Opinion
The battle for Broca’s region

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The intense effort to characterize Broca’s region has produced many views on its anatomy and function. Here, we present the leading approaches and consider ways to adjudicate among them empirically. Anatomically, we focus on the cytoarchitecture of Brodmann areas 44 and 45, which constitute Broca’s region. Functionally, we discuss four views: action perception, working memory, syntactic complexity and syntactic movement. We compare these views, reflect on how they can be distinguished experimentally and review relevant aphasia and functional magnetic resonance imaging (fMRI) studies. Although no single hypothesis accounts for all of the data, the role of Broca’s region in language comprehension is best explained by the syntactic movement account. This conclusion opens the door for an attempt to define general principles for the neural representation of linguistic knowledge.

Introduction

In the old days of neuropsychology, the living was easy. Functional anatomy was based on investigations with brain-damaged patients, whose lesions were identified through postmortem procedures, or later by low-resolution scans; the analysis of behavioral deficits was limited to intuitively formulated modalities that translated into simple error-inducing experiments. These days are gone. Advances in anatomy and imaging, and progress in (psycho)linguistics have brought dramatic changes to our practices.

The approaching 150th anniversary of Paul Broca’s landmark essay on the ‘seat of the faculty of language in the brain’ is a good time to take stock [1]. The intense effort to characterize the brain region named after Broca has produced a large number of experimental results and many ideas about its anatomy and function. It has also produced puzzles and debates. Here, we present the main current approaches and consider ways to adjudicate among them empirically, so that progress can be made.

Broca had several leading ideas: as a phrenologist, he believed that mental abilities are separable and that language is a special faculty – functionally individuated, neurologically distinguishable, left lateralized and localizable in a single region. Thanks to his pioneering effort, and to the work of other 19th century neurology giants (Wernicke, Lichteim, Hughlings-Jackson, and even Freud), a new functional neuroanatomy emerged, in which language was viewed as a collection of activities (speaking, listening, repetition, naming, reading and writing) that were attributed to several connected left-hemispheric loci 2, 3 (Figure 1).

The success of this model made aphasiology the flagship of a burgeoning neuropsychology. Although psycho- and neuro-linguists later refined these distinctions, to fit better what we know today about linguistic ability and functioning, the traditional view still forms the basis of the diagnostic schema featured in almost every neurology textbook 4, 5.

Below, we consider the current state of evidence concerning the linguistic functions of Broca’s region. If cognitive neuroscience is engaged (in part) in the identification of pieces of cognition with brain pieces, then we had better have a clear notion of what the pieces are (or at least of what they should be). Thus, we focus on central aspects of linguistic knowledge and practice, and their neuroanatomical substrate. Methodologically, we commend a multimodal approach, the main methods of which are reverse engineering through investigations with brain-damaged patients and activation detection through fMRI in healthy subjects. The lesion study method avails the experimenter of a relatively unconstrained testing environment, and the analysis of aberrant behavior detects functions that crucially rely on a given, albeit imprecisely described, anatomically inhomogeneous area. Functional imaging offers greater anatomical precision, yet the measurement instruments constrain testing at times, and the signal obtained indicates the participation of an area, rarely proving its crucial role in a task. We seek to combine the two approaches.

Section snippets

The anatomy of Broca’s region

Functional localization is contingent on a modular view of brain anatomy. Unless we assume that the brain is anatomically parcelated and demarcate sharp borders that delineate ‘areas’, precise functional anatomy is impossible. Brain parcelation currently relies on cytoarchitectonic border marking: the cortical ribbon exhibits ‘cytoarchitecture’ – different lamination and cell-packing density patterns at different loci. These patterns are stable, up to points of abrupt change – borders of

The functions of Broca’s region

That Broca’s region supports language processing is beyond doubt. But what exactly are its linguistic functions? To obtain an answer, we must first ask what proper linguistic functioning and subsequent successful communication presuppose. At a minimum, mastery of linguistic tools is required: knowledge of phonemes and words, and of rules governing their distribution and combination; knowledge of grammatical rules that allow their combination into phrases and sentences; knowledge of interpretive

The picture from aphasia

For over a century, researchers believed Broca’s region to be entrusted with only productive language functions, and they focused on the more noticeable aspects of the deficit in Broca’s aphasia – non-fluency, agrammatic production and repetition problems. Views diverged: some argued that Broca’s region serves grammatical functions 13, 14; others 15, 16 tended to follow Hughlings-Jackson and maintained that the proximity of Broca’s region to supplementary motor areas suggests that the language

The picture from functional magnetic resonance imaging of sentence comprehension

Broca not only pioneered reverse engineering but also dabbled in imaging. A ‘thermometric crown’ that he invented measured temperature changes at different scalp positions, which he thought would index local changes in cerebral blood flow [29]. Current imaging methods seem to have realized his vision. Positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) studies of language processing have created a rich picture, which is mostly consistent with the aphasia results.

Coda: a syntactic ‘homunculus’? Multiple brain loci for syntax

What lessons can be learned from this short tour? And what can we hope for? The neuroscience of language currently sports clearly articulated, empirically distinguishable, hypotheses. Of these, evidence suggests a highly structured role for Broca’s region in sentence analysis, favoring the SM view. However, this does not make non-linguistic results go away. Indeed, Broca’s region might be multifunctional, most notably supporting language production [38] and WM [39]. Future work might find

Acknowledgements

We are grateful to the following agencies for their continued support: Canada – SSHRC, CRC, NSERC; USA – NIH grant #DC000494; Germany – a Senior Researcher Award from the Humboldt Foundation. We would like to thank two anonymous reviewers and Katrin Amunts for their helpful comments.

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