The tract terminations in the temporal lobe: Their location and associated functions

Temporal lobe networks are associated with multiple cognitive domains. Despite an upsurge of interest in connectional neuroanatomy, the terminations of the main fibre tracts in the human brain are yet to be mapped. This information is essential given that neurological, neuroanatomical and computational accounts expect neural functions to be strongly shaped by the pattern of white-matter connections. This paper uses a probabilistic tractography approach to identify the main cortical areas that contribute to the major temporal lobe tracts. In order to associate the tract terminations to known functional domains of the temporal lobe, eight automated meta-analyses were performed using the Neurosynth database. Overlaps between the functional regions highlighted by the meta-analyses and the termination maps were identified in order to investigate the functional importance of the tracts of the temporal lobe. The termination maps are made available in the Supplementary Materials of this article for use by researchers in the field.

[1]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[2]  M. Catani,et al.  The arcuate fasciculus and the disconnection theme in language and aphasia: History and current state , 2008, Cortex.

[3]  O. Devinsky.  The Temporal Lobe and Limbic System , 1998 .

[4]  A W Roe,et al.  Visual projections routed to the auditory pathway in ferrets: receptive fields of visual neurons in primary auditory cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  Sophie K. Scott,et al.  Hemispheric Asymmetries in Speech Perception: Sense, Nonsense and Modulations , 2011, PloS one.

[6]  Fang-Cheng Yeh,et al.  Rethinking the role of the middle longitudinal fascicle in language and auditory pathways. , 2013, Cerebral cortex.

[7]  Matthew A. Lambon Ralph,et al.  Lateralization of ventral and dorsal auditory-language pathways in the human brain , 2005, NeuroImage.

[8]  D. N. Pandya,et al.  Further observations on parieto-temporal connections in the rhesus monkey , 2004, Experimental Brain Research.

[9]  R. Bronen,et al.  MR imaging of the temporal stem: anatomic dissection tractography of the uncinate fasciculus, inferior occipitofrontal fasciculus, and Meyer's loop of the optic radiation. , 2004, AJNR. American journal of neuroradiology.

[10]  D. Pandya,et al.  Delineation of the middle longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. , 2009, Cerebral cortex.

[11]  M. Catani,et al.  The anatomy of fronto-occipital connections from early blunt dissections to contemporary tractography , 2014, Cortex.

[12]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[13]  Jelliffe.  Vergleichende Lokalisationslehre der Grosshirnrinde , 1910 .

[14]  M. Jenkinson.  Non-linear registration aka Spatial normalisation , 2007 .

[15]  H. Duffau,et al.  Frontal terminations for the inferior fronto-occipital fascicle: anatomical dissection, DTI study and functional considerations on a multi-component bundle , 2011, Brain Structure and Function.

[16]  Matthew A. Lambon Ralph,et al.  Neurocognitive insights on conceptual knowledge and its breakdown , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[17]  J. Rauschecker,et al.  Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing , 2009, Nature Neuroscience.

[18]  Geoffrey J M Parker,et al.  A framework for a streamline‐based probabilistic index of connectivity (PICo) using a structural interpretation of MRI diffusion measurements , 2003, Journal of magnetic resonance imaging : JMRI.

[19]  E. J. Curran.  A new association fiber tract in the cerebrum with remarks on the fiber tract dissection method of studying the brain , 1909 .

[20]  Matthew P. G. Allin,et al.  Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography , 2011, NeuroImage.

[21]  Derek K. Jones,et al.  Frontotemporal Connections in Episodic Memory and Aging: A Diffusion MRI Tractography Study , 2011, The Journal of Neuroscience.

[22]  Hugues Duffau,et al.  Middle longitudinal fasciculus delineation within language pathways: a diffusion tensor imaging study in human. , 2013, European journal of radiology.

[23]  Jan Sijbers,et al.  Probabilistic fiber tracking using the residual bootstrap with constrained spherical deconvolution , 2011, Human brain mapping.

[24]  Timothy T Rogers,et al.  Semantic memory is impaired in patients with unilateral anterior temporal lobe resection for temporal lobe epilepsy. , 2012, Brain : a journal of neurology.

[25]  Lauren L. Cloutman,et al.  Using in vivo probabilistic tractography to reveal two segregated dorsal ‘language-cognitive’ pathways in the human brain☆ , 2013, Brain and Language.

[26]  Daniel C. Alexander,et al.  Using the Model-Based Residual Bootstrap to Quantify Uncertainty in Fiber Orientations From $Q$-Ball Analysis , 2009, IEEE Transactions on Medical Imaging.

[27]  Derek K. Jones,et al.  Perisylvian language networks of the human brain , 2005, Annals of neurology.

[28]  Emmanuel Mandonnet,et al.  A re-examination of neural basis of language processing: Proposal of a dynamic hodotopical model from data provided by brain stimulation mapping during picture naming , 2014, Brain and Language.

[29]  Nikos K. Logothetis,et al.  Validation of tractography against in vivo tracing in the macaque visual system: effect of distance correction , 2012 .

[30]  Matthew A. Lambon Ralph,et al.  Neurocognitive insights on conceptual knowledge and its breakdown , 2014 .

[31]  Jon H. Kaas,et al.  'What' and 'where' processing in auditory cortex , 1999, Nature Neuroscience.

[32]  Derek K. Jones,et al.  Symmetries in human brain language pathways correlate with verbal recall , 2007, Proceedings of the National Academy of Sciences.

[33]  Matthew A. Lambon Ralph,et al.  The variation of function across the human insula mirrors its patterns of structural connectivity: Evidence from in vivo probabilistic tractography , 2012, NeuroImage.

[34]  D. Pandya,et al.  The Complex History of the Fronto-Occipital Fasciculus , 2007, Journal of the history of the neurosciences.

[35]  Derek K. Jones,et al.  Virtual in Vivo Interactive Dissection of White Matter Fasciculi in the Human Brain , 2002, NeuroImage.

[36]  Lauren L. Cloutman,et al.  Interaction between dorsal and ventral processing streams: Where, when and how? , 2013, Brain and Language.

[37]  T. Rogers,et al.  Lichtheim 2: Synthesizing Aphasia and the Neural Basis of Language in a Neurocomputational Model of the Dual Dorsal-Ventral Language Pathways , 2011, Neuron.

[38]  P. Hoffman,et al.  Graded specialization within and between the anterior temporal lobes , 2015, Annals of the New York Academy of Sciences.

[39]  M. Sur,et al.  Experimentally induced visual projections into auditory thalamus and cortex. , 1988, Science.

[40]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[41]  Matthew A. Lambon Ralph,et al.  Convergent Connectivity and Graded Specialization in the Rostral Human Temporal Lobe as Revealed by Diffusion-Weighted Imaging Probabilistic Tractography , 2012, Journal of Cognitive Neuroscience.

[42]  Guy M. McKhann,et al.  Non-invasive Mapping of Connections Between Human Thalamus and Cortex Using Diffusion Imaging , 2004 .

[43]  P. Hoffman,et al.  The Roles of Left Versus Right Anterior Temporal Lobes in Conceptual Knowledge: An ALE Meta-analysis of 97 Functional Neuroimaging Studies , 2015, Cerebral cortex.

[44]  Karla L. Miller,et al.  The extreme capsule fiber complex in humans and macaque monkeys: a comparative diffusion MRI tractography study , 2015, Brain Structure and Function.

[45]  D. Poeppel,et al.  Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language , 2004, Cognition.

[46]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

[47]  Hugues Duffau,et al.  Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data , 2010, Cortex.

[48]  Jean-Francois Mangin,et al.  Toward global tractography , 2013, NeuroImage.

[49]  Nikos K. Logothetis,et al.  Validation of High-Resolution Tractography Against In Vivo Tracing in the Macaque Visual Cortex , 2015, Cerebral cortex.

[50]  C. Price.  The anatomy of language: a review of 100 fMRI studies published in 2009 , 2010, Annals of the New York Academy of Sciences.

[51]  T. L. Davis,et al.  Morphometry of in vivo human white matter association pathways with diffusion‐weighted magnetic resonance imaging , 1997, Annals of neurology.

[52]  Volkmar Glauche,et al.  Ventral and dorsal pathways for language , 2008, Proceedings of the National Academy of Sciences.

[53]  J. Kaas,et al.  Subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex in macaque monkeys , 1998, The Journal of comparative neurology.

[54]  Loyal Davis.  AN ANATOMIC STUDY OF THE INFERIOR LONGITUDINAL FASCICULUS , 1921 .

[55]  Alessandra Angelucci,et al.  Induction of visual orientation modules in auditory cortex , 2000, Nature.

[56]  D. Pandya,et al.  Fiber Pathways of the Brain , 2006 .

[57]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[58]  Valerie A. Carr,et al.  Spatiotemporal Dynamics of Modality-Specific and Supramodal Word Processing , 2003, Neuron.

[59]  Hugues Duffau,et al.  New Insights Into the Anatomic Dissection of the Temporal Stem With Special Emphasis on the Inferior Fronto‐occipital Fasciculus: Implications in Surgical Approach to Left Mesiotemporal and Temporoinsular Structures , 2010, Neurosurgery.

[60]  M. Petrides.  Neuroanatomy of Language Regions of the Human Brain , 2013 .

[61]  Cornelius Weiller,et al.  How the ventral pathway got lost – And what its recovery might mean , 2011, Brain and Language.

[62]  J. Dejerine.  Anatomie des centres nerveux , 1895 .

[63]  Karalyn Patterson,et al.  Taking both sides: do unilateral anterior temporal lobe lesions disrupt semantic memory? , 2010, Brain : a journal of neurology.

[64]  M. E. Shenton,et al.  Human middle longitudinal fascicle: segregation and behavioral-clinical implications of two distinct fiber connections linking temporal pole and superior temporal gyrus with the angular gyrus or superior parietal lobule using multi-tensor tractography , 2013, Brain Imaging and Behavior.

[65]  K. Grill-Spector,et al.  The human visual cortex. , 2004, Annual review of neuroscience.

[66]  Elizabeth Jefferies,et al.  Going beyond Inferior Prefrontal Involvement in Semantic Control: Evidence for the Additional Contribution of Dorsal Angular Gyrus and Posterior Middle Temporal Cortex , 2013, Journal of Cognitive Neuroscience.

[67]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[68]  Richard J. Binney,et al.  The ventral and inferolateral aspects of the anterior temporal lobe are crucial in semantic memory: evidence from a novel direct comparison of distortion-corrected fMRI, rTMS, and semantic dementia. , 2010, Cerebral cortex.

[69]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[70]  Evan Fletcher,et al.  Episodic memory function is associated with multiple measures of white matter integrity in cognitive aging , 2011, Front. Hum. Neurosci..

[71]  Claude J. Bajada,et al.  Transport for language south of the Sylvian fissure: The routes and history of the main tracts and stations in the ventral language network , 2015, Cortex.

[72]  M. L. Lambon Ralph,et al.  Conceptual knowledge is underpinned by the temporal pole bilaterally: convergent evidence from rTMS. , 2009, Cerebral cortex.

[73]  D. Louis Collins,et al.  Automatic 3‐D model‐based neuroanatomical segmentation , 1995 .

[74]  P. Basser.  Proceedings of the International Society for Magnetic Resonance in Medicine Fiber-tractography via Diffusion Tensor Mri (dt-mri) , 2022 .

[75]  Leslie G. Ungerleider,et al.  The inferior longitudinal fasciculus: A reexamination in humans and monkeys , 1985, Annals of neurology.

[76]  Hugues Duffau,et al.  Toward a pluri-component, multimodal, and dynamic organization of the ventral semantic stream in humans: lessons from stimulation mapping in awake patients , 2013, Front. Syst. Neurosci..

[77]  Giovanni Giulietti,et al.  Damage to the cingulum contributes to alzheimer's disease pathophysiology by deafferentation mechanism , 2012, Human brain mapping.

[78]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

[79]  Daniel C Alexander,et al.  Probabilistic anatomical connectivity derived from the microscopic persistent angular structure of cerebral tissue , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[80]  D. Plaut.  Graded modality-specific specialisation in semantics: A computational account of optic aphasia , 2002, Cognitive neuropsychology.

[81]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[82]  Derek K. Jones,et al.  Occipito-temporal connections in the human brain. , 2003, Brain : a journal of neurology.

[83]  H. Duffau,et al.  Evidence of a middle longitudinal fasciculus in the human brain from fiber dissection , 2013, Journal of anatomy.

[84]  D. Pandya,et al.  The extreme capsule in humans and rethinking of the language circuitry , 2009, Brain Structure and Function.

[85]  James L. McClelland,et al.  Why Bilateral Damage Is Worse than Unilateral Damage to the Brain , 2013, Journal of Cognitive Neuroscience.

[86]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[87]  Hugues Duffau,et al.  Cortex‐sparing fiber dissection: an improved method for the study of white matter anatomy in the human brain , 2011, Journal of anatomy.

[88]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[89]  Alan Connelly,et al.  Robust determination of the fibre orientation distribution in diffusion MRI: Non-negativity constrained super-resolved spherical deconvolution , 2007, NeuroImage.

[90]  S. Scott,et al.  Identification of a pathway for intelligible speech in the left temporal lobe. , 2000, Brain : a journal of neurology.

[91]  J Mazziotta,et al.  A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[92]  Geoff J M Parker,et al.  Distortion correction for diffusion‐weighted MRI tractography and fMRI in the temporal lobes , 2010, Human brain mapping.

[93]  Stefan Klöppel,et al.  Combining Functional and Anatomical Connectivity Reveals Brain Networks for Auditory Language Comprehension , 2022 .