A non-canonical striatopallidal Go pathway that supports motor control.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
23 10 2023
Historique:
received: 28 01 2023
accepted: 05 10 2023
medline: 27 10 2023
pubmed: 24 10 2023
entrez: 23 10 2023
Statut: epublish

Résumé

In the classical model of the basal ganglia, direct pathway striatal projection neurons (dSPNs) send projections to the substantia nigra (SNr) and entopeduncular nucleus to regulate motor function. Recent studies have re-established that dSPNs also possess axon collaterals within the globus pallidus (GPe) (bridging collaterals), yet the significance of these collaterals for behavior is unknown. Here we use in vivo optical and chemogenetic tools combined with deep learning approaches in mice to dissect the roles of dSPN GPe collaterals in motor function. We find that dSPNs projecting to the SNr send synchronous motor-related information to the GPe via axon collaterals. Inhibition of native activity in dSPN GPe terminals impairs motor activity and function via regulation of Npas1 neurons. We propose a model by which dSPN GPe axon collaterals (striatopallidal Go pathway) act in concert with the canonical terminals in the SNr to support motor control by inhibiting Npas1 neurons.

Identifiants

pubmed: 37872145
doi: 10.1038/s41467-023-42288-1
pii: 10.1038/s41467-023-42288-1
pmc: PMC10593790
doi:

Substances chimiques

Npas1 protein, mouse 0
Nerve Tissue Proteins 0
Basic Helix-Loop-Helix Transcription Factors 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

6712

Subventions

Organisme : NIMH NIH HHS
ID : T32 MH018870
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH093672
Pays : United States
Organisme : Intramural NIH HHS
ID : ZIA DA000069
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS069777
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH124858
Pays : United States
Organisme : NINDS NIH HHS
ID : R56 NS069777
Pays : United States

Commentaires et corrections

Type : UpdateOf

Informations de copyright

© 2023. Springer Nature Limited.

Références

Gerfen, C. R. & Surmeier, D. J. Modulation of striatal projection systems by dopamine. Annu. Rev. Neurosci. 34, 441–466 (2011).
pubmed: 21469956 pmcid: 3487690
Cox, J. & Witten, I. B. Striatal circuits for reward learning and decision-making. Nat. Rev. Neurosci. 20, 482–494 (2019).
pubmed: 31171839 pmcid: 7231228
Klaus, A., Alves da Silva, J. & Costa, R. M. What, if, and when to move: basal ganglia circuits and self-paced action initiation. Annu. Rev. Neurosci. 42, 459–483 (2019).
pubmed: 31018098
Xiao, X. et al. A genetically defined compartmentalized striatal direct pathway for negative reinforcement. Cell 183, 211–227.e20 (2020).
pubmed: 32937106 pmcid: 8605319
Lee, J. & Sabatini, B. L. Striatal indirect pathway mediates exploration via collicular competition. Nature 599, 645–649 (2021).
pubmed: 34732888 pmcid: 10281058
Cazorla, M. et al. Dopamine D2 receptors regulate the anatomical and functional balance of basal ganglia circuitry. Neuron 81, 153–164 (2014).
pubmed: 24411738 pmcid: 3899717
Dobbs, L. K. et al. D1 receptor hypersensitivity in mice with low striatal D2 receptors facilitates select cocaine behaviors. Neuropsychopharmacology 44, 805–816 (2019).
pubmed: 30504927
Parent, A. et al. Organization of the basal ganglia: the importance of axonal collateralization. Trends Neurosci. 23, S20–S27 (2000).
pubmed: 11052216
Taverna, S., Ilijic, E. & Surmeier, D. J. Recurrent collateral connections of striatal medium spiny neurons are disrupted in models of Parkinson’s disease. J. Neurosci. 28, 5504–5512 (2008).
pubmed: 18495884 pmcid: 3235738
McElvain, L. E. et al. Specific populations of basal ganglia output neurons target distinct brain stem areas while collateralizing throughout the diencephalon. Neuron 109, 1721–1738.e4 (2021).
pubmed: 33823137 pmcid: 8169061
Prensa, L., Giménez-Amaya, J. M., Parent, A., Bernácer, J. & Cebrián, C. The Nigrostriatal Pathway: Axonal Collateralization and Compartmental Specificity. in Birth, Life and Death of Dopaminergic Neurons in the Substantia Nigra (eds. Giovanni, G., Di Matteo, V. & Esposito, E.) 49–58 (Springer, 2009).
Fujiyama, F. et al. Exclusive and common targets of neostriatofugal projections of rat striosome neurons: a single neuron-tracing study using a viral vector. Eur. J. Neurosci. 33, 668–677 (2011).
pubmed: 21314848
Kawaguchi, Y., Wilson, C. J. & Emson, P. C. Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin. J. Neurosci. 10, 3421–3438 (1990).
pubmed: 1698947 pmcid: 6570194
Wu, Y., Richard, S. & Parent, A. The organization of the striatal output system: a single-cell juxtacellular labeling study in the rat. Neurosci. Res. 38, 49–62 (2000).
pubmed: 10997578
Aristieta, A. et al. A disynaptic circuit in the globus pallidus controls locomotion inhibition. Curr. Biol. 31, 707–721.e7 (2021).
pubmed: 33306949
Cui, Q. et al. Striatal direct pathway targets Npas1+ pallidal neurons. J. Neurosci. 41, 3966–3987 (2021).
Ketzef, M. & Silberberg, G. Differential synaptic input to external globus pallidus neuronal subpopulatons in vivo. Neuron 109, 516–529.e4 (2021).
pubmed: 33248017
Lilascharoen, V. et al. Divergent pallidal pathways underlying distinct Parkinsonian behavioral deficits. Nat. Neurosci. 24, 504–515 (2021).
pubmed: 33723433 pmcid: 8907079
Johansson, Y. & Ketzef, M. Sensory processing in external globus pallidus neurons. Cell Rep. 42, 111952 (2023).
pubmed: 36640317
Abdi, A. et al. Prototypic and arkypallidal neurons in the dopamine-intact external globus pallidus. J. Neurosci. 35, 6667–6688 (2015).
pubmed: 25926446 pmcid: 4412890
Glajch et al. Npas1+ pallidal neurons target striatal projection neurons. J. Neurosci. 36, 5472–5488 (2016).
pubmed: 27194328 pmcid: 4871984
Mallet, N. et al. Arkypallidal cells send a stop signal to striatum. Neuron 89, 308–316 (2016).
pubmed: 26777273 pmcid: 4871723
Mallet, N. et al. Dichotomous organization of the external globus pallidus. Neuron 74, 1075–1086 (2012).
pubmed: 22726837 pmcid: 3407962
Lee, Y. et al. Dynamic changes in the bridging collaterals of the basal ganglia circuitry control stress-related behaviors in mice. Mol. Cells 43, 360–372 (2020).
pubmed: 31940718 pmcid: 7191043
Mahn, M., Prigge, M., Ron, S., Levy, R. & Yizhar, O. Biophysical constraints of optogenetic inhibition at presynaptic terminals. Nat. Neurosci. 19, 554–556 (2016).
pubmed: 26950004 pmcid: 4926958
Bonnavion P. et al. Unexpected contributions of striatal projection neurons coexpressing dopamine D1 and D2 receptors in balancing motor control. Preprint at bioRxiv https://doi.org/10.1101/2022.04.05.487163 (2023).
Borgkvist, A. et al. Loss of striatonigral GABAergic presynaptic inhibition enables motor sensitization in Parkinsonian mice. Neuron 87, 976–988 (2015).
pubmed: 26335644 pmcid: 4559856
Freeze, B. S., Kravitz, A. V., Hammack, N., Berke, J. D. & Kreitzer, A. C. Control of basal ganglia output by direct and indirect pathway projection neurons. J. Neurosci. 33, 18531–18539 (2013).
pubmed: 24259575 pmcid: 3834057
Keifman, E. et al. Optostimulation of striatonigral terminals in substantia nigra induces dyskinesia that increases after L-DOPA in a mouse model of Parkinson’s disease. Br. J. Pharm. 176, 2146–2161 (2019).
Kravitz, A. V. et al. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466, 622–626 (2010).
pubmed: 20613723 pmcid: 3552484
Liu, C. et al. An action potential initiation mechanism in distal axons for the control of dopamine release. Science 375, 1378–1385 (2022).
pubmed: 35324301 pmcid: 9081985
Kramer, P. F. et al. Synaptic-like axo-axonal transmission from striatal cholinergic interneurons onto dopaminergic fibers. Neuron 110, 2949–2960.e4 (2022).
pubmed: 35931070 pmcid: 9509469
Kupferschmidt, D. A., Juczewski, K., Cui, G., Johnson, K. A. & Lovinger, D. M. Parallel, but dissociable, processing in discrete corticostriatal inputs encodes skill learning. Neuron 96, 476–489.e5 (2017).
pubmed: 29024667 pmcid: 5663197
Kress, G. J. & Mennerick, S. Action potential initiation and propagation: upstream influences on neurotransmission. Neuroscience 158, 211–222 (2009).
pubmed: 18472347
Sitzia, G., Abrahao, K. P., Liput, D., Calandra, G. M. & Lovinger, D. M. Distinct mechanisms of CB
Mizuno, T., Schmauss, C. & Rayport, S. Distinct roles of presynaptic dopamine receptors in the differential modulation of the intrinsic synapses of medium-spiny neurons in the nucleus accumbens. BMC Neurosci. 8, 8 (2007).
pubmed: 17239247 pmcid: 1783657
Ali, F. & Kwan, A. C. Interpreting in vivo calcium signals from neuronal cell bodies, axons, and dendrites: a review. NPh 7, 011402 (2019).
Arber, S. & Costa, R. M. Networking brainstem and basal ganglia circuits for movement. Nat. Rev. Neurosci. https://doi.org/10.1038/s41583-022-00581-w (2022).
Benthall, K. N., Cording, K. R., Agopyan-Miu, A. H. C. W., Chen, E. Y. & Bateup, H. S. Loss of Tsc1 from striatal direct pathway neurons impairs endocannabinoid-LTD and enhances motor routine learning. Cell Rep. 36, 109511 (2021).
Costa, R. M., Cohen, D. & Nicolelis, M. A. L. Differential corticostriatal plasticity during fast and slow motor skill learning in mice. Curr. Biol. 14, 1124–1134 (2004).
pubmed: 15242609
Dang, M. T. et al. Disrupted motor learning and long-term synaptic plasticity in mice lacking NMDAR1 in the striatum. Proc. Natl Acad. Sci. USA 103, 15254–15259 (2006).
pubmed: 17015831 pmcid: 1622809
Durieux, P. F., Schiffmann, S. N. & de Kerchove d’Exaerde, A. Differential regulation of motor control and response to dopaminergic drugs by D1R and D2R neurons in distinct dorsal striatum subregions. EMBO J. 31, 640–653 (2012).
pubmed: 22068054
Fobbs, W. C. et al. Continuous representations of speed by striatal medium spiny neurons. J. Neurosci. 40, 1679–1688 (2020).
pubmed: 31953369 pmcid: 7046334
Perez, S. et al. Striatum expresses region-specific plasticity consistent with distinct memory abilities. Cell Rep. 38, 110521 (2022).
pubmed: 35294877
Rothwell, P. E. et al. Autism-associated neuroligin-3 mutations commonly impair striatal circuits to boost repetitive behaviors. Cell 158, 198–212 (2014).
pubmed: 24995986 pmcid: 4120877
Yin, H. H. et al. Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat. Neurosci. 12, 333–341 (2009).
pubmed: 19198605 pmcid: 2774785
Dana, H. et al. High-performance calcium sensors for imaging activity in neuronal populations and microcompartments. Nat. Methods 16, 649–657 (2019).
pubmed: 31209382
Markowitz, J. E. et al. The striatum organizes 3D behavior via moment-to-moment action selection. Cell 174, 44–58.e17 (2018).
pubmed: 29779950 pmcid: 6026065
Jin, X., Tecuapetla, F. & Costa, R. M. Basal ganglia subcircuits distinctively encode the parsing and concatenation of action sequences. Nat. Neurosci. 17, 423–430 (2014).
pubmed: 24464039 pmcid: 3955116
Mathis, A. et al. DeepLabCut: markerless pose estimation of user-defined body parts with deep learning. Nat. Neurosci. 21, 1281–1289 (2018).
pubmed: 30127430
Cao, V. Y. et al. Motor learning consolidates arc-expressing neuronal ensembles in secondary motor cortex. Neuron 86, 1385–1392 (2015).
pubmed: 26051420 pmcid: 4474764
Koester, H. J. & Sakmann, B. Calcium dynamics associated with action potentials in single nerve terminals of pyramidal cells in layer 2/3 of the young rat neocortex. J. Physiol. 529, 625–646 (2000).
pubmed: 11118494 pmcid: 2270226
Broussard, G. J. et al. In vivo measurement of afferent activity with axon-specific calcium imaging. Nat. Neurosci. 21, 1272–1280 (2018).
pubmed: 30127424 pmcid: 6697169
Zhang, Y. et al. Fast and sensitive GCaMP calcium indicators for imaging neural populations. Nature 615, 884–891 (2023).
pubmed: 36922596 pmcid: 10060165
Stachniak, T. J., Ghosh, A. & Sternson, S. M. Chemogenetic synaptic silencing of neural circuits localizes a hypothalamus→midbrain pathway for feeding behavior. Neuron 82, 797–808 (2014).
pubmed: 24768300 pmcid: 4306349
Pardo-Garcia, T. R. et al. Ventral pallidum is the primary target for accumbens D1 projections driving cocaine seeking. J. Neurosci. 39, 2041–2051 (2019).
pubmed: 30622165 pmcid: 6507080
Gomez, J. L. et al. Chemogenetics revealed: DREADD occupancy and activation via converted clozapine. Science 357, 503–507 (2017).
pubmed: 28774929 pmcid: 7309169
Mahn, M. et al. Efficient optogenetic silencing of neurotransmitter release with a mosquito rhodopsin. Neuron 109, 1621–1635.e8 (2021).
pubmed: 33979634 pmcid: 7611984
Dodson, P. D. et al. Distinct developmental origins manifest in the specialized encoding of movement by adult neurons of the external globus pallidus. Neuron 86, 501–513 (2015).
pubmed: 25843402 pmcid: 4416107
Abrahao, K. P. & Lovinger, D. M. Classification of GABAergic neuron subtypes from the globus pallidus using wild-type and transgenic mice. J. Physiol. 596, 4219–4235 (2018).
pubmed: 29917235 pmcid: 6117588
Courtney, C. D., Pamukcu, A. & Chan, C. S. Cell and circuit complexity of the external globus pallidus. Nat. Neurosci. 26, 1147–1159 (2023).
Cui, Q. et al. Dissociable roles of pallidal neuron subtypes in regulating motor patterns. J. Neurosci. https://doi.org/10.1523/JNEUROSCI.2210-20.2021 (2021).
Pamukcu, A. et al. Parvalbumin+ and Npas1+ pallidal neurons have distinct circuit topology and function. J. Neurosci. 40, 7855–7876 (2020).
pubmed: 32868462 pmcid: 7548687
Hernández, V. M. et al. Parvalbumin+ neurons and Npas1+ neurons are distinct neuron classes in the mouse external globus pallidus. J. Neurosci. 35, 11830–11847 (2015).
pubmed: 26311767 pmcid: 4549397
Saunders, A. et al. A direct GABAergic output from the basal ganglia to frontal cortex. Nature 521, 85–89 (2015).
pubmed: 25739505 pmcid: 4425585
Hangya, B., Ranade, S. P., Lorenc, M. & Kepecs, A. Central cholinergic neurons are rapidly recruited by reinforcement feedback. Cell 162, 1155–1168 (2015).
pubmed: 26317475 pmcid: 4833212
Browne, T. J., Hughes, D. I., Dayas, C. V., Callister, R. J. & Graham, B. A. Projection neuron axon collaterals in the dorsal horn: placing a new player in spinal cord pain processing. Front. Physiol. 11, 560802 (2020).
pubmed: 33408637 pmcid: 7779806
Rockland, K. S. Axon collaterals and brain states. Front. Syst. Neurosci. 12, 32 (2018).
pubmed: 30065635 pmcid: 6056639
Nelson, A., Abdelmesih, B. & Costa, R. M. Corticospinal populations broadcast complex motor signals to coordinated spinal and striatal circuits. Nat. Neurosci. 24, 1721–1732 (2021).
pubmed: 34737448 pmcid: 8639707
Lee, J., Wang, W. & Sabatini, B. L. Anatomically segregated basal ganglia pathways allow parallel behavioral modulation. Nat. Neurosci. 23, 1388–1398 (2020).
pubmed: 32989293 pmcid: 7606600
Corbit, V. L. et al. Pallidostriatal projections promote β oscillations in a dopamine-depleted biophysical network model. J. Neurosci. 36, 5556–5571 (2016).
pubmed: 27194335 pmcid: 4871989
Baker, M. et al. External globus pallidus input to the dorsal striatum regulates habitual seeking behavior in male mice. Nat. Commun. 14, 4085 (2023).
pubmed: 37438336 pmcid: 10338526
Burke, D. A., Rotstein, H. G. & Alvarez, V. A. Striatal local circuitry: a new framework for lateral inhibition. Neuron 96, 267–284 (2017).
pubmed: 29024654 pmcid: 5649445
Abecassis, Z. A. et al. Npas1 + -Nkx2.1+ neurons are an integral part of the cortico-pallido-cortical loop. J. Neurosci. 40, 743–768 (2020).
pubmed: 31811030 pmcid: 6975296
Spix, T. A. et al. Population-specific neuromodulation prolongs therapeutic benefits of deep brain stimulation. Science 374, 201–206 (2021).
pubmed: 34618556
Saunders, A., Huang, K. W. & Sabatini, B. L. Globus pallidus externus neurons expressing parvalbumin interconnect the subthalamic nucleus and striatal interneurons. PLoS ONE 11, e0149798 (2016).
pubmed: 26905595 pmcid: 4764347
Guillery, R. W. & Sherman, S. M. Branched thalamic afferents: what are the messages that they relay to the cortex? Brain Res. Rev. 66, 205–219 (2011).
pubmed: 20696186
Straka, H., Simmers, J. & Chagnaud, B. P. A new perspective on predictive motor signaling. Curr. Biol. 28, R232–R243 (2018).
pubmed: 29510116
Franks, K. M. et al. Recurrent circuitry dynamically shapes the activation of piriform cortex. Neuron 72, 49–56 (2011).
pubmed: 21982368 pmcid: 3219421
Witter, L., Rudolph, S., Pressler, R. T., Lahlaf, S. I. & Regehr, W. G. Purkinje cell collaterals enable output signals from the cerebellar cortex to feed back to purkinje cells and interneurons. Neuron 91, 312–319 (2016).
pubmed: 27346533 pmcid: 4969194
Chuhma, N., Tanaka, K. F., Hen, R. & Rayport, S. Functional connectome of the striatal medium spiny neuron. J. Neurosci. 31, 1183–1192 (2011).
pubmed: 21273403 pmcid: 3074638
Moehle, M. S. et al. Cholinergic projections to the Substantia Nigra Pars Reticulata inhibit dopamine modulation of basal ganglia through the M4 muscarinic receptor. Neuron 96, 1358–1372.e4 (2017).
pubmed: 29268098 pmcid: 5753765
Soria-Gomez, E. et al. Subcellular specificity of cannabinoid effects in striatonigral circuits. Neuron 109, 1513–1526.e11 (2021).
pubmed: 33770505
Connelly, W. M., Schulz, J. M., Lees, G. & Reynolds, J. N. J. Differential short-term plasticity at convergent inhibitory synapses to the Substantia Nigra Pars Reticulata. J. Neurosci. 30, 14854–14861 (2010).
pubmed: 21048144 pmcid: 6633647
Acebes, A. & Ferrús, A. Cellular and molecular features of axon collaterals and dendrites. Trends Neurosci. 23, 557–565 (2000).
pubmed: 11074265
Baimel, C., McGarry, L. M. & Carter, A. G. The projection targets of medium spiny neurons govern cocaine-evoked synaptic plasticity in the nucleus accumbens. Cell Rep. 28, 2256–2263.e3 (2019).
pubmed: 31461643 pmcid: 6733522
Soares-Cunha, C. et al. Nucleus accumbens medium spiny neurons subtypes signal both reward and aversion. Mol. Psychiatry 25, 3241–3255 (2020).
pubmed: 31462765
Mizutani, K., Takahashi, S., Okamoto, S., Karube, F. & Fujiyama, F. Substance P effects exclusively on prototypic neurons in mouse globus pallidus. Brain Struct. Funct. 222, 4089–4110 (2017).
pubmed: 28608288
Armbruster, B. N., Li, X., Pausch, M. H., Herlitze, S. & Roth, B. L. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc. Natl Acad. Sci. USA 104, 5163–5168 (2007).
pubmed: 17360345 pmcid: 1829280
Gallo, E. F. et al. Accumbens dopamine D2 receptors increase motivation by decreasing inhibitory transmission to the ventral pallidum. Nat. Commun. 9, 1086 (2018).
pubmed: 29540712 pmcid: 5852096
Wess, J., Nakajima, K. & Jain, S. Novel designer receptors to probe GPCR signaling and physiology. Trends Pharm. Sci. 34, 385–392 (2013).
pubmed: 23769625
Labouesse, M. A., Sun, X., Greenwald, J. & Kellendonk, C. DeepLabCut network trained to track mouse ‘back’ body parts during rotarod running (back-view). https://doi.org/10.5281/zenodo.6448813 (2022).
Labouesse, M. A., Gershbaum, S., Greenwald, J. & Kellendonk, C. DeepLabCut network trained to track mouse body parts during open field locomotion (top-down view). https://doi.org/10.5281/zenodo.6448595 (2022).
Labouesse, M. A., Torres-Herraez, A., Greenwald, J. & Kellendonk, C. Code used to analyze data published in Labouesse et al., Nat. Commun. 2023. https://doi.org/10.6084/m9.figshare.23609595.v5 (2023).

Auteurs

Marie A Labouesse (MA)

Department of Psychiatry, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, NY, 10032, USA. marie.labouesse@hest.ethz.ch.
Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY, 10032, USA. marie.labouesse@hest.ethz.ch.
Department of Health, Sciences and Technology, ETH Zurich, 8092, Zurich, Switzerland. marie.labouesse@hest.ethz.ch.
Neuroscience Center Zurich, ETH Zurich and University of Zurich, 8057, Zurich, Switzerland. marie.labouesse@hest.ethz.ch.

Arturo Torres-Herraez (A)

Department of Psychiatry, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, NY, 10032, USA.
Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY, 10032, USA.

Muhammad O Chohan (MO)

Department of Psychiatry, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, NY, 10032, USA.
Division of Child and Adolescent Psychiatry, New York State Psychiatric Institute, New York, NY, 10032, USA.

Joseph M Villarin (JM)

Department of Psychiatry, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, NY, 10032, USA.
Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY, 10032, USA.

Julia Greenwald (J)

Department of Psychiatry, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, NY, 10032, USA.
Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY, 10032, USA.

Xiaoxiao Sun (X)

Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY, 10032, USA.
Department of Biomedical Engineering, Columbia University, New York, NY, 10027, USA.

Mysarah Zahran (M)

Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY, 10032, USA.
Barnard College, Columbia University, New York, NY, 10027, USA.

Alice Tang (A)

Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY, 10032, USA.
Columbia College, Columbia University, New York, NY, 10027, USA.

Sherry Lam (S)

Biobehavioral Imaging and Molecular Neuropsychopharmacology Unit, National Institute on Drug Abuse Intramural Research Program, Baltimore, MD, 21224, USA.

Jeremy Veenstra-VanderWeele (J)

Department of Psychiatry, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, NY, 10032, USA.
Division of Child and Adolescent Psychiatry, New York State Psychiatric Institute, New York, NY, 10032, USA.

Clay O Lacefield (CO)

Department of Psychiatry, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, NY, 10032, USA.
Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY, 10032, USA.

Jordi Bonaventura (J)

Biobehavioral Imaging and Molecular Neuropsychopharmacology Unit, National Institute on Drug Abuse Intramural Research Program, Baltimore, MD, 21224, USA.
Departament de Patologia i Terapèutica Experimental, Institut de Neurociències, L'Hospitalet de Llobregat, Universitat de Barcelona, Barcelona, Spain.

Michael Michaelides (M)

Biobehavioral Imaging and Molecular Neuropsychopharmacology Unit, National Institute on Drug Abuse Intramural Research Program, Baltimore, MD, 21224, USA.
Department of Psychiatry & Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, MD, 21205, USA.

C Savio Chan (CS)

Department of Neuroscience, Feinberg School of Medicine, Northwestern University, Chicago, IL, 60611, USA.

Ofer Yizhar (O)

Departments of Brain Sciences and Molecular Neuroscience, Weizmann Institute of Science, Rehovot, 76100, Israel.

Christoph Kellendonk (C)

Department of Psychiatry, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, NY, 10032, USA. ck491@cumc.columbia.edu.
Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY, 10032, USA. ck491@cumc.columbia.edu.
Department of Molecular Pharmacology & Therapeutics, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, NY, 10032, USA. ck491@cumc.columbia.edu.

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