Home » Neurology » From Broca’s area to Broca’s aphasia: a tale of two eponyms

From Broca’s area to Broca’s aphasia: a tale of two eponyms

The definitive version of this post was originally published on May 27, 2015 on the PLOS Neuroscience Community website, where I serve as an editor.


In 1861, the French scientific journal Bulletin de la Societe Anatomique published an article that would prove immeasurably important to the study of language and of the human brain [1]. The article described M. Leborgne, a middle-aged patient who had suffered for the past 20 years from a striking inability to speak; so much so that he had become known as “Tan”, after the only syllable that he could utter. Leborgne had the misfortune to die soon afterwards, and the physician who had taken care of him in his last days performed an autopsy and collected the brain. What he found almost definitively established the notion of the cerebral localization of cognitive functions: Leborgne’s brain bore a single lesion in the inferior part of the left frontal lobe. Thus, focal and circumscribed brain damage was responsible for Leborgne’s loss of the ability to speak. The features of Leborgne’s speech impairment and the damaged area of his brain both came to bear the name of the physician who reported on his plight: Paul Broca.

The area and the syndrome do not match

Today, Broca’s area refers to the posterior portion of the inferior frontal gyrus on the left cerebral hemisphere, and Broca’s aphasia to an acquired alteration of spoken and written language that includes problems with speech fluency, word finding, repetition, and the ability to construct and understand grammatically complex sentences: patients suffering from Broca’s aphasia have a hard time getting words out and speak in short and hesitant sentences, sometimes called telegraphic speech. But the careful observation of numerous patients led many physicians and scientists to question the existence of an exclusive and absolute link between the two eponyms: there are patients whose Broca’s area is damaged, yet whose speech does not resemble that of Leborgne, and can even be almost normal; conversely, some patients speak like Leborgne after brain damage that does not involve the inferior frontal gyrus. How can one determine the precise role of Broca’s area given this discrepancy?

The rise of functional neuroimaging and neurophysiology affords another approach: rather than study patients whose brain is damaged or whose speech is abnormal, functional studies would measure the brain activity of healthy people while they speak. The question then becomes: what aspects of speech production—from conceptualizing a word to selecting its correct grammatical form to translating it into syllables to preparing the motor commands that would produce those syllables to finally executing the motor commands and speak—are under the control of Broca’s area? Unfortunately, technicalities got in the way: the phenomenon of speech production unfolds rather quickly in time, over a few hundreds of milliseconds, far beyond the temporal resolution of functional magnetic resonance imaging, which generally produces only about one “brain map” per second. On the other hand, several brain areas involved in speech production sit next to each other in the brain, which makes them impossible to resolve using electroencephalography and magnetoencephalography, despite the millisecond temporal resolution of those methods.

Probing the human brain’s function from within

If functional MRI is too slow and EEG is too blurry, would it mean that studying brain function during the production of normal speech is altogether impossible? Not quite: there are situations when medical conditions such as brain tumors or epilepsy dictate the placing of electrodes directly in contact with the human brain. These electrodes have the same millisecond temporal resolution as EEG, but with a spatial resolution and specificity that rivals that of functional MRI. In other words, they provide a uniquely detailed window onto the human brain’s functions. Neuroscientific research using intracranial electrodes is made possible thanks to the extraordinary generosity of the patients who agree to participate in extra tests and experiments despite the fact that they have just undergone a significant neurosurgical procedure.

A grid of intracranial electrodes is placed over the surface of the cerebral cortex (source: Electrocorticography. Wikipedia. Retrieved April 12, 2015).

A grid of intracranial electrodes is placed over the surface of the cerebral cortex (source: Electrocorticography. Wikipedia. Retrieved April 12, 2015).

In a study recently published in the Proceedings of the National Academy of Sciences, Dr. Adeen Flinker and colleagues, from the University of California, Berkeley and the Johns Hopkins University in Baltimore, used intracranial electrodes to reexamine the role of Broca’s area in speech production [2]. They studied seven patients whose epilepsy could not be controlled by drugs and who were candidates for surgical removal of the epileptic focus in their brain. In these patients, the intracranial electrodes were necessary both to determine the exact origin of the seizures, and also to map cortical functions in order to spare areas essential for speech. Dr. Flinker asked the patients to repeat out loud words that they had just heard or read while he measured with millisecond precision neural activity in Broca’s area as well as in the motor cortex that ultimately controls the movements of the tongue and mouth, further back on the surface of the frontal lobe, and in parts of the temporal lobe important for hearing and the comprehension of language.

Resolving the role of Broca’s area with millisecond precision

When patients were repeating words that they had just heard or read, Dr. Flinker found a characteristic pattern of activation: first the auditory cortex, then Broca’s area, and finally the motor cortex. Importantly, activity in Broca’s area closely followed that in the auditory cortex, and by the time the patients were starting to speak themselves, neural activity in Broca’s area had resumed to its resting level. This suggests that Broca’s area cannot be responsible for actually coordinating speech movements. Flinker and colleagues then used Granger causality analysis, a statistical method originally developed in economic forecasting, in order to estimate the direction of information flow from one brain area to another. That analysis confirmed that the auditory cortex first influenced Broca’s area, which in turn influenced the motor cortex. Importantly, the influence of Broca’s area over the motor cortex had terminated before the patients started speaking. These results confirm that it could not be responsible for coordinating articulation.

The graphs on the left side of the figure represent the amount of activity in the auditory cortex (superior temporal gyrus, STG, top), Broca’s area (middle) and the motor cortex (bottom). Yellows and reds indicate larger amounts of activity, whereas green indicates baseline activity. Notice how activity in Broca’s area has returned to baseline by the time the patient is speaking (later than the vertical dashed line). (Source: Flinker A, et al. Redefining the role of Broca’s area in speech. PNAS 2015;112:2871-2875)

The graphs on the left side of the figure represent the amount of activity in the auditory cortex (superior temporal gyrus, STG, top), Broca’s area (middle) and the motor cortex (bottom). Yellows and reds indicate larger amounts of activity, whereas green indicates baseline activity. Notice how activity in Broca’s area has returned to baseline by the time the patient is speaking (later than the vertical dashed line). (Source: Flinker A, et al. Redefining the role of Broca’s area in speech. PNAS 2015;112:2871-2875)

In a clever twist built into the word repeating task, Flinker and colleagues included pseudo-words such as “yode” in addition to existing words such as “book”. The patients were able to speak these pseudo-words just as well as the standard ones, although it took them a little more time to do so. Crucially, Broca’s area was more intensely at work before the patients repeated the pseudo-words, suggesting that the role of that area was to prepare the novel articulatory combinations that were then executed in the motor cortex.

Flinker and colleagues’ findings nicely align with those of another study that directly assessed Broca’s area in different conditions: Dr. Matthew Tate and colleagues from the University Hospital of Montpellier, France, applied bursts of electrical stimulation directly to the surface of the cerebral cortex in patients who were undergoing neurosurgery [3] (I reported about that study here). Such a procedure, known as intraoperative mapping, sounds more painful and uncomfortable than it really is: after the patient’s brain has been exposed under general anesthesia, the patient is allowed to wake up on the operating table, with local anesthetics taking care of the pain caused by the surgery. She is then asked to repeat words, just as Dr. Flinker’s patients, while the neurosurgeon transiently and reversibly disrupts cortical function with electricity. Not your typical day in the park, but it is worth the effort: direct stimulation mapping yields the most precise functional maps of the human brain, and therefore ensures that the surgery won’t affect the patient’s language or cause any other disability. Dr. Tate and colleagues found that briefly tampering with Broca’s area while patients were speaking rarely prevented them from getting the words out altogether. Instead, it caused them to have “slips of the tongue”, paraphasias in technical parlance: incorrect wrong speech sounds would be inserted into words, but articulation would then proceed normally.

To scan a dead brain

If Broca’s area is not active during articulation itself, and if transiently impairing its function leaves patients able to articulate, why did Leborgne, and why do patients with Broca’s aphasia, have such massive difficulties to get any word out at all? Here, neuroimaging did make a critical contribution: Broca had the good idea of preserving Leborgne’s brain for posterity, which meant that it could be examined with a modern MRI scanner. That is just what Dr. Dronkers and colleagues, from the University of California, Davis and the Université Pierre et Marie Curie, Paris, did, and they found that the damage extended far beyond Broca’s area per se, also involving the neighboring parietal and temporal lobes, but especially reaching into the depth of the cerebral hemisphere and destroying most of the insula and part of the basal ganglia [4]. In fairness to Broca, he did mention in his original report that the damage seemed more extensive than what he could see from the surface of the brain; but he chose not to dissect the brain precisely because he wanted to preserve it, and could therefore not assess the extent of the lesion completely. Thus, the apparent discrepancy between Broca’s area and Broca’s aphasia stems from the fact that the damage to Leborgne’s brain extended far beyond the confines of Broca’s area!

The story of Broca’s foundational discovery, and how modern neuroscience carefully refined and improved our understanding of the functional organization of speech production in the brain, is a vibrant example of cognitive neuroscience at work. There is no understating the absolutely crucial role of serendipitous clinical observations of patients with brain damage, the unfortunate victims of “Nature’s experiments”. Armed with modern neuroimaging and neurophysiological techniques, we can now functionally dissect the brain’s activity in health as well as in disease. The resulting, ever more detailed picture of the human brain at work changes the way we conceive of the relationship between our brains and our minds.

References

  1. Broca P. Remarques sur le siége de la faculté du langage articulé, suivies d’une observation d’aphémie (perte de la parole). Bull Soc Anat 1861;6:330–357.
  2. Flinker A, Korzeniewska A, Shestyuk AY, Franaszczuk PJ, Dronkers NF, Knight RT, & Crone NE (2015). Redefining the role of Broca’s area in speech. Proceedings of the National Academy of Sciences of the United States of America, 112 (9), 2871-5 PMID: 25730850
  3. Tate MC, Herbet G, Moritz-Gasser S, Tate JE, & Duffau H (2014). Probabilistic map of critical functional regions of the human cerebral cortex: Broca’s area revisited. Brain : a journal of neurology, 137 (Pt 10), 2773-82 PMID: 24970097
  4. Dronkers NF, Plaisant O, Iba-Zizen MT, & Cabanis EA (2007). Paul Broca’s historic cases: high resolution MR imaging of the brains of Leborgne and Lelong. Brain : a journal of neurology, 130 (Pt 5), 1432-41 PMID: 17405763
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