Cortical Glutamatergic Projection Neuron Types Contribute to Distinct Functional Subnetworks

Overview

Journal Nat Neurosci

Date 2023 Jan 23

PMID 36690901

Authors

Hemanth Mohan

Xu An

X Hermione Xu

Hideki Kondo

Shengli Zhao

Katherine S Matho

Bor-Shuen Wang

Simon Musall

Partha Mitra

Z Josh Huang

Affiliations

Soon will be listed here.

Abstract

The cellular basis of cerebral cortex functional architecture remains not well understood. A major challenge is to monitor and decipher neural network dynamics across broad cortical areas yet with projection-neuron-type resolution in real time during behavior. Combining genetic targeting and wide-field imaging, we monitored activity dynamics of subcortical-projecting (PT) and intratelencephalic-projecting (IT) types across dorsal cortex of mice during different brain states and behaviors. IT and PT neurons showed distinct activation patterns during wakeful resting, during spontaneous movements and upon sensory stimulation. Distinct IT and PT subnetworks were dynamically tuned to different sensorimotor components of a naturalistic feeding behavior, and optogenetic inhibition of ITs and PTs in subnetwork nodes disrupted distinct components of this behavior. Lastly, IT and PT projection patterns are consistent with their subnetwork activation patterns. Our results show that, in addition to the concept of columnar organization, dynamic areal and projection-neuron-type specific subnetworks are a key feature of cortical functional architecture linking microcircuit components with global brain networks.

Citing Articles

Wide-field calcium imaging of cortical activation and functional connectivity in externally- and internally-driven locomotion.

West S, Gerhart M, Ebner T Nat Commun. 2024; 15(1):7792.

PMID: 39242572 PMC: 11379880. DOI: 10.1038/s41467-024-51816-6.

Functional Dynamics and Selectivity of Two Parallel Corticocortical Pathways from Motor Cortex to Layer 5 Circuits in Somatosensory Cortex.

Kim H, Bonekamp K, Gillie G, Autio D, Keller T, Crandall S eNeuro. 2024; 11(6).

PMID: 38834298 PMC: 11209671. DOI: 10.1523/ENEURO.0154-24.2024.

Organization of corticocortical and thalamocortical top-down inputs in the primary visual cortex.

Liu Y, Zhang J, Jiang Z, Qin M, Xu M, Zhang S Nat Commun. 2024; 15(1):4495.

PMID: 38802410 PMC: 11130321. DOI: 10.1038/s41467-024-48924-8.

Functional dynamics and selectivity of two parallel corticocortical pathways from motor cortex to layer 5 circuits in somatosensory cortex.

Kim H, Bonekamp K, Gillie G, Autio D, Keller T, Crandall S bioRxiv. 2024; .

PMID: 38405888 PMC: 10888929. DOI: 10.1101/2024.02.11.579810.

Wide-field imaging in behaving mice as a tool to study cognitive function.

Gilad A Neurophotonics. 2024; 11(3):033404.

PMID: 38384657 PMC: 10879934. DOI: 10.1117/1.NPh.11.3.033404.

References

Bota M, Sporns O, Swanson L . Architecture of the cerebral cortical association connectome underlying cognition. Proc Natl Acad Sci U S A. 2015; 112(16):E2093-101. PMC: 4413280. DOI: 10.1073/pnas.1504394112. View

Van Essen D, Glasser M . Parcellating Cerebral Cortex: How Invasive Animal Studies Inform Noninvasive Mapmaking in Humans. Neuron. 2018; 99(4):640-663. PMC: 6149530. DOI: 10.1016/j.neuron.2018.07.002. View

Hubel D, Wiesel T . Shape and arrangement of columns in cat's striate cortex. J Physiol. 1963; 165:559-68. PMC: 1359325. DOI: 10.1113/jphysiol.1963.sp007079. View

MOUNTCASTLE V, DAVIES P, BERMAN A . Response properties of neurons of cat's somatic sensory cortex to peripheral stimuli. J Neurophysiol. 1957; 20(4):374-407. DOI: 10.1152/jn.1957.20.4.374. View

Douglas R, Martin K . Mapping the matrix: the ways of neocortex. Neuron. 2007; 56(2):226-38. DOI: 10.1016/j.neuron.2007.10.017. View

Harris K, Shepherd G . The neocortical circuit: themes and variations. Nat Neurosci. 2015; 18(2):170-81. PMC: 4889215. DOI: 10.1038/nn.3917. View

Markram H, Muller E, Ramaswamy S, Reimann M, Abdellah M, Sanchez C . Reconstruction and Simulation of Neocortical Microcircuitry. Cell. 2015; 163(2):456-92. DOI: 10.1016/j.cell.2015.09.029. View

Lerner T, Ye L, Deisseroth K . Communication in Neural Circuits: Tools, Opportunities, and Challenges. Cell. 2016; 164(6):1136-1150. PMC: 5725393. DOI: 10.1016/j.cell.2016.02.027. View

Engel T, Scholvinck M, Lewis C . The diversity and specificity of functional connectivity across spatial and temporal scales. Neuroimage. 2021; 245:118692. PMC: 9531047. DOI: 10.1016/j.neuroimage.2021.118692. View

10.

Huang Z . Toward a genetic dissection of cortical circuits in the mouse. Neuron. 2014; 83(6):1284-302. PMC: 4169123. DOI: 10.1016/j.neuron.2014.08.041. View

11.

Tasic B, Yao Z, Graybuck L, Smith K, Nguyen T, Bertagnolli D . Shared and distinct transcriptomic cell types across neocortical areas. Nature. 2018; 563(7729):72-78. PMC: 6456269. DOI: 10.1038/s41586-018-0654-5. View

12.

Gamanut R, Kennedy H, Toroczkai Z, Ercsey-Ravasz M, Van Essen D, Knoblauch K . The Mouse Cortical Connectome, Characterized by an Ultra-Dense Cortical Graph, Maintains Specificity by Distinct Connectivity Profiles. Neuron. 2018; 97(3):698-715.e10. PMC: 5958229. DOI: 10.1016/j.neuron.2017.12.037. View

13.

Zingg B, Hintiryan H, Gou L, Song M, Bay M, Bienkowski M . Neural networks of the mouse neocortex. Cell. 2014; 156(5):1096-111. PMC: 4169118. DOI: 10.1016/j.cell.2014.02.023. View

14.

Oh S, Harris J, Ng L, Winslow B, Cain N, Mihalas S . A mesoscale connectome of the mouse brain. Nature. 2014; 508(7495):207-14. PMC: 5102064. DOI: 10.1038/nature13186. View

15.

Harris J, Mihalas S, Hirokawa K, Whitesell J, Choi H, Bernard A . Hierarchical organization of cortical and thalamic connectivity. Nature. 2019; 575(7781):195-202. PMC: 8433044. DOI: 10.1038/s41586-019-1716-z. View

16.

Munoz-Castaneda R, Zingg B, Matho K, Chen X, Wang Q, Foster N . Cellular anatomy of the mouse primary motor cortex. Nature. 2021; 598(7879):159-166. PMC: 8494646. DOI: 10.1038/s41586-021-03970-w. View

17.

Gozzi A, Schwarz A . Large-scale functional connectivity networks in the rodent brain. Neuroimage. 2015; 127:496-509. DOI: 10.1016/j.neuroimage.2015.12.017. View

18.

Smith S, Vidaurre D, Beckmann C, Glasser M, Jenkinson M, Miller K . Functional connectomics from resting-state fMRI. Trends Cogn Sci. 2013; 17(12):666-82. PMC: 4004765. DOI: 10.1016/j.tics.2013.09.016. View

19.

Svoboda K, Helmchen F, Denk W, Tank D . Spread of dendritic excitation in layer 2/3 pyramidal neurons in rat barrel cortex in vivo. Nat Neurosci. 1999; 2(1):65-73. DOI: 10.1038/4569. View

20.

Cardin J, Crair M, Higley M . Mesoscopic Imaging: Shining a Wide Light on Large-Scale Neural Dynamics. Neuron. 2020; 108(1):33-43. PMC: 7577373. DOI: 10.1016/j.neuron.2020.09.031. View