Functional Development of Large-Scale Sensorimotor Cortical Networks in the Brain

Large-scale neuronal networks integrating several cortical areas mediate the complex functions of the brain such as sensorimotor integration. Little is known about the functional development of these networks and the maturational processes by which distant networks become functionally connected. We addressed this question in the postnatal rat sensorimotor system. Using epicranial multielectrode grids that span most of the cortical surface and intracortical electrodes, we show that sensory evoked cortical responses continuously maturate throughout the first 3 weeks with the strongest developmental changes occurring in a very short time around postnatal day 13 (P13). Before P13, whisker stimulation evokes slow, initially surface-negative activity restricted mostly to the lateral parietal area of the contralateral hemisphere. In a narrow time window of ∼48 h around P13, a new early, sharp surface-positive component emerges that coincides with subsequent propagation of activity to sensory and motor areas of both hemispheres. Our data show that this new component developing at the end of the second week corresponds principally to functional maturation of the supragranular cortical layers and appears to be crucial for the functional associations in the large-scale sensorimotor cortical network. It goes along with the onset of whisking behavior, as well as major synaptic and functional changes within the S1 cortex that are known to develop during this period.

[1]  K. Fox,et al.  Glutamate receptor blockade alters the development of intracortical connections in rat barrel cortex , 2003, Somatosensory & motor research.

[2]  B. Schlaggar,et al.  Early development of the somatotopic map and barrel patterning in rat somatosensory cortex , 1994, The Journal of comparative neurology.

[3]  Shubhodeep Chakrabarti,et al.  Differential origin of projections from SI barrel cortex to the whisker representations in SII and MI , 2006, The Journal of comparative neurology.

[4]  N. Wittenburg,et al.  Transformation from temporal to rate coding in a somatosensory thalamocortical pathway , 2022 .

[5]  K. Svoboda,et al.  Rapid Development and Plasticity of Layer 2/3 Maps in Rat Barrel Cortex In Vivo , 2001, Neuron.

[6]  D. Simons,et al.  Development of thalamocortical response transformations in the rat whisker-barrel system. , 2008, Journal of neurophysiology.

[7]  Kevin D Alloway,et al.  Contralateral corticothalamic projections from MI whisker cortex: Potential route for modulating hemispheric interactions , 2008, The Journal of comparative neurology.

[8]  U. Mitzdorf Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.

[9]  M. Sur,et al.  Development and plasticity of cortical areas and networks , 2001, Nature Reviews Neuroscience.

[10]  Kristina D. Micheva,et al.  Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry , 1996, The Journal of comparative neurology.

[11]  J. Tiago Gonçalves,et al.  Internally Mediated Developmental Desynchronization of Neocortical Network Activity , 2009, The Journal of Neuroscience.

[12]  H. Killackey,et al.  Evidence for the complementary organization of callosal and thalamic connections within rat somatosensory cortex , 1984, Brain Research.

[13]  K. Alloway,et al.  Septal columns in rodent barrel cortex: Functional circuits for modulating whisking behavior , 2004, The Journal of comparative neurology.

[14]  F. Haiss,et al.  Spatiotemporal Dynamics of Cortical Sensorimotor Integration in Behaving Mice , 2007, Neuron.

[15]  Heiko J. Luhmann,et al.  Early patterns of electrical activity in the developing cerebral cortex of humans and rodents , 2006, Trends in Neurosciences.

[16]  Daniel E Feldman,et al.  Synaptic basis for developmental plasticity in somatosensory cortex , 2004, Current Opinion in Neurobiology.

[17]  S. Czellár,et al.  Epicranial sensory evoked potential recordings for repeated assessment of cortical functions in mice , 2000, Journal of Neuroscience Methods.

[18]  M. Molinari,et al.  Efferent fibers from the motor cortex terminate bilaterally in the thalamus of rats and cats , 2004, Experimental Brain Research.

[19]  J. D. Macklis,et al.  Large‐scale maintenance of dual projections by callosal and frontal cortical projection neurons in adult mice , 2005, The Journal of comparative neurology.

[20]  C. Welker Receptive fields of barrels in the somatosensory neocortex of the rat , 1976, The Journal of comparative neurology.

[21]  David Kleinfeld,et al.  Closed-loop neuronal computations: focus on vibrissa somatosensation in rat. , 2003, Cerebral cortex.

[22]  F. Cicirata,et al.  Functional organization of thalamic projections to the motor cortex. An anatomical and electrophysiological study in the rat , 1986, Neuroscience.

[23]  D. Simons,et al.  Biometric analyses of vibrissal tactile discrimination in the rat , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  J. Olavarria,et al.  Areal and laminar organization of corticocortical projections in the rat somatosensory cortex , 1990, The Journal of comparative neurology.

[25]  Henry Kennedy,et al.  The development of cortical connections , 2006, The European journal of neuroscience.

[26]  Y. Matsubayashi,et al.  Whisker-Related Axonal Patterns and Plasticity of Layer 2/3 Neurons in the Mouse Barrel Cortex , 2010, The Journal of Neuroscience.

[27]  G. Buzsáki,et al.  Early motor activity drives spindle bursts in the developing somatosensory cortex , 2004, Nature.

[28]  K. Fox,et al.  Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex , 2002, Neuroscience.

[29]  S P Wise,et al.  Developmental studies of thalamocortical and commissural connections in the rat somatic sensory cortex , 1978, The Journal of comparative neurology.

[30]  E. Grove,et al.  Area and layer patterning in the developing cerebral cortex , 2006, Current Opinion in Neurobiology.

[31]  J. Poulet,et al.  Facilitating sensory responses in developing mouse somatosensory barrel cortex. , 2007, Journal of neurophysiology.

[32]  G. W. Huntley,et al.  Developmental and comparative aspects of posterior medial thalamocortical innervation of the barrel cortex in mice and rats , 2008, The Journal of comparative neurology.

[33]  T. Woolsey,et al.  Postnatal growth of intrinsic connections in mouse barrel cortex , 2001, The Journal of comparative neurology.

[34]  Barbara Clancy,et al.  Extrapolating brain development from experimental species to humans. , 2007, Neurotoxicology.

[35]  H. Killackey,et al.  Early ingrowth of thalamocortical afferents to the neocortex of the prenatal rat. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[36]  M. Armstrong‐James The functional status and columnar organization of single cells responding to cutaneous stimulation in neonatal rat somatosensory cortex S1. , 1975, The Journal of physiology.

[37]  E. Welker,et al.  Organization of feedback and feedforward projections of the barrel cortex: a PHA-L study in the mouse , 2004, Experimental Brain Research.

[38]  K. Svoboda,et al.  Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo , 2000, Nature.

[39]  C. Schroeder,et al.  Interpretation of high-resolution current source density profiles: a simulation of sublaminar contributions to the visual evoked potential , 1993, Experimental Brain Research.

[40]  C E Schroeder,et al.  Neural generators of early cortical somatosensory evoked potentials in the awake monkey. , 1995, Electroencephalography and clinical neurophysiology.

[41]  B. Finlay,et al.  Translating developmental time across mammalian species , 2001, Neuroscience.

[42]  Elina Pihko,et al.  Somatosensory processing in healthy newborns , 2004, Experimental Neurology.

[43]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[44]  Gilles Bonvento,et al.  Glial glutamate transporters and maturation of the mouse somatosensory cortex. , 2003, Cerebral cortex.

[45]  C. Quairiaux,et al.  Functional deficit and recovery of developing sensorimotor networks following neonatal hypoxic-ischemic injury in the rat. , 2010, Cerebral cortex.

[46]  Lei Zhang,et al.  Activity-Dependent Development of Callosal Projections in the Somatosensory Cortex , 2007, The Journal of Neuroscience.

[47]  R. Fields,et al.  Myelination: An Overlooked Mechanism of Synaptic Plasticity? , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[48]  W Karniski,et al.  The late somatosensory evoked potential in premature and term infants. I. Principal component topography. , 1992, Electroencephalography and clinical neurophysiology.

[49]  David M Rector,et al.  Hemispheric mapping of secondary somatosensory cortex in the rat. , 2007, Journal of neurophysiology.

[50]  Kevin D Alloway,et al.  Functional circuits mediating sensorimotor integration: Quantitative comparisons of projections from rodent barrel cortex to primary motor cortex, neostriatum, superior colliculus, and the pons , 2005, The Journal of comparative neurology.

[51]  R. S. Waters,et al.  Early development of the SI cortical barrel field representation in neonatal rats follows a lateral-to-medial gradient: an electrophysiological study , 2004, Experimental Brain Research.

[52]  W Singer,et al.  Laminar segregation of afferents to lateral geniculate nucleus of the cat: an analysis of current source density. , 1977, Journal of neurophysiology.

[53]  K. Toyama,et al.  Development of functional thalamocortical synapses studied with current source-density analysis in whole forebrain slices in the rat , 2003, Brain Research Bulletin.

[54]  Christoph M. Michel,et al.  A mouse model for studying large-scale neuronal networks using EEG mapping techniques , 2008, NeuroImage.

[55]  J. Stephen,et al.  Maturation of somatosensory cortical processing from birth to adulthood revealed by magnetoencephalography , 2009, Clinical Neurophysiology.

[56]  Karel Svoboda,et al.  Precise Development of Functional and Anatomical Columns in the Neocortex , 2004, Neuron.

[57]  Michael Brecht,et al.  Organization of rat vibrissa motor cortex and adjacent areas according to cytoarchitectonics, microstimulation, and intracellular stimulation of identified cells , 2004, The Journal of comparative neurology.

[58]  H. Killackey,et al.  Ontogenetic changes in the projections of neocortical neurons , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[59]  Sampsa Vanhatalo,et al.  Neonatal SEP - back to bedside with basic science. , 2006, Seminars in fetal & neonatal medicine.

[60]  M. Armstrong‐James,et al.  Spatiotemporal convergence and divergence in the rat S1 “Barrel” cortex , 1987, The Journal of comparative neurology.

[61]  R S Erzurumlu,et al.  Thalamic axons confer a blueprint of the sensory periphery onto the developing rat somatosensory cortex. , 1990, Brain research. Developmental brain research.

[62]  Shubhodeep Chakrabarti,et al.  Running Headline: Sensorimotor Integration in MI , 2022 .

[63]  David Kleinfeld,et al.  Active sensation: insights from the rodent vibrissa sensorimotor system , 2006, Current Opinion in Neurobiology.

[64]  B. Connors,et al.  Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[65]  M A Nicolelis,et al.  Bilateral Integration of Whisker Information in the Primary Somatosensory Cortex of Rats , 2001, The Journal of Neuroscience.

[66]  地藤 純哉,et al.  Maturational changes in diffusion anisotropy in the rat corpus callosum : comparison with quantitative histological evaluation , 2008 .