Phenotypic variation within and across transcriptomic cell types in mouse motor cortex

Cortical neurons exhibit astounding diversity in gene expression as well as in morphological and electrophysiological properties. Most existing neural taxonomies are based on either transcriptomic or morpho-electric criteria, as it has been technically challenging to study both aspects of neuronal diversity in the same set of cells. Here we used Patch-seq to combine patch-clamp recording, biocytin staining, and single-cell RNA sequencing of over 1300 neurons in adult mouse motor cortex, providing a comprehensive morpho-electric annotation of almost all transcriptomically defined neural cell types. We found that, although broad families of transcriptomic types (Vip, Pvalb, Sst, etc.) had distinct and essentially non-overlapping morpho-electric phenotypes, individual transcriptomic types within the same family were not well-separated in the morpho-electric space. Instead, there was a continuum of variability in morphology and electrophysiology, with neighbouring transcriptomic cell types showing similar morpho-electric features, often without clear boundaries between them. Our results suggest that neural types in the neocortex do not always form discrete entities. Instead, neurons follow a hierarchy consisting of distinct non-overlapping branches at the level of families, but can form continuous and correlated transcriptomic and morpho-electrical landscapes within families.

[1]  H. Markram,et al.  Anatomy and physiology of the thick-tufted layer 5 pyramidal neuron , 2015, Front. Cell. Neurosci..

[2]  G. Fishell,et al.  Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons , 2011, Developmental neurobiology.

[3]  Oscar Marín,et al.  Tuning of fast-spiking interneuron properties by an activity-dependent transcriptional switch , 2015, Science.

[4]  Christof Koch,et al.  Adult Mouse Cortical Cell Taxonomy by Single Cell Transcriptomics , 2016, Nature Neuroscience.

[5]  Shreejoy J. Tripathy,et al.  Assessing Transcriptome Quality in Patch-Seq Datasets , 2018, Front. Mol. Neurosci..

[6]  James G. King,et al.  Reconstruction and Simulation of Neocortical Microcircuitry , 2015, Cell.

[7]  Z Josh Huang,et al.  The diversity of GABAergic neurons and neural communication elements , 2019, Nature Reviews Neuroscience.

[8]  Jean Rossier,et al.  Diversity of GABAergic interneurons in layer VIa and VIb of mouse barrel cortex. , 2013, Cerebral cortex.

[9]  N. Seidah,et al.  Regulation by gastric acid of the processing of progastrin‐derived peptides in rat antral mucosa , 1997, The Journal of physiology.

[10]  Carol Ann Paul,et al.  The nissl stain: a stain for cell bodies in brain sections. , 2008, CSH protocols.

[11]  Alex M. Thomson,et al.  Neocortical Layer 6, A Review , 2010, Front. Neuroanat..

[12]  Jochen F. Staiger,et al.  Characterizing VIP Neurons in the Barrel Cortex of VIPcre/tdTomato Mice Reveals Layer-Specific Differences , 2015, Cerebral cortex.

[13]  Jason C. Wester,et al.  Hippocampal GABAergic Inhibitory Interneurons. , 2017, Physiological reviews.

[14]  Thomas R. Gingeras,et al.  STAR: ultrafast universal RNA-seq aligner , 2013, Bioinform..

[15]  Yaoyao Li,et al.  A simplified morphological classification scheme for pyramidal cells in six layers of primary somatosensory cortex of juvenile rats , 2018, IBRO Reports.

[16]  J. Ngai,et al.  Perspectives on defining cell types in the brain , 2019, Current Opinion in Neurobiology.

[17]  Oscar Marín,et al.  Development and Functional Diversification of Cortical Interneurons , 2018, Neuron.

[18]  Kenneth D Harris,et al.  Classes and continua of hippocampal CA1 inhibitory neurons revealed by single-cell transcriptomics , 2017, bioRxiv.

[19]  Allan R. Jones,et al.  Shared and distinct transcriptomic cell types across neocortical areas , 2017, bioRxiv.

[20]  Henry Markram,et al.  Objective Morphological Classification of Neocortical Pyramidal Cells , 2019, Cerebral cortex.

[21]  Juan Carlos Fernández,et al.  Multiobjective evolutionary algorithms to identify highly autocorrelated areas: the case of spatial distribution in financially compromised farms , 2014, Ann. Oper. Res..

[22]  R. Masland Neuronal cell types , 2004, Current Biology.

[23]  Hongkui Zeng,et al.  Neuronal cell-type classification: challenges, opportunities and the path forward , 2017, Nature Reviews Neuroscience.

[24]  Philipp Berens,et al.  The art of using t-SNE for single-cell transcriptomics , 2019, Nature Communications.

[25]  Stefan Steinerberger,et al.  Fast Interpolation-based t-SNE for Improved Visualization of Single-Cell RNA-Seq Data , 2017, Nature Methods.

[26]  Philipp Berens,et al.  The art of using t-SNE for single-cell transcriptomics , 2018, Nature Communications.

[27]  Mark S. Cembrowski,et al.  Spatial Gene-Expression Gradients Underlie Prominent Heterogeneity of CA1 Pyramidal Neurons , 2016, Neuron.

[28]  Shawn R. Olsen,et al.  Translaminar Inhibitory Cells Recruited by Layer 6 Corticothalamic Neurons Suppress Visual Cortex , 2014, Neuron.

[29]  Andreas S Tolias,et al.  Multimodal profiling of single-cell morphology, electrophysiology, and gene expression using Patch-seq , 2017, Nature Protocols.

[30]  Yuchio Yanagawa,et al.  Integration of electrophysiological recordings with single-cell RNA-seq data identifies novel neuronal subtypes , 2015, Nature Biotechnology.

[31]  S. Linnarsson,et al.  Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq , 2015, Science.

[32]  William Muñoz,et al.  Layer-specific modulation of neocortical dendritic inhibition during active wakefulness , 2017, Science.

[33]  S. Phinn,et al.  Australian vegetated coastal ecosystems as global hotspots for climate change mitigation , 2019, Nature Communications.

[34]  Theofanis Karayannis,et al.  Neuronal activity is required for the development of specific cortical interneuron subtypes , 2011, Nature.

[35]  Kenneth D Harris,et al.  A genuine layer 4 in motor cortex with prototypical synaptic circuit connectivity , 2014, eLife.

[36]  Alexander S. Ecker,et al.  Principles of connectivity among morphologically defined cell types in adult neocortex , 2015, Science.

[37]  R. Tremblay,et al.  GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits , 2016, Neuron.

[38]  Philipp Berens,et al.  A Systematic Evaluation of Interneuron Morphology Representations for Cell Type Discrimination , 2019, Neuroinformatics.

[39]  Christoph Ziegenhain,et al.  zUMIs - A fast and flexible pipeline to process RNA sequencing data with UMIs , 2017, bioRxiv.

[40]  Shaoqun Zeng,et al.  Brain-wide single neuron reconstruction reveals morphological diversity in molecularly defined striatal, thalamic, cortical and claustral neuron types , 2019, bioRxiv.

[41]  Saumil S. Patel,et al.  Layer 4 of mouse neocortex differs in cell types and circuit organization between sensory areas , 2019, Nature Communications.

[42]  Philipp Berens,et al.  Sparse reduced-rank regression for exploratory visualization of multimodal data sets , 2018, bioRxiv.

[43]  Daniel P. Mossing,et al.  Figures and figure supplements Complementary networks of cortical somatostatin interneurons enforce layer specific control , 2019 .

[44]  Charles R. Gerfen,et al.  Distinct descending motor cortex pathways and their roles in movement , 2017, Nature.

[45]  Gord Fishell,et al.  Genetic and activity-dependent mechanisms underlying interneuron diversity , 2017, Nature Reviews Neuroscience.

[46]  Lars E. Borm,et al.  Molecular Architecture of the Mouse Nervous System , 2018, Cell.

[47]  Manuel Marx,et al.  Morphology and Physiology of Excitatory Neurons in Layer 6b of the Somatosensory Rat Barrel Cortex , 2012, Cerebral cortex.

[48]  Geoffrey E. Hinton,et al.  Visualizing Data using t-SNE , 2008 .

[49]  G. Miyoshi,et al.  Common Origins of Hippocampal Ivy and Nitric Oxide Synthase Expressing Neurogliaform Cells , 2010, The Journal of Neuroscience.

[50]  Allan R. Jones,et al.  Shared and distinct transcriptomic cell types across neocortical areas , 2018, Nature.

[51]  Martin Hemberg,et al.  M3Drop: dropout-based feature selection for scRNASeq , 2018, Bioinform..

[52]  M. Deschenes,et al.  Intracortical Axonal Projections of Lamina VI Cells of the Primary Somatosensory Cortex in the Rat: A Single-Cell Labeling Study , 1997, The Journal of Neuroscience.

[53]  G. Fishell,et al.  Interneuron cell types are fit to function , 2014, Nature.

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

[55]  H. Markram,et al.  Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. , 1997, The Journal of physiology.

[56]  Athanasia G. Palasantza,et al.  Electrophysiological, transcriptomic and morphologic profiling of single neurons using Patch-seq , 2015, Nature Biotechnology.

[57]  Brian R. Lee,et al.  Classification of electrophysiological and morphological neuron types in the mouse visual cortex , 2019, Nature Neuroscience.

[58]  R. Empson,et al.  Diversity of layer 5 projection neurons in the mouse motor cortex , 2013, Front. Cell. Neurosci..

[59]  S. Quake,et al.  Continuous and Discrete Neuron Types of the Adult Murine Striatum , 2019, Neuron.

[60]  Vincent A. Traag,et al.  From Louvain to Leiden: guaranteeing well-connected communities , 2018, Scientific Reports.

[61]  Spyros Darmanis,et al.  Single-cell RNAseq reveals cell adhesion molecule profiles in electrophysiologically defined neurons , 2016, Proceedings of the National Academy of Sciences.

[62]  Ian R. Wickersham,et al.  The BRAIN Initiative Cell Census Consortium: Lessons Learned toward Generating a Comprehensive Brain Cell Atlas , 2017, Neuron.

[63]  Bernardo Rudy,et al.  Diversity and Connectivity of Layer 5 Somatostatin-Expressing Interneurons in the Mouse Barrel Cortex , 2018, The Journal of Neuroscience.

[64]  Kenneth D. Harris,et al.  Diversity of Interneurons in the Dorsal Striatum Revealed by Single-Cell RNA Sequencing and PatchSeq , 2018, Cell reports.

[65]  H. S. Meyer,et al.  Cell Type–Specific Three-Dimensional Structure of Thalamocortical Circuits in a Column of Rat Vibrissal Cortex , 2011, Cerebral cortex.

[66]  Åsa K. Björklund,et al.  Smart-seq2 for sensitive full-length transcriptome profiling in single cells , 2013, Nature Methods.

[67]  Matthew G. Keefe,et al.  Development and Arealization of the Cerebral Cortex , 2019, Neuron.

[68]  G. Fishell,et al.  Four Unique Interneuron Populations Reside in Neocortical Layer 1 , 2018, The Journal of Neuroscience.

[69]  Alison L. Barth,et al.  Somatostatin-expressing neurons in cortical networks , 2016, Nature Reviews Neuroscience.

[70]  M. Scharf,et al.  Rapid evolutionary responses to insecticide resistance management interventions by the German cockroach (Blattella germanica L.) , 2019, Scientific Reports.