ReviewBroca’s area: Nomenclature, anatomy, typology and asymmetry
Introduction
The anatomist, anthropologist and surgeon Paul Broca is widely regarded as the founding father of functional localisation in the human brain, despite the significant contributions of Gall, Dax and Bouillard who predated Broca (Finger & Roe, 1999). Although he made many contributions to the understanding of functional neuroanatomy and aphasia, his most notable contribution was to associate disturbances of speech production with lesions to the left lateral frontal lobe, citing the importance of the third frontal convolution (Broca, 1861a, Broca, 1861b, Broca, 1863, Broca, 1865). This brain region was among the first areas of brain tissue to which a circumscribed function – articulate language – was specifically related (Amunts & Grodzinsky, 2006). Over a century of research has confirmed and developed many of the ideas Broca outlined in his original manuscripts. The functional (i.e. neuroimaging) and clinical (i.e. lesion) literature building on Broca’s work gave rise to the idea that structural cerebral asymmetry of the region Broca described as crucial for language expression may underlie the more obvious functional asymmetry of this region comparable to the hypothesised association between lateralised speech perception and asymmetry of the planum temporale (Galaburda, 1993, Galaburda and Geschwind, 1980, Galaburda, LeMay et al., 1978, Galaburda, Sanides et al., 1978, Geschwind, 1970, Geschwind, 1972a, Geschwind, 1972b, Geschwind, 1978, Geschwind, 1984, Geschwind and Galaburda, 1985a, Geschwind and Galaburda, 1985b, Geschwind and Galaburda, 1985c, Geschwind and Levitsky, 1968). Given the predominantly leftward lateralised language functions in the human brain, many have sought to demonstrate a leftward morphological asymmetry of Broca’s area.
In a recent review of cerebral asymmetry of the human brain it was stated that “Broca’s speech area is larger in volume than its homologue in the right hemisphere” (Toga & Thompson, 2003, p. 39). Citing two studies in support, the first a cytoarchitectonic analysis of area 44 and area 45 in 10 human brains (Amunts et al., 1999), the second a post-mortem study of the inferior frontal gyrus in 12 human brains (Falzi, Perrone, & Vignolo, 1982), Toga and Thompson (2003) dedicated no more text to this region of the brain. Similarly in a review in Nature, Carroll (2003) stated that “Broca’s area ... is larger in the left hemisphere of the (human) brain than in the right, an asymmetry that has been correlated with language ability.” (p. 851), without supportive evidence. Cantalupo and Hopkins (2001) claimed an “Asymmetric Broca’s area in the Great Apes” under the assumption that a leftward asymmetry exists in the human brain.
It has often been assumed that structural asymmetry is the basis of hemispheric dominance for language, and that the assumed leftward asymmetry of Broca’s area in part underlies this functional dominance. However, there is no complete consensus as to what constitutes Broca’s area anatomically, and as we will describe, the cortical region arbitrarily defined as Broca’s area is not robustly leftwardly asymmetric. This conclusion echo’s the earlier comment of Witelson and Kigar (1988) that “... there is no evidence of a statistically larger left than right ‘Broca’ region. This is in contrast to frequent references to the contrary in the literature” (p. 125).
Building on the Witelson and Kigar review, the present manuscript reviews subsequent evidence for and against a structural asymmetry of Broca’s area in the human brain, and
- (i)
Discusses how the term ‘Broca’s area’ has become disassociated from the cerebral damage causing Broca’s aphasia.
- (ii)
Describes in detail how the gross anatomy of Broca’s area varies between people, and how the definitions vary between studies.
- (iii)
Attempts to reconcile the findings of structural asymmetry of Broca’s area with the differences in methodological approaches.
- (iv)
Considers the functional significance of cytoarchitectonic definitions of Broca’s area.
- (v)
Critically considers the significance of circumscribed regions of cortex for language lateralisation and language development.
Section snippets
Nomenclature
In 1861, Paul Broca presented behavioural and neuropathological data to the Anthropological Society of Paris of a 51 year old male who had a severe disturbance in spoken language, whilst other mental faculties remained as far as could be determined intact (Broca, 1861b) (translated and reproduced in Broca, 2006).
Gross anatomy
Paul Broca described the posterior third frontal convolution – hereon referred to as the inferior frontal gyrus – as most crucial for the expression of speech. The majority of studies limit the definition of Broca’s area to the sulcal contours defining the inferior frontal gyrus (Albanese et al., 1989, Falzi et al., 1982, Foundas et al., 1996, Foundas et al., 1995, Foundas, Weisberg et al., 2001, Galaburda, 1980, Keller, Highley et al., 2007, Knaus et al., 2006, Knaus et al., 2007, Petrides,
Cytoarchitectonics
Paul Broca’s definition of the cerebral region most crucial for expressive language was based on the gyral convolutions of the brain. Broca’s macroscopic observations preceded the cytoarchitectonic and myeloarchitectonic maps of the human brain of the early 20th century, which suggested that Broca’s area could be defined on a microscopic basis, given that changes in the laminar distribution of neuronal cell bodies and myelinated fibres could define cytoarchitectonic areas in the cerebral
Putting asymmetry of Broca’s area into context
Three issues arise.
Concluding remarks
In March 2000, 140 years after Paul Broca presented his data on Leborgne to the Anthropological Society of Paris, Chris McManus stated that the literature on cerebral asymmetry generally consists of many artefacts and bias, and that a review of this data on asymmetry has to be treated with caution, particularly as the reporting of asymmetries is desirable whereas the reporting of symmetries are not. When questioned in response to this statement “What can we reasonably not doubt?”, McManus
Acknowledgements
This work was supported by a European Commission Grant from the Sixth Framework Programme entitled ‘Paul Broca II – The Evolution of Cerebral Asymmetry in Homo Sapiens’ Project no. 12880.
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