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A contemporary framework of language processing in the human brain in the context of preoperative and intraoperative language mapping

  • Functional Neuroradiology
  • Published:
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Abstract

Introduction

The emergence of advanced in vivo neuroimaging methods has redefined the understanding of brain function with a shift from traditional localizationist models to more complex and widely distributed neural networks. In human language processing, the traditional localizationist models of Wernicke and Broca have fallen out of favor for a dual-stream processing system involving complex networks organized over vast areas of the dominant hemisphere. The current review explores the cortical function and white matter connections of human language processing, as well as their relevance to surgical planning.

Methods

We performed a systematic review of the literature with narrative data analysis.

Results

Although there is significant heterogeneity in the literature over the past century of exploration, modern evidence provides new insight into the true cortical function and white matter anatomy of human language. Intraoperative data and postoperative outcome studies confirm a widely distributed language network extending far beyond the traditional cortical areas of Wernicke and Broca.

Conclusions

The anatomic distribution of language networks, based on current theories, is explored to present a modern and clinically relevant interpretation of language function. Within this framework, we present current knowledge regarding the known effects of damage to both cortical and subcortical components of these language networks. Ideally, we hope this framework will provide a common language for which to base future clinical studies in human language function.

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Abbreviations

AF:

arcuate fasciculus

AG:

angular gyrus

BA:

Brodmann Area

BTLA:

basal temporal language area

DES:

Direct electrical stimulation

DLPFC:

dorsolateral prefrontal cortex

DMPFC:

dorsomedial prefrontal cortex

dPMC:

dorsal premotor cortex

dSMC:

dorsal sensorimotor cortex

FAT:

frontal aslant tract

FST:

frontostriatal tract

IFG:

inferior frontal gyrus

IFOF:

inferior fronto-occipital fasciculus

ILF:

inferior longitudinal fasciculus

ITG:

inferior temporal gyrus

MdLF:

middle longitudinal fasciculus

MTG:

middle temporal gyrus

pOp:

pars opercularis

pOrb:

pars orbitalis

pTri:

pars triangularis

SLF:

superior longitudinal fasciculus

SMA:

supplementary motor area

SMG:

supramarginal gyrus

STG:

superior temporal gyrus

TP:

temporal pole

UF:

uncinate fasciculus

VOF:

vertical occipital fasciculus

vPMC:

ventral premotor cortex

vSMC:

ventral sensorimotor cortex;

VWFA:

visual word form area

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Acknowledgements

We are forever indebted to the late Albert L. Rhoton, Jr. MD, whose guidance and contributions made this work possible. His impact on medicine, those he treated and those he educated will never be forgotten.

Data were provided in part by the Human Connectome Project, WU-Minn Consortium (Principal Investigators: David Van Essen and Kamil Ugurbil; 1U54MH091657) funded by the 16 NIH Institutes and Centers that support the NIH Blueprint for Neuroscience Research and by the McDonnell Center for Systems Neuroscience at Washington University.

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Authors and Affiliations

  1. Department of Radiology, College of Medicine, University of Alabama at Birmingham, 619 19th St. S., JT N409, Birmingham, AL, 35249, USA

    Erik H. Middlebrooks

  2. Division of Neurological Surgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, AZ, USA

    Kaan Yagmurlu

  3. Department of Neurology, University of Alabama at Birmingham, Birmingham, AL, USA

    Jerzey P. Szaflarski

  4. Department of Neurosurgery, University of Florida, Gainesville, FL, USA

    Maryam Rahman

  5. Department of Neurosurgery, University of Minnesota, Minneapolis, MN, USA

    Baran Bozkurt

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  1. Erik H. Middlebrooks
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Correspondence to Erik H. Middlebrooks.

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Supp Fig 1

The complex course of the inferior fronto-occipital fasciculus (IFOF) is further illustrated in a series of axial (top row) and coronal (bottom row) slices. S = superior; I = inferior; A = anterior; P = posterior. (GIF 2177 kb)

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Middlebrooks, E.H., Yagmurlu, K., Szaflarski, J.P. et al. A contemporary framework of language processing in the human brain in the context of preoperative and intraoperative language mapping. Neuroradiology 59, 69–87 (2017). https://doi.org/10.1007/s00234-016-1772-0

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