The Crossed Projection to the Striatum in Two Species of Monkey and in Humans: Behavioral and Evolutionary Significance

The corpus callosum establishes the anatomical continuity between the 2 hemispheres and coordinates their activity. Using histological tracing, single axon reconstructions, and diffusion tractography, we describe a callosal projection to n caudatus and putamen in monkeys and humans. In both species, the origin of this projection is more restricted than that of the ipsilateral projection. In monkeys, it consists of thin axons (0.4-0.6 µm), appropriate for spatial and temporal dispersion of subliminal inputs. For prefrontal cortex, contralateral minus ipsilateral delays to striatum calculated from axon diameters and conduction distance are <2 ms in the monkey and, by extrapolation, <4 ms in humans. This delay corresponds to the performance in Poffenberger's paradigm, a classical attempt to estimate central conduction delays, with a neuropsychological task. In both species, callosal cortico-striatal projections originate from prefrontal, premotor, and motor areas. In humans, we discovered a new projection originating from superior parietal lobule, supramarginal, and superior temporal gyrus, regions engaged in language processing. This projection crosses in the isthmus the lesion of which was reported to dissociate syntax and prosody. The projection might originate from an overproduction of callosal projections in development, differentially pruned depending on species.

[1]  T. Verstynen,et al.  Converging Structural and Functional Connectivity of Orbitofrontal, Dorsolateral Prefrontal, and Posterior Parietal Cortex in the Human Striatum , 2014, The Journal of Neuroscience.

[2]  Martin Parent,et al.  Single‐axon tracing study of corticostriatal projections arising from primary motor cortex in primates , 2006, The Journal of comparative neurology.

[3]  R. Caminiti,et al.  Evolution amplified processing with temporally dispersed slow neuronal connectivity in primates , 2009, Proceedings of the National Academy of Sciences.

[4]  Thyagarajan Subramanian,et al.  The interhemispheric connections of the striatum: Implications for Parkinson's disease and drug-induced dyskinesias , 2012, Brain Research Bulletin.

[5]  G. Paxinos,et al.  Atlas of the Human Brain , 2000 .

[6]  Giorgio M. Innocenti,et al.  Exuberance in the development of cortical networks , 2005, Nature Reviews Neuroscience.

[7]  Tim B. Dyrby,et al.  Distribution of collateral fibers in the monkey cervical spinal cord detected with diffusion-weighted magnetic resonance imaging , 2011, NeuroImage.

[8]  P. Goldman-Rakic,et al.  Interhemispheric integration: II. Symmetry and convergence of the corticostriatal projections of the left and the right principal sulcus (PS) and the left and the right supplementary motor area (SMA) of the rhesus monkey. , 1991, Cerebral cortex.

[9]  G. Wagner,et al.  Functional connectivity and grey matter volume of the striatum in schizophrenia , 2014, British Journal of Psychiatry.

[10]  K. Hasan,et al.  Decoding the superior parietal lobule connections of the superior longitudinal fasciculus/arcuate fasciculus in the human brain , 2014, Neuroscience.

[11]  Stefan Skare,et al.  How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging , 2003, NeuroImage.

[12]  A. Friederici.  The brain basis of language processing: from structure to function. , 2011, Physiological reviews.

[13]  Kevin D Alloway,et al.  Bilateral projections from rat MI whisker cortex to the neostriatum, thalamus, and claustrum: Forebrain circuits for modulating whisking behavior , 2009, The Journal of comparative neurology.

[14]  Timothy E. J. Behrens,et al.  The evolution of the arcuate fasciculus revealed with comparative DTI , 2008, Nature Neuroscience.

[15]  G. Feng,et al.  Striatal circuits, habits, and implications for obsessive–compulsive disorder , 2014, Current Opinion in Neurobiology.

[16]  Timothy E. J. Behrens,et al.  Measuring macroscopic brain connections in vivo , 2015, Nature Neuroscience.

[17]  René Westerhausen,et al.  Interhemispheric transfer time and structural properties of the corpus callosum , 2006, Neuroscience Letters.

[18]  Kyle S. Smith,et al.  A dual operator view of habitual behavior reflecting cortical and striatal dynamics. , 2013, Neuron.

[19]  H. Künzle.  Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study inMacaca fascicularis , 1975, Brain Research.

[20]  E. Welker,et al.  Constant and variable aspects of axonal phenotype in cerebral cortex. , 1998, Cerebral cortex.

[21]  R. Caminiti,et al.  The diameter of cortical axons depends both on the area of origin and target. , 2014, Cerebral cortex.

[22]  Y. Kawaguchi,et al.  Recurrent Connection Patterns of Corticostriatal Pyramidal Cells in Frontal Cortex , 2006, The Journal of Neuroscience.

[23]  T. Nakamae,et al.  Altered Fronto-Striatal Fiber Topography and Connectivity in Obsessive-Compulsive Disorder , 2014, PloS one.

[24]  Marco Iacoboni,et al.  Interhemispheric visuo-motor integration in humans: the role of the superior parietal cortex , 2004, Neuropsychologia.

[25]  P. Rakić,et al.  Axon overproduction and elimination in the corpus callosum of the developing rhesus monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  Robert Leech,et al.  Overlapping Networks Engaged during Spoken Language Production and Its Cognitive Control , 2014, The Journal of Neuroscience.

[27]  C. Marzi,et al.  Differential impairment of interhemispheric transmission in bipolar disease , 2013, Experimental Brain Research.

[28]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[29]  R. Caminiti,et al.  Areal differences in diameter and length of corticofugal projections. , 2012, Cerebral Cortex.

[30]  C.J. Wilson,et al.  Morphology and synaptic connections of crossed corticostriatal neurons in the rat , 1987, The Journal of comparative neurology.

[31]  Thomas R. Knösche,et al.  White matter integrity, fiber count, and other fallacies: The do's and don'ts of diffusion MRI , 2013, NeuroImage.

[32]  Ian R. Wickersham,et al.  Convergent cortical innervation of striatal projection neurons , 2013, Nature Neuroscience.

[33]  J. Fallon,et al.  The crossed cortico-caudate projection in the rhesus monkey , 1979, Neuroscience Letters.

[34]  G. Silberberg,et al.  Multisensory Integration in the Mouse Striatum , 2014, Neuron.

[35]  C. Marzi.  Asymmetry of interhemispheric communication , 2010 .

[36]  Jacob Jelsing,et al.  Validation of in vitro probabilistic tractography , 2007, NeuroImage.

[37]  Jelliffe.  Le Corps Calleux , 1911 .

[38]  R. Porter,et al.  Cells of origin and terminal distrubution of corticostriatal fibers arising in the sensory‐motor cortex of monkeys , 1977, The Journal of comparative neurology.

[39]  Adam G. Thomas,et al.  The Organization of Dorsal Frontal Cortex in Humans and Macaques , 2013, The Journal of Neuroscience.

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

[41]  G. Shepherd.  Corticostriatal connectivity and its role in disease , 2013, Nature Reviews Neuroscience.

[42]  A. Anwander,et al.  Validation of tractography: Comparison with manganese tracing , 2015, Human brain mapping.

[43]  A. Zador,et al.  Corticostriatal neurones in auditory cortex drive decisions during auditory discrimination , 2013, Nature.

[44]  Sten Grillner,et al.  Independent circuits in the basal ganglia for the evaluation and selection of actions , 2013, Proceedings of the National Academy of Sciences.

[45]  T. Powell,et al.  The cortico-striate projection in the monkey. , 1970, Brain : a journal of neurology.

[46]  D. Geschwind,et al.  Cortical Evolution: Judge the Brain by Its Cover , 2013, Neuron.

[47]  C. Price,et al.  Phonological decisions require both the left and right supramarginal gyri , 2010, Proceedings of the National Academy of Sciences.

[48]  J. Doyon,et al.  Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[49]  H. Killackey,et al.  Process elimination underlies ontogenetic change in the distribution of callosal projection neurons in the postcentral gyrus of the fetal rhesus monkey. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[50]  R. Caminiti,et al.  Diameter, Length, Speed, and Conduction Delay of Callosal Axons in Macaque Monkeys and Humans: Comparing Data from Histology and Magnetic Resonance Imaging Diffusion Tractography , 2013, The Journal of Neuroscience.

[51]  A. Parent,et al.  The Primate Basal Ganglia Connectome As Revealed By Single-Axon Tracing , 2016 .

[52]  Stephen M. Smith,et al.  A Bayesian model of shape and appearance for subcortical brain segmentation , 2011, NeuroImage.

[53]  W M COWAN,et al.  A bilateral cortico-striate projection , 1965, Journal of neurology, neurosurgery, and psychiatry.

[54]  Pasko Rakic,et al.  Renewed focus on the developing human neocortex , 2010, Journal of anatomy.

[55]  W. Baaré,et al.  An ex vivo imaging pipeline for producing high‐quality and high‐resolution diffusion‐weighted imaging datasets , 2011, Human brain mapping.

[56]  J. Schall,et al.  Comparative diffusion tractography of corticostriatal motor pathways reveals differences between humans and macaques. , 2015, Journal of neurophysiology.