The Location of Speech and Writing Functions in the Frontal Language Area: Results of Extraoperative Cortical Stimulation

Lesser, R.P.; Lueders, Hans; Dinner, Dudley S.; Hahn, Joseph; Cohen, Laurent D.

doi:10.1093/brain/107.1.275

Cited by 121 publications

(43 citation statements)

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“…As a testament to his ingenuity, the technique of speech mapping has been largely unchanged over time except for minor modifications in this above described technique, and can also be performed extraoperatively with implanted electrode arrays. 59,60 Penfield described several forms of speech interference from electrical stimulation, including total speech arrest (anarthria), hesitation, slurring, distortion, repetition, and confusion (jumping from "six" to "twenty" and then back to "nine"). 86 During the picture-naming task, he described other more complex effects such as the inability to name with retained ability to speak and the perseveration of words that were presented previously.…”

Section: Intraoperative Cortical Mappingmentioning

confidence: 99%

Contemporary model of language organization: an overview for neurosurgeons

Chang¹,

Raygor²,

Berger³

2015

JNS

329

285

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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...

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Section: Intraoperative Cortical Mappingmentioning

confidence: 99%

Contemporary model of language organization: an overview for neurosurgeons

Chang¹,

Raygor²,

Berger³

2015

JNS

329

285

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“…Only one electrode, K8, produced an arrest in the reading without producing a positive or negative motor effect. This electrode probably corresponds to the posterior speech area (Wernicke) [ 19,25). Note that the electrodes from which we recorded the SII potentials (mainly G7 and H?)…”

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confidence: 96%

The second sensory area in humans: Evoked potential and electrical stimulation studies

Lüders

Lesser

Dinner

et al. 1985

Annals of Neurology

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119

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A patient with intractable seizures originating from a right frontal focus was evaluated for surgical treatment. This evaluation was carried out using a chronically implanted array of 96 stainless steel electrodes 1 cm apart and covering the perirolandic and frontal areas. Somatosensory evoked potentials and electrical stimulation of the subdural electrodes localized the primary sensory hand area. Evoked potentials of identical waveform but of lower amplitude and 2.4 ms longer latency were recorded in the inferior frontal gyrus immediately anterior to the face area of the motor strip. Electrical stimulation of that area elicited: (1) a "paralyzing" feeling in the left arm and face; (2) inhibition of rapid alternating movements of left fingers, left hand, and tongue; (3) inability to maintain a strong voluntary muscle contraction of the left hand or tongue; and (4) speech arrest. This appears to be the first report of a secondary sensory area in humans demonstrated by both electrical stimulation and evoked potential studies. Electrical stimulation showed that the secondary sensory area overlapped an area of complex motor control, suggesting that the secondary sensory area provides direct sensory feedback information for appropriate motor integration.

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“…However, there may be considerable variation among and within subjects in both the gross structure and the cytoarchitecture of the IFG, and the cytoarchitectonic borders do not consistently coincide with sulcal boundaries (Bailey and Bonin, 1951;Ebeling et al, 1989;Amunts et al, 1999;Tomaiuolo et al, 1999;Damasio, 2005). Since Broca's original description of the effects of lesions of this area on speaking ability (1861; see translation by von Bonin, 1950), evidence for the IFG as a structure critical for speech and language function has come from many studies using a variety of experimental approaches including lesion/behavior (Mohr et al, 1978;Damasio and Geschwind, 1984), electrical stimulation functional mapping (Penfield and Roberts, 1959;Ojemann, 1979;Lesser et al, 1984;Ojemann et al, 1989), functional magnetic resonance imaging (fMRI; Wildgruber et al, 1996;Paulesu et al, 1997;Lazar et al, 2000), magnetoencephalography (MEG; Sasaki et al, 1995;Dhond et al, 2001), positron emission tomography (PET; Klein et al, 1997;Bookheimer et al, 2000;Caplan et al, 2000), and singlephoton emission computed tomography (SPECT; Otsuki et al, 1998). These studies suggest that the IFG region is involved in numerous language-specific tasks including phonologic, semantic, and sentence-and discourse-level processing, as well as detection of the emotional content of speech (Gernsbacher and Kaschak, 2003;Martin, 2003).…”

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confidence: 99%

Functional connections within the human inferior frontal gyrus

Greenlee

Oya

Kawasaki

et al. 2007

J of Comparative Neurology

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The highly convoluted and cytoarchitectonically diverse inferior frontal gyrus (IFG) of humans is known to be critically involved in a wide range of complex operations including speech and language processing. The neural circuitry that underlies these operations is not fully understood. We hypothesized that this neural circuitry includes functional connections within and between the three major IFG subgyri: the pars orbitalis, pars triangularis, and pars opercularis. To test this hypothesis we employed electrical stimulation tract-tracing techniques in 10 human patients undergoing surgical treatment for intractable epilepsy. The approach involved delivering repeated bipolar electrical stimuli to one site on the IFG while recording the electrical response evoked by that stimulus from a 64-contact grid overlying more distant IFG sites. In all subjects, stimulation of a site on one subgyrus evoked polyphasic potentials at distant sites, either on the same subgyrus or on an adjacent subgyrus. This provided prima facie evidence for a functional connection between the site of stimulation and the sites of the evoked response. The averaged evoked potentials tended to aggregate as response fields. The spatial spread of a response field indicated a divergent projection from the site of stimulation. When two or more sites were stimulated, the resulting evoked potentials exhibited different waveforms while the respective response fields could overlap substantially, suggesting that input from multiple sites converged but by engaging different neural circuits. The earliest deflection in the evoked potential ranged from 2 to 10 msec. No differences were noted between language-dominant and language-nondominant hemispheres.

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The Location of Speech and Writing Functions in the Frontal Language Area: Results of Extraoperative Cortical Stimulation

Cited by 121 publications

References 0 publications

Contemporary model of language organization: an overview for neurosurgeons

Contemporary model of language organization: an overview for neurosurgeons

The second sensory area in humans: Evoked potential and electrical stimulation studies

Functional connections within the human inferior frontal gyrus

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