Cited by 175Neuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on BehaviorDeep Brain Stimulation and Movement Disorders

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Cholinergic Interneurons Mediate Fast VGluT3-Dependent Glutamatergic Transmission in the Striatum

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Higley, Michael J., Gittis, Aryn H., Oldenburg, Ian A., Balthasar, Nina, Seal, Rebecca P., Edwards, Robert H., Lowell, Bradford B., Kreitzer, Anatol C., Sabatini, Bernardo L.·2011·PLoS ONE

DOI 10.1371/journal.pone.0019155PMC PMC3081336

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Abstract

The neurotransmitter glutamate is released by excitatory projection neurons throughout the brain. However, non-glutamatergic cells, including cholinergic and monoaminergic neurons, express markers that suggest that they are also capable of vesicular glutamate release. Striatal cholinergic interneurons (CINs) express the Type-3 vesicular glutamate transporter (VGluT3), although whether they form functional glutamatergic synapses is unclear. To examine this possibility, we utilized mice expressing Cre-recombinase under control of the endogenous choline acetyltransferase locus and conditionally expressed light-activated Channelrhodopsin2 in CINs. Optical stimulation evoked action potentials in CINs and produced postsynaptic responses in medium spiny neurons that were blocked by glutamate receptor antagonists. CIN-mediated glutamatergic responses exhibited a large contribution of NMDA-type glutamate receptors, distinguishing them from corticostriatal inputs. CIN-mediated glutamatergic responses were insensitive to antagonists of acetylcholine receptors and were not seen in mice lacking VGluT3. Our results indicate that CINs are capable of mediating fast glutamatergic transmission, suggesting a new role for these cells in regulating striatal activity.

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Figure 1 ChR2-mediated activation of striatal cholinergic interneurons. (Ai) Confocal image of mCherry-positive ChR2-expressing neurons in the dorsal striatum of a ChAT-IRES-Cre mouse injected with AAV encoding DFI-ChR2-mCherry. (Aii) Fluorescence immunohistochemical staining for ChAT reveals cholinergic neurons. (Aiii) Merged image. (B) inset, Schematic diagram of the recording conditions: cell-attached recordings were made from ChR2-expressing CINs (red) in the dorsal striatum and blue light was delivered to the surrounding area (blue circle) through the microscope objective. main panel, Example action potential recorded in cell-attached mode from a ChR2-expressing CIN evoked by a 4 ms pulse of 473 nm light.CC BY · PubMed Central

Figure 2 Light-evoked CIN action potentials evoke glutamatergic responses in MSNs. (A) inset, Schematic diagram of the recording conditions: whole-cell recordings were made from MSNs that neighbored ChR2-expressing CINs (red). The blue circle indicates the region stimulated by blue light. main panel, Example EPSP recorded in an MSN in response to a 4 ms light pulse (blue bar). (B) Amplitudes of light-evoked EPSPs in the presence of antagonists of GABAA (Picrotoxin, Ptx), muscarinic (Scopolamine, Scop), and nicotinic (Mecamylamine, Mec) receptors and following application of the AMPA/kainate glutamate receptor antagonist NBQX. (C) Example of light evoked (blue bar) CIN-mediated EPSCs in a voltage-clamped MSN at holding potentials of −70 and +40 mV demonstrating the large current that is visible more than 100 ms after the light pulse at +40 mV. The amplitudes of the rapid −70 and prolonged +40 mV EPSC components were measured in the periods indicated by the gray bars. (D) Confocal image of mCherry-positive ChR2-expressing fibers in the motor cortex, white matter (WM) and underlying striatum (Str). Large bundles of corticofugal fibers (white arrowheads) and diffuse small axonal collaterals are visible throughout the dorsolateral striatum. Scale bar 200 µm. (E) inset, Schematic diagram of the recording conditions: whole-cell recordings were made from MSNs neighboring ChR2-expressing corticostriatal fibers (red), and blue light was delivered to the region indicated by the blue circle. main panel, Example EPSCs recorded in an MSN in response to a blue light pulse at the indicated holding potentials. (F) left, Average amplitudes of light-evoked EPSCs measured in MSNs held at either −70 or +40 mV in response to ChR2-mediated activation of either CINs or corticostriatal fibers (Cx). right, Average ratio of +40/−70 mV current amplitudes measured following ChR2-mediated activation of either CINs or corticostriatal fibers.CC BY · PubMed Central

Figure 3 CIN-mediated glutamatergic currents in MSNs require VGluT3 expression. (A) Example light-evoked EPSCs at 32–34°C in an MSN held at −70 or +40 mV in an acute striatal slice of a DFI-ChR2-mCherry AAV injected ChAT-IRES-Cre mouse. (B) As in Panel A, showing recordings at 32–34°C obtained from an MSN in an acute slice of a DFI-ChR2-mCherry AAV injected GM60 mouse that expresses Cre under control of a BAC spanning the ChAT genomic locus. (C) As in Panel B, showing failures to evoke EPSCs in an MSN of a DFI-ChR2-mCherry AAV injected GM60; VGluT3−/− mouse. (D) Average light-evoked EPSC amplitudes measured in MSNs at holding potentials of −70 and +40 mV in acute slices prepared from mice of the indicated genotypes.CC BY · PubMed Central

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“In particular, using optogenetic approaches it was shown that ChIs are capable of releasing glutamate (Higley et al., 2011; Nelson et al., 2014).”
Distinct synchronization, cortical coupling and behavioral function of two basal forebrain cholinergic neuron types
Laszlovszky, T., Schlingloff, D., Hegedüs, P., Freund, T. F., Gulyás, A. I., Kepecs, Á., & Hangya, B. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0648-0 · Cited by 98
“Ethics oversight Adult (over 2 months old) ChAT-Cre (N = 15, 14/15 male, Higley et al., 2011), ChAT-ChR2 (N = 3, 3/3 male, Zhao et al., 2011) and PV-Cre (n = 4, 4/4 male) mice were used for behavioral recording experiments under the protocol approved by Cold Spring Harbor Laboratory Institutional…”
Biphasic Cholinergic Synaptic Transmission Controls Action Potential Activity in Thalamic Reticular Nucleus Neurons
Sun, Y.-G., Pita‐Almenar, J. D., Wu, C., Renger, J. J., Uebele, V. N., Lu, H., & Beierlein, M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3177-12.2013 · Cited by 79
“Recent studies have demonstrated the synaptic release of glutamate from cholinergic neurons (Higley et al., 2011; Ren et al., 2011).”
Background
Opposing regulation of dopaminergic activity and exploratory motor behavior by forebrain and brainstem cholinergic circuits
Patel, J. C., Rossignol, E., Rice, M. E., & Machold, R. P. (2012) · Nature Communications · doi:10.1038/ncomms2144 · Cited by 80
Protons Regulate Vesicular Glutamate Transporters through an Allosteric Mechanism
Eriksen, J., Chang, R., McGregor, M., Silm, K., Suzuki, T., & Edwards, R. H. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.026 · Cited by 76
Glutamate Cotransmission in Cholinergic, GABAergic and Monoamine Systems: Contrasts and Commonalities
Trudeau, L., & Mestikawy, S. E. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00113 · Cited by 83
“…DA neurons (Sulzer et al., 1998; Bourque and Trudeau, 2000; Hnasko et al., 2010; Tecuapetla et al., 2010; Chuhma et al., 2014; Trudeau et al., 2014), ACh (Huh et al., 2008; Higley et al., 2011; Nelson et al., 2014; Frahm et al., 2015) and GABA neurons (Shabel et al., 2014; Root et al., 2018).”
Basal forebrain subcortical projections
Agostinelli, L. J., Geerling, J. C., & Scammell, T. E. (2019) · Brain Structure and Function · doi:10.1007/s00429-018-01820-6 · Cited by 77
Dopamine facilitates dendritic spine formation by cultured striatal medium spiny neurons through both D1 and D2 dopamine receptors
Fasano, C., Bourque, M.-J., Lapointe, G., Leo, D., Thibault, D., Haber, M., Kortleven, C., DesGroseillers, L., Murai, K. K., & Trudeau, L.-É. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.11.030 · Cited by 67
Colocalization of different neurotransmitter transporters on synaptic vesicles is sparse except for VGLUT1 and ZnT3
Upmanyu, N., Jin, J., Emde, H. V. D., Ganzella, M., Bösche, L., Malviya, V. N., Zhuleku, E., Politi, A. Z., Ninov, M., Silbern, I., et al. (2022) · Neuron · doi:10.1016/j.neuron.2022.02.008 · Cited by 69
“, 2009), or with acetylcholine in striatal interneurons and medial habenula projections (Frahm et al., 2015; Gras et al., 2008; Higley et al., 2011; Ren et al., 2011).”
Background
Illuminating the role of cholinergic signaling in circuits of attention and emotionally salient behaviors
Luchicchi, A., Bloem, B., ViaÃ±a, J. N. M., Mansvelder, H. D., & Role, L. W. (2014) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2014.00024 · Cited by 74
Developmental specification of forebrain cholinergic neurons
Allaway, K. C., & Machold, R. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2016.11.007 · Cited by 68
“However, some of these populations (e.g., striatal cholinergic interneurons) have also been found to express the vesicular glutamate transporter VGLUT3 (slc17a8) and co-release glutamate (Higley et al., 2011), an indication of additional functional heterogeneity.”
Spontaneous Synaptic Activation of Muscarinic Receptors by Striatal Cholinergic Neuron Firing
Mamaligas, A. A., & Ford, C. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.021 · Cited by 70
“, 2012) and the co-release of glutamate from cholinergic interneurons (Higley et al., 2011; Nelson et al., 2014a) onto MSNs.”
Audiogenic Seizures in theFmr1Knock-Out Mouse Are Induced byFmr1Deletion in Subcortical, VGlut2-Expressing Excitatory Neurons and Require Deletion in the Inferior Colliculus
Gonzalez, D., Tomasek, M. P., Hays, S. A., Sridhar, V., Ammanuel, S. G., Chang, C.-W., Pawlowski, K. S., Huber, K. M., & Gibson, J. R. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0886-19.2019 · Cited by 64
“Serotonergic and cholinergic neurons have been reported to release glutamate, but VGlut3 is the transporter in these neurons (Higley et al., 2011; Wang et al., 2019).”
Background
The absence of VGLUT3 predisposes to cocaine abuse by increasing dopamine and glutamate signaling in the nucleus accumbens
Sakae, D. Y., Marti, F., Lecca, S., Vorspan, F., Martín‐García, E., Morel, L. J., Henrion, A., Cuesta, J., Besnard, A., Heck, N., et al. (2015) · Molecular Psychiatry · doi:10.1038/mp.2015.104 · Cited by 68
Regulation of the Hippocampal Network by VGLUT3-Positive CCK- GABAergic Basket Cells
Fasano, C., Rocchetti, J., Pietrajtis, K., Zander, J.-F., Manseau, F., Sakae, D. Y., Marcus-Sells, M., Ramet, L., Morel, L. J., Carrel, D., et al. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00140 · Cited by 67
Glycogen synthase kinase 3 beta alters anxiety-, depression-, and addiction-related behaviors and neuronal activity in the nucleus accumbens shell
Crofton, E. J., Nenov, M. N., Zhang, Y., Scala, F., Page, S. A., McCue, D. L., Li, D., Hommel, J. D., Laezza, F., & Green, T. A. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.01.020 · Cited by 64
“…role of TANs in cocaine addiction with immunotoxin mediated cell ablation resulting in increased sensitivity to cocaine (Hikida et al., 2001) and preventing behavioral abnormalities associated with cocaine induced by centrally active acetylcholinesterase inhibitors in the NAc (Hikida et al., 2003).”
Background
Alcohol exposure disrupts mu opioid receptor-mediated long-term depression at insular cortex inputs to dorsolateral striatum
Muñoz, B., Fritz, B. M., Yin, F., & Atwood, B. K. (2018) · Nature Communications · doi:10.1038/s41467-018-03683-1 · Cited by 63
Loss of VGLUT3 Produces Circadian-Dependent Hyperdopaminergia and Ameliorates Motor Dysfunction and l-Dopa-Mediated Dyskinesias in a Model of Parkinson's Disease
Divito, C. B., Steece‐Collier, K., Case, D. T., Williams, S. G., Stancati, J. A., Zhi, L., Rubio, M. E., Sortwell, C. E., Collier, T. J., Sulzer, D., et al. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2124-15.2015 · Cited by 62
“Therefore, deletion of VGLUT3 from these cells not only abolishes the glutamate signaling (Higley et al., 2011), but also markedly reduces cholinergic transmission (Nelson et al., 2014).”
Background
Dopaminergic Regulation of Striatal Interneurons in Reward and Addiction: Focus on Alcohol
Clarke, R. B. C., & Adermark, L. (2015) · Neural Plasticity · doi:10.1155/2015/814567 · Cited by 68
“Tonically active cholinergic interneurons modulate dopamine output through activation of both muscarinic and nicotinic cholinergic receptors on dopamine terminals [125, 139–141] and through the corelease of glutamate [142, 143].”
Background
Synaptic and circuit functions of multitransmitter neurons in the mammalian brain
Wallace, M. L., & Sabatini, B. L. (2023) · Neuron · doi:10.1016/j.neuron.2023.06.003 · Cited by 59
Self-citation
Linking Cholinergic Interneurons, Synaptic Plasticity, and Behavior during the Extinction of a Cocaine-Context Association
Lee, J., Finkelstein, J., Choi, J. Y., & Witten, I. B. (2016) · Neuron · doi:10.1016/j.neuron.2016.05.001 · Cited by 59
“, 2001), and their activity modulates the activity of themedium spiny neurons (MSNs), the output neurons in the striatum (English et al., 2012; Oldenburg and Ding, 2011; Witten et al., 2010; Nelson et al., 2014; Higley et al., 2011).”
Background
Optogenetic interrogations of the neural circuits underlying addiction
Britt, J. P., & Bonci, A. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.01.010 · Cited by 64
Chronic alcohol drinking persistently suppresses thalamostriatal excitation of cholinergic neurons to impair cognitive flexibility
Ma, T., Huang, Z., Xie, X., Cheng, Y., Zhuang, X., Childs, M., Gangal, H., Wang, X., Smith, L., Smith, R., et al. (2021) · Journal of Clinical Investigation · doi:10.1172/jci154969 · Cited by 53
Paradoxical network excitation by glutamate release from VGluT3+ GABAergic interneurons
Pelkey, K. A., Calvigioni, D., Fang, C., Vargish, G., Ekins, T., Auville, K., Wester, J. C., Lai, M., Mackenzie-Gray Scott, C., Yuan, X., et al. (2020) · eLife · doi:10.7554/elife.51996 · Cited by 46
“In many of these systems, VGluT3 imparts unique synaptic properties such as glutamate corelease and vesicular synergy (Amilhon et al., 2010; Gras et al., 2008; Higley et al., 2011; Nelson et al., 2014; Noh et al., 2010; Sakae et al., 2015; Varga et al., 2009; Wang et al., 2019).”
Background
Recurrent Implication of Striatal Cholinergic Interneurons in a Range of Neurodevelopmental, Neurodegenerative, and Neuropsychiatric Disorders
Poppi, L. A., Ho-Nguyen, K.-T., Shi, A., Daut, C. T., & Tischfield, M. A. (2021) · Cells · doi:10.3390/cells10040907 · Cited by 47
“To add to the complexity, ChINs can also co-release GABA [141] and glutamate [68,142], in addition to ACh.”
Background
In vivo optogenetic control of striatal and thalamic neurons in non-human primates
Galvan, A., Hu, X., Smith, Y., & Wichmann, T. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050808 · Cited by 45
“The value of using the far more specific optogenetic techniques to study the physiology of the basal ganglia is well established in rodent studies [12,13,14,15,16,17].”
Background
Acetylcholine Muscarinic M4 Receptors as a Therapeutic Target for Alcohol Use Disorder: Converging Evidence From Humans and Rodents
Walker, L. C., Berizzi, A. E., Chen, N. A., Rueda, P., Perreau, V. M., Huckstep, K., Srisontiyakul, J., Govitrapong, P., Jia, X., Lindsley, C. W., et al. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.02.019 · Cited by 45
Stereological Estimates of Glutamatergic, GABAergic, and Cholinergic Neurons in the Pedunculopontine and Laterodorsal Tegmental Nuclei in the Rat
Luquin, E., Huerta, I., Aymerich, M. S., & Mengual, E. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00034 · Cited by 46
Alcohol intake enhances glutamatergic transmission from D2 receptor-expressing afferents onto D1 receptor-expressing medium spiny neurons in the dorsomedial striatum
Lu, J., Cheng, Y., Wang, X., Woodson, K., Kemper, W. C., Disney, E., & Wang, J. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0332-9 · Cited by 42
Relationships and Interactions between Ionotropic Glutamate Receptors and Nicotinic Receptors in the CNS
Stone, T. W. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.06.007 · Cited by 49
Different correlation patterns of cholinergic and GABAergic interneurons with striatal projection neurons
Adler, A., Katabi, S., Finkes, I., Prut, Y., & Bergman, H. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2013.00047 · Cited by 41
“Thus, they can modulate (in conjunction with the dopaminergic and other modulators of the striatum) the efficacy of the cortico and thalamo-striatal synapses, rather than directly affecting their target neurons’ ongoing discharge (Kreitzer, 2009; Higley et al., 2011).”
Background
VGluT3-Expressing CCK-Positive Basket Cells Construct Invaginating Synapses Enriched with Endocannabinoid Signaling Proteins in Particular Cortical and Cortex-Like Amygdaloid Regions of Mouse Brains
Omiya, Y., Uchigashima, M., Konno, K., Yamasaki, M., Miyazaki, T., Yoshida, T., Kusumi, I., & Watanabe, M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4681-14.2015 · Cited by 42
“Both CCK and CCK2R are densely expressed in the BLA (Larsson and Rehfeld, 1979; Vanderhaeghen et al., 1985; Honda et al., 1993; Mascagni and McDonald, 2003), and rich CCK2R mRNA expression in BA pyramidal cells was shown in the present study.”
Background
Benzophenone-3 Passes Through the Blood-Brain Barrier, Increases the Level of Extracellular Glutamate, and Induces Apoptotic Processes in the Hippocampus and Frontal Cortex of Rats
Pomierny, B., Krzyżanowska, W., Broniowska, Ż., Strach, B., Bystrowska, B., Starek‐Świechowicz, B., Maciejska, A., Skórkowska, A., Wesołowska, J., Walczak, M., et al. (2019) · Toxicological Sciences · doi:10.1093/toxsci/kfz160 · Cited by 42
M 1 muscarinic activation induces long-lasting increase in intrinsic excitability of striatal projection neurons
Lv, X., Dickerson, J. W., Rook, J. M., Lindsley, C. W., Conn, P. J., & Xiang, Z. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.03.017 · Cited by 40
“A previous study indicated that striatal cholinergic interneurons could co-release glutamate, which activates NMDA and AMPA/ kainate glutamate receptors in MSNs (Higley et al., 2011).”
Influential
Co-release of glutamate and GABA from single vesicles in GABAergic neurons exogenously expressing VGLUT3
Zimmermann, J., Herman, M. A., & Rosenmund, C. (2015) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2015.00016 · Cited by 37
Continuous cholinergic-dopaminergic updating in the nucleus accumbens underlies approaches to reward-predicting cues
Skirzewski, M., Princz‐Lebel, O., German‐Castelan, L., Crooks, A. M., Kim, K., Tarnow, S. H., Reichelt, A. C., Memar, S., Palmer, D. D., Li, Y., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-35601-x · Cited by 41
“Please, improve statistics/analysis section including these and other relevant details for better understanding of the data analysis.”
Cholinergic/glutamatergic co‐transmission in striatal cholinergic interneurons: new mechanisms regulating striatal computation
Kljakic, O., Janíčková, H., Prado, V. F., & Prado, M. A. M. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14003 · Cited by 39
Striatal Cholinergic Interneurons Modulate Spike-Timing in Striosomes and Matrix by an Amphetamine-Sensitive Mechanism
Crittenden, J. R., Lacey, C. J., Weng, F., Garrison, C. E., Gibson, D. J., Lin, Y., & Graybiel, A. M. (2017) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00020 · Cited by 42
“Analyses of SPN responses to ChI stimulation have shown that there are multiple inhibitory post-synaptic currents with fast, slow and very slow time-courses (English et al., 2012), and small excitatory post-synaptic currents (Higley et al., 2011).”
Background
Nucleus accumbens in the pathogenesis of major depressive disorder: A brief review
Yajie, J., Zou, M., Wang, Y., & Wang, Y. (2023) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2023.03.004 · Cited by 41
“At the circuit level, activation of TANs has been shown to elicit both fast glutamatergic transmission (Higley et al., 2011) and GABAergic inhibition of MSNs, the latter coincident with synchronous cholinergic activation and sufficient to pause MSNs firing (English et al.”
A distinct set of synaptic‐like microvesicles in atroglial cells contain VGLUT3
Ormel, L., Stensrud, M. J., Chaudhry, F. A., & Gundersen, V. (2012) · Glia · doi:10.1002/glia.22348 · Cited by 38
“Indeed, it has recently been reported that glutamate is released from cholinergic neurons to give fast glutamatergic postsynaptic responses (Higley et al., 2011; Ren et al., 2011).”
Background
Vesicular glutamate transporter‐3 in the rodent brain: Vesicular colocalization with vesicular γ‐aminobutyric acid transporter
Stensrud, M. J., Chaudhry, F. A., Leergaard, T. B., Bjaalie, J. G., & Gundersen, V. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23331 · Cited by 35
“Recently, VGLUT3dependent glutamate receptor responses were detected in the striatum (Higley et al., 2011), indicative of glutamate release from cholinergic neurons.”
Background
Descending projections from the basal forebrain to the orexin neurons in mice
Agostinelli, L. J., Ferrari, L. L., Mahoney, C. E., Mochizuki, T., Lowell, B. B., Arrigoni, E., & Scammell, T. E. (2016) · The Journal of Comparative Neurology · doi:10.1002/cne.24158 · Cited by 38
“The ChAT-Cre mice have been validated in prior studies (Higley et al., 2011; Rossi et al., 2011).”
BackgroundMethod
Dopaminergic modulation of basal ganglia output through coupled excitation–inhibition
Budzillo, A., Duffy, A., Miller, K. E., Fairhall, A. L., & Perkel, D. J. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1611146114 · Cited by 35
“It is not the cholinergic neuron type, which also releases glutamate in mammals (40, 46), but may nonetheless have similar function.”
Background
Segregation of glutamatergic and cholinergic transmission at the mixed motoneuron Renshaw cell synapse
d’Incamps, B. L., Bhumbra, G. S., Foster, J. D., Beato, M., & Ascher, P. (2017) · Scientific Reports · doi:10.1038/s41598-017-04266-8 · Cited by 38
Effect of VGLUT inhibitors on glutamatergic synaptic transmission in the rodent hippocampus and prefrontal cortex
Neale, S. A., Copeland, C. S., & Salt, T. E. (2013) · Neurochemistry International · doi:10.1016/j.neuint.2013.10.001 · Cited by 35
Dual recombinase fate mapping reveals a transient cholinergic phenotype in multiple populations of developing glutamatergic neurons
Nasirova, N., Quina, L. A., Agosto‐Marlin, I. M., Ramirez, J., Lambe, E. K., & Turner, E. E. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24753 · Cited by 33
“…cholinergic neurons can exhibit glutamatergic transmission dependent on the glutamate transporter VGluT3 (Boulland et al., 2004; Gras et al., 2002; Higley et al., 2011), which is atypical in that it is gener- ally coexpressed in neurons with other neurotransmitters (El…”
Background
Persistent Alterations of Accumbal Cholinergic Interneurons and Cognitive Dysfunction after Adolescent Intermittent Ethanol Exposure
Galaj, E., Kipp, B. T., Floresco, S., & Savage, L. M. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.01.062 · Cited by 37
“Cholinergic interneurons in the NAc control local circuits (Cachope et al. 2012; Higley et al. 2011; Threlfell et al. 2012), modulate the activity of GABAergic projection neurons (Witten et al.”
Background
Multiplexed neurotransmission emulated for emotion control
Ni, Y., Ma, M., Wei, H., Gong, J., Han, H., Liu, L., Xu, Z., & Xu, W. (2021) · Nano Energy · doi:10.1016/j.nanoen.2021.106038 · Cited by 34
A Feud that Wasn't: Acetylcholine Evokes Dopamine Release in the Striatum
Surmeier, D. J., & Graybiel, A. M. (2012) · Neuron · doi:10.1016/j.neuron.2012.06.028 · Cited by 32
“They linked this to the recently described corelease of glutamate and AChbyChIs (Higley et al., 2011).”
Background
Role of the atypical vesicular glutamate transporter VGLUT3 in l-DOPA-induced dyskinesia
Gangarossa, G., Guzmán, M. S., Prado, V. F., Prado, M. A. M., Daumas, S., Mestikawy, S. E., & Valjent, E. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.12.010 · Cited by 35
High‐frequency electrical stimulation suppresses cholinergic accumbens interneurons in acute rat brain slices through GABA B receptors
Xie, Y., Heida, T., Stegenga, J., Zhao, Y., Moser, A., Tronnier, V. M., Feuerstein, T. J., & Hofmann, U. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12736 · Cited by 30
“DBS is currently proposed as an effective surgical intervention for various dysfunctional syndromes, such as epilepsy, depression and obsessive-compulsive disorder (OCD) (Tronnier & Fogel, 2000; Gross, 2004; Huff et al., 2010).”
Background
Protonic conductor: better understanding neural resting and action potential
Lee, J. W. (2020) · Journal of Neurophysiology · doi:10.1152/jn.00281.2020 · Cited by 28
Pyramidal tract neurons drive amplification of excitatory inputs to striatum through cholinergic interneurons
Morgenstern, N. A., Isidro, A. F., Israely, I., & Costa, R. M. (2022) · Science Advances · doi:10.1126/sciadv.abh4315 · Cited by 30
“However, in the DLS, ChIs corelease glutamate together with acetylcholine ( 63 ).”
Cholinergic activity reflects reward expectations and predicts behavioral responses
Hegedüs, P., Sviatkó, K., Király, B., Martínez‐Bellver, S., & Hangya, B. (2022) · iScience · doi:10.1016/j.isci.2022.105814 · Cited by 28
Cholinergic modulation of striatal nitric oxide‐producing interneurons
Melendez-Zaidi, A. E., Lakshminarasimhah, H., & Surmeier, D. J. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14528 · Cited by 25
“It is also worth noting that strong optogenetic stimulation of ChIs did evoke an excitatory response in some LTSIs (Figure 5d; Higley et al., 2011).”
Background
Synapse-specific expression of mu opioid receptor long-term depression in the dorsomedial striatum
Muñoz, B., Haggerty, D. L., & Atwood, B. K. (2020) · Scientific Reports · doi:10.1038/s41598-020-64203-0 · Cited by 27
Elevated antibody binding to striatal cholinergic interneurons in patients with pediatric acute-onset neuropsychiatric syndrome
Xu, J., Frankovich, J., Liu, R.-J., Thienemann, M., Silverman, M. A., Farhadian, B., Willett, T. A., Manko, C., Columbo, L. A., Leibold, C. M., et al. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.07.044 · Cited by 28

Authors: Higley, M. J., Gittis, A. H., Oldenburg, I. A., Balthasar, N., Seal, R. P., Edwards, R. H., Lowell, B. B., Kreitzer, A. C., & Sabatini, B. L.
Affiliations: Howard Hughes Medical Institute (US)
University of California, San Francisco (US)
Beth Israel Deaconess Medical Center (US)
Corresponding author: Sabatini, Bernardo L.
ORCID: Higley, Michael J.
Gittis, Aryn H.
Oldenburg, Ian A.
Seal, Rebecca P.
Edwards, Robert H.
Lowell, Bradford B.
Kreitzer, Anatol C.
Sabatini, Bernardo L.
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2011-04-22
Volume: 6
Issue: 4
Pages: e19155
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0019155
PMC: PMC3081336
OpenAlex: W2137833675
Cited by: 175
References: 35
Citations by year: 2026: 4 · 2025: 6 · 2024: 8 · 2023: 10 · 2022: 14 · 2021: 11 · 2020: 14 · 2019: 10 · 2018: 12 · 2017: 16 · 2016: 14 · 2015: 16 · 2014: 12 · 2013: 10 · 2012: 13
FWCI: 5.30
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Explore Bristol Research (publishedVersion)
Figshare (submittedVersion, cc-by)
Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
KiltHub Repository (submittedVersion, other-oa)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
eScholarship (California Digital Library) (submittedVersion)
eScholarship (California Digital Library) (submittedVersion, cc-by)
Bristol Research (University of Bristol) (submittedVersion)
KiltHub Repository (cc-by)
Funders: Howard Hughes Medical Institute
W. M. Keck Foundation
Parkinson's Disease Foundation
National Alliance for Research on Schizophrenia and Depression
National Institutes of Health (DK057521, DK046200, DA10154, NS046579)
National Institute of Mental Health (F32MH068085, MH50712, R01MH050712, R37MH050712, F31MH093026)
National Institute on Drug Abuse (P01DA010154, DA-10154)
National Institute of Diabetes and Digestive and Kidney Diseases (P30DK057521, R01DK075632, P30DK046200, DK075632)
National Institute of Neurological Disorders and Stroke (NS064984, R01NS046579, F32NS063663, R01NS064984, R37NS046579, NS063663, NS046579)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Health Sciences › Medicine › Clinical Neurology › Deep Brain Stimulation and Movement Disorders
Keywords: cholinergic interneurons, striatum, VGLUT3, glutamatergic neurotransmission, medium spiny neurons, NMDA receptor, choline acetyltransferase, channelrhodopsin-2, optogenetic stimulation
MeSH terms: Channelrhodopsins, Central Nervous System Stimulants, Animals, Corpus Striatum, Evoked Potentials, Female, Interneurons, Male, Mecamylamine, Picrotoxin, Receptors, Cholinergic, Scopolamine, Receptors, N-Methyl-D-Aspartate, Amino Acid Transport Systems, Acidic, Mice

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Cholinergic Interneurons Mediate Fast VGluT3-Dependent Glutamatergic Transmission in the Striatum

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