Contemporary model of language organization: an overview for neurosurgeons

Abstract

T he pursuit of defining how the human brain processes language is one of the greatest challenges in neuroscience. Pierre Broca and Karl Wernicke made fundamental contributions at a time when the practice of localization by phrenology was pervasive. Their careful studies were some of the first to define functional localization in the brain by studying patients with defined brain injuries and lesions. Over time, their names have become synonymous with two key brain areas for language function: the inferior frontal gyrus and superior posterior temporal area, respectively. The brain regions that bear their names are now universal in every medical student's education. However, the dichotomy of language production based in the frontal lobe and language comprehension based in the temporal lobe is a commonly oversimplified interpretation of their work. For example, injuries to Wernicke's area result in abnormal speech production in addition to deficits in comprehension. Frontal lesions can also result in higherorder comprehension deficits. Thus, the language network is more complicated and integrated than commonly appreciated. In the last 15 years, an exponential increase in the number of studies on the neurobiology of language has improved our understanding of potential mechanisms, but many fundamental questions remain unresolved.Our goal in this overview is to provide an update to neurosurgeons by comparing classic with more recent models of language organization. It is not meant to be an exhaustive review of language research, which is beyond our intended scope, but rather to introduce contemporary theories and briefly review selected neurosurgical experience with stimulation-based language mapping. This will abbreviatioNs DTI = diffusion tensor imaging; fMRI = functional MRI; IFOF = inferior fronto-occipital fasciculus; MTG = middle temporal gyrus; PVWM = periventricular white matter; SLF = superior longitudinal fasciculus; SMA = supplementary motor area; STG = superior temporal gyrus; STS = superior temporal sulcus. Classic models of language organization posited that separate motor and sensory language foci existed in the inferior frontal gyrus (Broca's area) and superior temporal gyrus (Wernicke's area), respectively, and that connections between these sites (arcuate fasciculus) allowed for auditory-motor interaction. These theories have predominated for more than a century, but advances in neuroimaging and stimulation mapping have provided a more detailed description of the functional neuroanatomy of language. New insights have shaped modern network-based models of speech processing composed of parallel and interconnected streams involving both cortical and subcortical areas. Recent models emphasize processing in "dorsal" and "ventral" pathways, mediating phonological and semantic processing, respectively. Phonological processing occurs along a dorsal pathway, from the posterosuperior temporal to the inferior frontal cortices. On the other hand, semantic information is carried in a ventral pathway that runs fro...

Insights into the Neural and Genetic Basis of Vocal Communication

“…These early descriptions, along with later accounts provided by the pioneering work of the neurosurgeon Wilder Penfield who carried out stimulation and recording of specific neocortical areas in awake patients (known as electrocorticography, ECoG, or intracranial electroencephalography, iEEG) (Penfield and Rasmussen, 1949), laid the basis for attributing neural mechanisms to speech and language. Modern approaches have additionally used non-invasive techniques such as magnetoencephalography (MEG), transcranical magnetic stimulation (TMS), and functional MRI (fMRI) to study speech in both patient and neuro-typical populations (for an in-depth discussion and primary references please see (Cattaneo, 2013; Chang et al, 2015; Devlin and Watkins, 2007; Poeppel, 2012; Price, 2010)).…”

Fiber tracts of the dorsal language stream in the human brain

“…11,59 The arcuate (AF) and superior longitudinal fasciculi (SLF) are involved in the dorsal language stream, while the middle longitudinal (MLF), inferior longitudinal (ILF), inferior frontooccipital (IFOF), and uncinate fasciculi (UF) are associated with the ventral language stream (see Fig. 3C).…”

A Cool Approach to Probing Speech Cortex

“…If the applied electrical current reliably disrupts the patient’s speech output, or causes naming errors with intact speech output, the cortical site is deemed to be critical for language and is spared from resection. Even though counting and picture naming tasks tap into a relatively small subset of language functions, sparing of sites identified by ESM dramatically reduces postoperative deficits and the procedure remains the gold standard in the field (Chang et al, 2015; Sanai et al, 2008). …”