Developmental genetic programs and activity-dependent mechanisms instruct neocortical area mapping

The subdivision of the mammalian neocortex into specialized modality-specific areas is responsible for the processing of sensory information followed by an adequate motor response. This process, called arealization, depends on the graded expression of transcription factors in neocortical progenitors and postmitotic neurons prenatally, and on external activity-dependent cues driven by thalamocortical axons during postnatal stages. Thalamic inputs are guided within an intrinsically determined genetic framework to selectively target and innervate layer 4 (L4) cortical neurons in a somatotopic manner. L4 spiny stellate neurons are excitatory locally projecting neurons, which undergo a drastic dendrite remodeling during the first postnatal week and represent the principal sensory gateway to the neocortex. In this review, we will discuss the way intrinsic cortical gene regulation and extrinsic activity-dependent inputs instruct the cellular reorganization of L4 spiny stellate neurons, necessary for proper formation of the barrel cortex during the development of primary somatosensory maps.

[1]  Masaharu Ogawa,et al.  BTBD3 Controls Dendrite Orientation Toward Active Axons in Mammalian Neocortex , 2013, Science.

[2]  K. Kitamura,et al.  Patchwork-Type Spontaneous Activity in Neonatal Barrel Cortex Layer 4 Transmitted via Thalamocortical Projections. , 2018, Cell reports.

[3]  G. Shepherd,et al.  The neocortical circuit: themes and variations , 2015, Nature Neuroscience.

[4]  M. Minlebaev,et al.  Horizontal Synchronization of Neuronal Activity in the Barrel Cortex of the Neonatal Rat by Spindle-Burst Oscillations , 2018, Front. Cell. Neurosci..

[5]  S. Sherman,et al.  The corticothalamocortical circuit drives higher-order cortex in the mouse , 2009, Nature Neuroscience.

[6]  Michael C. Crair,et al.  Laminar and Columnar Development of Barrel Cortex Relies on Thalamocortical Neurotransmission , 2013, Neuron.

[7]  D. Jabaudon.  Fate and freedom in developing neocortical circuits , 2017, Nature Communications.

[8]  H. Luhmann,et al.  Modulation of Neocortical Development by Early Neuronal Activity: Physiology and Pathophysiology , 2017, Front. Cell. Neurosci..

[9]  G. López-Bendito,et al.  Developmental interactions between thalamus and cortex: a true love reciprocal story , 2018, Current Opinion in Neurobiology.

[10]  Heiko J Luhmann,et al.  The subplate and early cortical circuits. , 2010, Annual review of neuroscience.

[11]  S. Itohara,et al.  Thalamic adenylyl cyclase 1 is required for barrel formation in the somatosensory cortex , 2015, Neuroscience.

[12]  J. D. Macklis,et al.  RORβ induces barrel-like neuronal clusters in the developing neocortex. , 2012, Cerebral cortex.

[13]  D. O'Leary,et al.  Geniculocortical Input Drives Genetic Distinctions Between Primary and Higher-Order Visual Areas , 2013, Science.

[14]  Y. Inoue,et al.  A sharp cadherin-6 gene expression boundary in the developing mouse cortical plate demarcates the future functional areal border. , 2013, Cerebral cortex.

[15]  E. Grove,et al.  Neocortex Patterning by the Secreted Signaling Molecule FGF8 , 2001, Science.

[16]  Andrei Rozov,et al.  Developmental Changes in Electrophysiological Properties and a Transition from Electrical to Chemical Coupling between Excitatory Layer 4 Neurons in the Rat Barrel Cortex , 2016, Front. Neural Circuits.

[17]  Patrick O Kanold,et al.  Subplate Neurons Promote Spindle Bursts and Thalamocortical Patterning in the Neonatal Rat Somatosensory Cortex , 2012, The Journal of Neuroscience.

[18]  Jianhua Cang,et al.  Developmental mechanisms of topographic map formation and alignment. , 2013, Annual review of neuroscience.

[19]  Heiko J. Luhmann,et al.  Neuronal Activity Patterns in the Developing Barrel Cortex , 2018, Neuroscience.

[20]  Y. Fujiyoshi,et al.  Control of Spontaneous Ca2+ Transients Is Critical for Neuronal Maturation in the Developing Neocortex. , 2016, Cerebral cortex.

[21]  K. L. Tucker,et al.  Postnatal neuronal apoptosis in the cerebral cortex: Physiological and pathophysiological mechanisms , 2013, Neuroscience.

[22]  L. Goff,et al.  Variation in Activity State, Axonal Projection, and Position Define the Transcriptional Identity of Individual Neocortical Projection Neurons. , 2018, Cell reports.

[23]  S. Nelson,et al.  Prenatal thalamic waves regulate cortical area size prior to sensory processing , 2017, Nature Communications.

[24]  J. Buxbaum,et al.  Maturation of cortical circuits requires Semaphorin 7A , 2014, Proceedings of the National Academy of Sciences.

[25]  A. Pierani,et al.  Tangential migration of glutamatergic neurons and cortical patterning during development: Lessons from Cajal‐Retzius cells , 2016, Developmental neurobiology.

[26]  H. Luhmann,et al.  Control of programmed cell death by distinct electrical activity patterns. , 2011, Cerebral cortex.

[27]  D. Feldmeyer.  Excitatory neuronal connectivity in the barrel cortex , 2012, Front. Neuroanat..

[28]  D. O'Leary,et al.  Postmitotic regulation of sensory area patterning in the mammalian neocortex by Lhx2 , 2015, Proceedings of the National Academy of Sciences.

[29]  A. Holtmaat,et al.  Modality-specific thalamocortical inputs instruct the identity of postsynaptic L4 neurons , 2014, Nature.

[30]  Michael J. Albright,et al.  mGluR5 in Cortical Excitatory Neurons Exerts Both Cell-Autonomous and -Nonautonomous Influences on Cortical Somatosensory Circuit Formation , 2010, The Journal of Neuroscience.

[31]  Marla B. Feller,et al.  A Role for Correlated Spontaneous Activity in the Assembly of Neural Circuits , 2013, Neuron.

[32]  M. Feller,et al.  Mechanisms underlying spontaneous patterned activity in developing neural circuits , 2010, Nature Reviews Neuroscience.

[33]  Heiko J. Luhmann,et al.  Spontaneous Neuronal Activity in Developing Neocortical Networks: From Single Cells to Large-Scale Interactions , 2016, Front. Neural Circuits.

[34]  Laura C. Andreae,et al.  The role of spontaneous neurotransmission in synapse and circuit development , 2017, Journal of neuroscience research.

[35]  Jui-Yen Huang,et al.  mGluR5 Exerts Cell-Autonomous Influences on the Functional and Anatomical Development of Layer IV Cortical Neurons in the Mouse Primary Somatosensory Cortex , 2016, The Journal of Neuroscience.

[36]  S Murray Sherman,et al.  Properties of the primary somatosensory cortex projection to the primary motor cortex in the mouse. , 2015, Journal of neurophysiology.

[37]  E. Callaway,et al.  Developmental Sculpting of Dendritic Morphology of Layer 4 Neurons in Visual Cortex: Influence of Retinal Input , 2011, The Journal of Neuroscience.

[38]  S Murray Sherman,et al.  Thalamus plays a central role in ongoing cortical functioning , 2016, Nature Neuroscience.

[39]  P. Gaspar,et al.  ROR&agr; Coordinates Thalamic and Cortical Maturation to Instruct Barrel Cortex Development , 2018, Cerebral cortex.

[40]  T. Südhof,et al.  Neurotransmitter Release at the Thalamocortical Synapse Instructs Barrel Formation But Not Axon Patterning in the Somatosensory Cortex , 2012, The Journal of Neuroscience.

[41]  Ugo Tomasello,et al.  Transient Cell‐intrinsic Activity Regulates the Migration and Laminar Positioning of Cortical Projection Neurons , 2017, Cerebral cortex.

[42]  M. Crair,et al.  Cortical Adenylyl Cyclase 1 Is Required for Thalamocortical Synapse Maturation and Aspects of Layer IV Barrel Development , 2008, The Journal of Neuroscience.

[43]  M. Studer,et al.  Neocortical arealization: Evolution, mechanisms, and open questions , 2013, Developmental neurobiology.

[44]  T. Shimogori,et al.  FGF8 acts as a classic diffusible morphogen to pattern the neocortex , 2010, Development.

[45]  M. Studer,et al.  The pleiotropic transcriptional regulator COUP-TFI plays multiple roles in neural development and disease , 2019, Brain Research.

[46]  M. Nieto,et al.  Lhx2 Expression in Postmitotic Cortical Neurons Initiates Assembly of the Thalamocortical Somatosensory Circuit. , 2017, Cell reports.

[47]  Anirvan Ghosh,et al.  Calcium Activation of the LMO4 Transcription Complex and Its Role in the Patterning of Thalamocortical Connections , 2006, The Journal of Neuroscience.

[48]  Y. Yoshimura,et al.  NMDAR-Regulated Dynamics of Layer 4 Neuronal Dendrites during Thalamocortical Reorganization in Neonates , 2014, Neuron.

[49]  J. D. Macklis,et al.  Molecular logic of neocortical projection neuron specification, development and diversity , 2013, Nature Reviews Neuroscience.

[50]  Y. Inoue,et al.  Classic cadherin expressions balance postnatal neuronal positioning and dendrite dynamics to elaborate the specific cytoarchitecture of the mouse cortical area , 2016, Neuroscience Research.

[51]  P. Gaspar,et al.  Development and critical period plasticity of the barrel cortex , 2012, The European journal of neuroscience.

[52]  K. Amunts,et al.  Centenary of Brodmann's Map — Conception and Fate , 2022 .