Sublayer-specific microcircuits of corticospinal and corticostriatal neurons in motor cortex

The mammalian motor system is organized around distinct subcortical subsystems, suggesting that the intracortical circuits immediately upstream of spinal cord and basal ganglia might be functionally differentiated as well. We found that the main excitatory pathway in mouse motor cortex, layer 2/3→5, is fractionated into distinct pathways targeting corticospinal and corticostriatal neurons, which are involved in motor control. However, connections were selective for neurons in certain sublayers: corticospinal neurons in upper layer 5B and corticostriatal neurons in lower 5A. A simple structural combinatorial principle accounts for this highly specific functional circuit architecture: potential connectivity is established by neuronal sublayer positioning and actual connectivity in this framework is determined by long-range axonal projection targets. Thus, intracortical circuits of these pyramidal neurons are specified not only by their long-range axonal targets or their layer or sublayer positions, but by both, in specific combinations.

[1]  S. Nelson,et al.  Region-Specific Spike-Frequency Acceleration in Layer 5 Pyramidal Neurons Mediated by Kv1 Subunits , 2008, The Journal of Neuroscience.

[2]  K. Svoboda,et al.  Channelrhodopsin-2–assisted circuit mapping of long-range callosal projections , 2007, Nature Neuroscience.

[3]  Katsuei Shibuki,et al.  Dynamic Imaging of Somatosensory Cortical activity in the Rat Visualized by Flavoprotein Autofluorescence , 2003, The Journal of physiology.

[4]  Edward M Callaway,et al.  Local connections to specific types of layer 6 neurons in the rat visual cortex. , 2006, Journal of neurophysiology.

[5]  B. Alstermark,et al.  In vivo recordings of bulbospinal excitation in adult mouse forelimb motoneurons. , 2004, Journal of neurophysiology.

[6]  C. Gerfen The neostriatal mosaic: striatal patch-matrix organization is related to cortical lamination. , 1989, Science.

[7]  Wenjun Gao,et al.  Target‐specific differences in somatodendritic morphology of layer V pyramidal neurons in rat motor cortex , 2004, The Journal of comparative neurology.

[8]  Edward M. Callaway,et al.  Retrograde Tracing with Recombinant Rabies Virus Reveals Correlations Between Projection Targets and Dendritic Architecture in Layer 5 of Mouse Barrel Cortex , 2007, Frontiers in neural circuits.

[9]  M. Brecht,et al.  Monosynaptic Pathway from Rat Vibrissa Motor Cortex to Facial Motor Neurons Revealed by Lentivirus-Based Axonal Tracing , 2005, The Journal of Neuroscience.

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

[11]  A. Thomson,et al.  Interlaminar connections in the neocortex. , 2003, Cerebral cortex.

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

[13]  G. Striedter Principles of brain evolution. , 2005 .

[14]  Hanno S Meyer,et al.  Cell-type specific properties of pyramidal neurons in neocortex underlying a layout that is modifiable depending on the cortical area. , 2010, Cerebral cortex.

[15]  Jianing Yu,et al.  Top-down laminar organization of the excitatory network in motor cortex , 2008, Nature Neuroscience.

[16]  R. Reep,et al.  Overlap and interdigitation of cortical and thalamic afferents to dorsocentral striatum in the rat , 2005, Brain Research.

[17]  Yasuo Kawaguchi,et al.  Firing-Pattern-Dependent Specificity of Cortical Excitatory Feed-Forward Subnetworks , 2008, The Journal of Neuroscience.

[18]  M. Deschenes,et al.  Corticothalamic projections from layer V cells in rat are collaterals of long-range corticofugal axons , 1994, Brain Research.

[19]  R. S. Waters,et al.  Organization of the Mouse Motor Cortex Studied by Retrograde Tracing and Intracortical Microstimulation (ICMS) Mapping , 1991, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[20]  T. Kaneko,et al.  Predominant information transfer from layer III pyramidal neurons to corticospinal neurons , 2000, The Journal of comparative neurology.

[21]  G. Shepherd,et al.  Geometric and functional organization of cortical circuits , 2005, Nature Neuroscience.

[22]  Taro Kiritani,et al.  Frontiers in Neural Circuits Neural Circuits Local-circuit Phenotypes of Layer 5 Neurons in Motor-frontal Cortex of Yfp-h Mice , 2022 .

[23]  S. Nelson,et al.  Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. , 2007, Journal of neurophysiology.

[24]  T. Murphy,et al.  Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice , 2009, Nature Methods.

[25]  S. Hestrin,et al.  Cell-type identity: a key to unlocking the function of neocortical circuits , 2009, Current Opinion in Neurobiology.

[26]  D. Tank,et al.  Functional Clustering of Neurons in Motor Cortex Determined by Cellular Resolution Imaging in Awake Behaving Mice , 2009, The Journal of Neuroscience.

[27]  A. Laverghetta,et al.  Differential morphology of pyramidal tract‐type and intratelencephalically projecting‐type corticostriatal neurons and their intrastriatal terminals in rats , 2003, The Journal of comparative neurology.

[28]  Gordon M. G. Shepherd,et al.  Intracortical Cartography in an Agranular Area , 2009, Front. Neurosci..

[29]  Robert H. Brown,et al.  Molecular biology of amyotrophic lateral sclerosis: insights from genetics , 2006, Nature Reviews Neuroscience.

[30]  Alex S. Ferecskó,et al.  Local Potential Connectivity in Cat Primary Visual Cortex , 2008 .

[31]  P. Arlotta,et al.  Neuronal subtype specification in the cerebral cortex , 2007, Nature Reviews Neuroscience.

[32]  D. Chklovskii,et al.  Neurogeometry and potential synaptic connectivity , 2005, Trends in Neurosciences.

[33]  B. Alstermark,et al.  Lack of monosynaptic corticomotoneuronal EPSPs in rats: disynaptic EPSPs mediated via reticulospinal neurons and polysynaptic EPSPs via segmental interneurons. , 2004, Journal of neurophysiology.

[34]  P. Strick,et al.  Muscle representation in the macaque motor cortex: an anatomical perspective. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[35]  T. Hirano,et al.  Evidence for Activity-Dependent Cortical Wiring: Formation of Interhemispheric Connections in Neonatal Mouse Visual Cortex Requires Projection Neuron Activity , 2007, The Journal of Neuroscience.

[36]  S. Hestrin,et al.  Intracortical circuits of pyramidal neurons reflect their long-range axonal targets , 2009, Nature.

[37]  P. Strick,et al.  Subdivisions of primary motor cortex based on cortico-motoneuronal cells , 2009, Proceedings of the National Academy of Sciences.

[38]  S M Sherman,et al.  Rapid and sensitive mapping of long-range connections in vitro using flavoprotein autofluorescence imaging combined with laser photostimulation. , 2009, Journal of neurophysiology.

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

[40]  R. Douglas,et al.  Neuronal circuits of the neocortex. , 2004, Annual review of neuroscience.

[41]  M. Deschenes,et al.  Corticostriatal projections from layer V cells in rat are collaterals of long-range corticofugal axons , 1996, Brain Research.

[42]  R. Douglas,et al.  A Quantitative Map of the Circuit of Cat Primary Visual Cortex , 2004, The Journal of Neuroscience.

[43]  Bartlett W. Mel,et al.  Cortical rewiring and information storage , 2004, Nature.

[44]  J. Lübke,et al.  Morphometric analysis of the columnar innervation domain of neurons connecting layer 4 and layer 2/3 of juvenile rat barrel cortex. , 2003, Cerebral cortex.

[45]  C. G. Phillips,et al.  Corticospinal neurones. Their role in movement. , 1977, Monographs of the Physiological Society.

[46]  Kevan A. C. Martin,et al.  Topology and dynamics of the canonical circuit of cat V1 , 2009, Neural Networks.

[47]  Francois Gonon,et al.  Intratelencephalic corticostriatal neurons equally excite striatonigral and striatopallidal neurons and their discharge activity is selectively reduced in experimental parkinsonism , 2008, European Journal of Neuroscience.

[48]  Bertrand Fontaine,et al.  Spastin, a new AAA protein, is altered in the most frequent form of autosomal dominant spastic paraplegia , 1999, Nature Genetics.

[49]  C. Stevens,et al.  Neuronal diversity: Too many cell types for comfort? , 1998, Current Biology.

[50]  Lydia Wood,et al.  Synaptic Circuit Abnormalities of Motor-Frontal Layer 2/3 Pyramidal Neurons in an RNA Interference Model of Methyl-CpG-Binding Protein 2 Deficiency , 2009, The Journal of Neuroscience.