Asymmetric Broca's area in great apes

Abstract

Brodmann's area 44 delineates part of Broca's area within the inferior frontal gyrus of the human brain and is a critical region for speech production 1,2 , being larger in the left hemisphere than in the right 1-4 -an asymmetry that has been correlated with language dominance 2,3 . Here we show that there is a similar asymmetry in this area, also with left-hemisphere dominance, in three great ape species (Pan troglodytes, Pan paniscus and Gorilla gorilla). Our findings suggest that the neuroanatomical substrates for left-hemisphere dominance in speech production were evident at least five million years ago and are not unique to hominid evolution.To our knowledge, no one has assessed whether there is any consistent left-right anatomical asymmetry in the inferior frontal gyrus (IFG) of any non-human primate. This is surprising because it is known from cytoarchitectonic and electrical stimulation studies that many nonhuman primates, including the great apes 5,6 , possess a homologue of area 44. We have therefore investigated whether homologous neuro-anatomical asymmetries are present in area 44 in great apes.From magnetic resonance images (MRI) obtained from 20 chimpanzees (P. troglodytes), 5 bonobos (P. paniscus) and 2 gorillas (G. gorilla; Fig. 1a), we found that area 44 in these species shows a pattern of morphological asymmetry that has left-hemisphere surface-area predominance similar to the homologous cortical area of humans (mean left, 127.7 mm 2 ±8.1 s.e.; mean right, 104.2 mm 2 ±6.1 s.e.; F(1,25) = 7.45, P=0.011; see supplementary information for details of the statistical analysis, and see Fig. 1b for individual asymmetry measures). In humans, this region is part of Broca's area, a key anatomical substrate for speech functions, particularly in motor aspects of speech such as articulation and fluency 2,7 .The part possession by great apes of a homologue of Broca's area is puzzling, particularly considering the discrepancy between sophisticated human speech and the primitive vocalizations of great apes. This may be explained by the contribution that gestures have made to the evolution of human language and speech 8 . In monkeys, the so-called 'mirror neurons' in area 44 seem to subserve the imitation of hand grasping and manipulation, and this neural system may have been specialized initially for gestural and later for vocal communication 9 . In captive great apes, manual gestures are both referential and intentional 10,11 , and are preferentially produced by the right hand (which is controlled by the left hemisphere). This right-hand bias is consistently greater when gesturing is accompanied by vocalization 10 .From an evolutionary standpoint, therefore, asymmetry in area 44 may be associated with the production of gestures accompanied by vocalizations in great apes, an ability that eventually Supplementary information accompanies this communication on Nature's website (www.nature.com).

Language in shadow

“…This possibility finds further support from a recent experiment based on the analysis of brain MRIs of three great ape species (Pan troglodytes, Pan paniscus and Gorilla gorilla) showing that the extension of BA 44 is larger in the left hemisphere than in the right. While a similar asymmetry in humans has been correlated with language dominance (Cantalupo & Hopkins, 2001), this hypothesis does not fit in the case of apes. It might be, however, indicative of an initial specialization of BA 44 for communication.…”

Wernicke's area homologue in chimpanzees (Pan troglodytes) and its relation to the appearance of modern human language

“…In humans, the leftward asymmetry in the planum temporale has been one of the most consistent asymmetries reported in the human brain (Beaton 1997;Shapleske et al 1999), whereas reports of population-level asymmetries in the frontal operculum have been far less consistent across studies (Keller et al 2007(Keller et al , 2009. Similarly, in chimpanzees, postmortem and in vivo analysis of the planum temporale have revealed significant leftward asymmetries (Hopkins & Nir in press) but this is less clear for the inferior frontal gyrus (Cantalupo & Hopkins 2001;Hopkins et al 2008;Keller et al 2009;Schenker et al 2010) and appears to depend on the landmarks used to define the region-of-interest as well as other factors.…”

“…In particular, gross structural asymmetries have been observed in non-human primates, including chimpanzees, for homologues of areas implicated in human language and speech production (e.g. Gannon et al 1998;Cantalupo & Hopkins 2001;Hopkins 2007). …”

Cerebral Asymmetry: A Quantitative, Multifactorial, and Plastic Brain Phenotype

“…The planum temporale displays pronounced leftward asymmetry in most humans. Early studies reported that this feature was also present -although to a lower degree -in chimpanzees and other great apes (Cantalupo & Hopkins, 2001). Later, Taglialatela et al (2008) discovered that Broca's area homolog activates in chimpanzee brains when they communicate with gestures or vocalizations, which led to the theory that enlargement of Broca's area, and its role in communication, began before the evolutionary split between humans and chimpanzees.…”