ReviewThe error of Broca: From the traditional localizationist concept to a connectomal anatomy of human brain
Introduction
As a consequence of the seminal lesional work of Broca (1861) who described that a damage in the left inferior frontal gyrus induced a reduced capacity for articulate speech, a decade before Wernicke (1874), who associated speech comprehension with the left superior posterior temporal gyrus, a localisationist view of the organization of cerebral functioning (especially for language) was inexorably established. According to this fixed work-frame, it has been postulated that the organization of the human brain is based upon highly specialized eloquent regions (such as Broca’s and Wernicke’s areas) for which any damage results in permanent neurological impairments, opposed to “non-eloquent” stuctures for which no functional consequences occur in case of injury In addition, such a dogma of localizationism implicitly resulted in the principle of a similar brain functional anatomy between individuals, as for example the pars opercularis and pars triangularis of the left “dominant” hemisphere, that is, the Broca's area, that is a priori considered to the speech area in all human brains. Of note, this traditional view of a static functional organization of the brain had numerous implications not only in fundamental neurosciences, by resulting notably in the elaboration of simplistic and rigid models of conation and cognition, but also in clinical practice – especially by claiming that surgery was impossible in the so-called “eloquent” structures (Sawaya et al., 1998).
In this article, the aim is to break with this classical modular and inflexible model by proposing a dynamic and connectomal anatomy underlying neural circuits, that explains a major inter-individual anatomo-functional variability (Duffau, 2016) and that allows postlesional cerebral adaptive phenomena able to maintain neurological and cognitive functions (Duffau, 2014a), opening the window to new therapeutic strategies in brain-damaged patients, especially in the field of neurooncology (Duffau and Taillandier, 2015). In this state of mind, recent data provided by serial mappings performed in patients who underwent awake surgery for diffuse glioma infiltrating eloquent structures will be reviewed.
Section snippets
Methodological shortcomings inherent to the classical lesion method
The localizationist concept was mainly built on behavioral-structural correlations based upon lesion method. However, this methodology suffers from serious limitations (Herbet et al., 2015a).
The first is the size of the injuries, which are often large, especially in stroke, with usually an inhomogeneous spatial distribution of lesions and a small number of patients.
Secondly, the accurate three dimensional delineation of damages was very difficult until development of MRI. Indeed, recent MRIs of
Intraoperative electrical cortical and axonal mapping: an original technique to evoke a transient virtual lesion of neural network
Advances in functional neuroimaging have recently provided new insights into the neurobiology of cerebral functions, especially with regard to language, by studying the whole brain during functional tasks, both in healthy subjects and in brain-damaged patients. Using task-based functional MRI, the classical concept of language organization shifted towards distributed models (Vigneau et al., 2006). However, functional MRI can not differentiate cortical areas crucial for the neural functions from
The concept of postlesional neuroplasticity
Neuroplasticity can be defined as a continuous process subserving short, middle and long-term remodeling of the neurono-synaptic organization, in order to optimize the functioning of neural networks – during phylogeny, ontogeny, physiological learning and after brain insult (Duffau, 2006). Neural plasticity is possible solely in a dynamic account of cerebral distribution, in which the nervous system is an ensemble of complex subcircuits that form, reshape and flush information dynamically (
Clinical implications of a networking model of neural processes
From a clinical perspective, such a paradigmatic shift from localizationism to connectomics results in numerous implications. In brain surgery for tumors or epilepsy, it is in fine possible to achieve massive excisions in “eloquent” structures wrongly conceived as inoperable for many decades, with nonetheless preservation or even improvement of the quality of life. Especially in surgical neurooncology, owing to the phenomenon of adaptive neuroplasticity, glioma removal can be performed with a
Conclusions and perspectives
It is time to switch from a modular to a connectomal (delocalized) and dynamic model of neural processes, breaking with the traditional localisationist dogma. Multimodal investigations based upon combination of serial peri-operative functional neuroimaging and intraoperative DES has resulted in original individual and integrative models of functioning of neurono-synaptic circuits. Such networking account permits a greater knowledge of the dynamic potential of spatiotemporal reallocation of
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2021, CortexCitation Excerpt :The absence of prominent inferior frontal GM is complementary to earlier studies in stroke patients (Bates et al., 2003) and direct electrical stimulation (DES) findings (Sarubbo et al., 2020; Tate, Herbet, Moritz-Gasser, Tate, & Duffau, 2014). The absence of inferior frontal GM clusters in the VLSM results is in line with previous observations on the absence of long lasting aphasia after resection of Broca's area (BA 44 and 45) (Duffau, 2018). A potential explanation for this observation may be seen in neuroplasticity processes, compensating for effects of brain tumor or specifically glioma related lesions on language performance, as it has been reported earlier (Amoruso et al., 2021; Piai et al., 2020; Yuan et al., 2020).
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