their efforts to address them. I have no further comments.

PLoS Biol. 2023 Sep 1;21(9):e3002266. doi: 10.1371/journal.pbio.3002266.r005

Author response to Decision Letter 2

18 Jul 2023

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PLoS Biol. doi: 10.1371/journal.pbio.3002266.r006

Decision Letter 3

Paula Jauregui, PhD

21 Jul 2023

Dear Dr. Gallardo,

Thank you for the submission of your revised Short Reports "Uncovering the Morphological Evolution of Broca’s area: A Comparison of Human and Chimpanzee Brains" for publication in PLOS Biology. On behalf of my colleagues and the Academic Editor, Simon Townsend, I am pleased to say that we can in principle accept your manuscript for publication, provided you address any remaining formatting and reporting issues. These will be detailed in an email you should receive within 2-3 business days from our colleagues in the journal operations team; no action is required from you until then. Please note that we will not be able to formally accept your manuscript and schedule it for publication until you have completed any requested changes.

We suggest a change in the title to improve readability and accessibility: "Morphological evolution of the human language-relevant area of Broca in comparison with the chimpanzee brain" or "Morphological evolution of language-relevant brain areas".

The academic editor also suggests a couple of edits (in capital letters) that you could change along with the title and the requests from the journal operations team:

1. Change "during the evolution of THE prefrontal cortex"

2. Change to: "In contrast, human brains solely recruit the frontal operculum for simple grammars, whereas BA44 comes into play when processing MORE complex grammatical sequences which non-human primates HAVE BEEN ARGUED TO BE unable to process [44,45].

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Sincerely,

Paula

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 Table. Demographics of the included subjects.

(DOCX)

Click here for additional data file.^{(12.7KB, docx)}

S1 Fig. Comparing the overlap of Functional Subdivisions of the Human BA44 and the Chimpanzee BA44 Probabilistic Atlas at different levels of threshold.

(EPS)

Click here for additional data file.^{(98.4KB, eps)}

S2 Fig. Visual comparison between our derived atlases for BA44 and the receptorarchitectonic parcellation from Amunts and colleagues [22].

(EPS)

Click here for additional data file.^{(1.3MB, eps)}

S1 Supplementary Methods. Chimpanzee data.

(DOCX)

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Click here for additional data file.^{(30.6KB, docx)}

Data Availability Statement

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PERMALINK

Morphological evolution of language-relevant brain areas

Guillermo Gallardo

Cornelius Eichner

Chet C Sherwood

William D Hopkins

Alfred Anwander

Angela D Friederici

Roles

Abstract

Introduction

Results

Symmetry of Broca’s area homolog in chimpanzee and a surface probabilistic atlas

Fig 1.

Comparison between human Broca’s area and its chimpanzee homolog

Fig 2.

Comparing the projection of chimpanzee BA44 with human functional maps

Fig 3. Percentage of overlap between the chimpanzee BA44 and functional subdivisions of the human BA44 [17,36–38].

Table 1. Anatomical overlap between functional areas [17,36] with the projected BA44 chimpanzee thresholded at 0.5.

Discussion

BA44 became increasingly left lateralized in evolution

BA44 expanded the most in humans relative to chimpanzees, extending anteriorly

The chimpanzee BA44 projects to human areas related to action, and not syntax

Cross-species differences in BA44 support a segregation of action and syntax in humans

Materials and methods

Ethics statement

Cytoarchitecture segmentation of Broca’s area in human brains

Cytoarchitecture segmentation of Broca’s area homolog in chimpanzee brains

Broca’s homolog in chimpanzees: Deriving a probabilistic atlas and studying population symmetry

Mapping chimpanzee cytoarchitectural maps to the human brain

Expansion of BA44 and BA45 in humans relative to chimpanzees

Functional aspects of the BA44 homolog in the human brain

Supporting information

Acknowledgments

Data Availability

Funding Statement

References

Decision Letter 0

Kris Dickson, PhD

Roles

Decision Letter 1

Paula Jauregui, PhD

Roles

Author response to Decision Letter 1

Decision Letter 2

Paula Jauregui, PhD

Roles

Author response to Decision Letter 2

Decision Letter 3

Paula Jauregui, PhD

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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