Synaptic and circuit functions of multitransmitter neurons in the mammalian brain
Open accessAbstract
Neurons in the mammalian brain are not limited to releasing a single neurotransmitter but often release multiple neurotransmitters onto postsynaptic cells. Here, we review recent findings of multitransmitter neurons found throughout the mammalian central nervous system. We highlight recent technological innovations that have made the identification of new multitransmitter neurons and the study of their synaptic properties possible. We also focus on mechanisms and molecular constituents required for neurotransmitter corelease at the axon terminal and synaptic vesicle, as well as some possible functions of multitransmitter neurons in diverse brain circuits. We expect that these approaches will lead to new insights into the mechanism and function of multitransmitter neurons, their role in circuits, and their contribution to normal and pathological brain function.
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Written from the paper’s full text.
TL;DR
This review synthesizes evidence that many mammalian central nervous system neurons release multiple small-molecule neurotransmitters, with mechanisms ranging from co-packaging in the same synaptic vesicle to independent vesicle pools and release sites. It argues that identifying these multitransmitter neurons and their release mechanisms is necessary to understand circuit function, plasticity, and behavior.
Key findings
- A screen for GABA/glutamate coreleasing neurons found 30 different brain regions with neurons expressing genes required for vesicular packaging of both GABA (vGAT; *Slc32a1*) and glutamate (vGluT2/3; *Slc17a6/Slc17a8*), though cotransmission was physiologically confirmed in only some regions, notably SuM, VTA, and EP.
- Mechanisms differ by transmitter pair: EP Sst GABA/glutamate synapses showed optical quantal responses consistent only with co-packaging into the same vesicle; VTA→LHb terminals had >60% of axon terminals positive for both vGAT and vGluT2, but vesicles were largely vGluT2- or vGAT-positive and rarely copositive. ACh/glutamate can be co-packaged with transporter synergy, GABA/glycine compete for vGAT, and DA/GABA release from dopamine neurons requires vMAT2 rather than vGAT.
- Cotransmission can produce frequency-dependent and target-specific signaling: mHb→IPN synapses release glutamate reliably with single stimuli, while nicotinic ACh responses require prolonged stimulation (50 Hz, 5 s; or 20–50 Hz), and cortical VIP/ChAT+ neurons use ACh or GABA depending on postsynaptic target.
- The review proposes circuit functions including multiple timescales of postsynaptic control (DA effects delayed by ~500 ms versus GABA/glutamate currents at 2–4 ms), frequency-dependent volume transmission, and signed/graded synapses for value learning in LHb.
Methods
- Review article, not a primary experimental study; it synthesizes recent findings on activity-dependent small-molecule cotransmission in the mammalian CNS and excludes developmental neurotransmitter switching and corelease in other model organisms.
- Evidence is drawn from cited genetic, single-cell sequencing, in situ hybridization, EM/immunogold, immunoprecipitation, optogenetic, electrophysiological, optical quantal, and behavioral studies across regions including SuM, VTA, EP/GPi, spinal cord, auditory brainstem, cerebellum, striatum, basal forebrain, mHb, raphe, retina, and cortex.
- Main analysis is narrative synthesis and model-building, with tables of neurotransmitters and vesicular transporters and figures illustrating co-packaging, independent release, and hypothesized circuit functions.
Limitations
- Stated: most single-cell sequencing analyses are performed on populations, so individual neurons must be confirmed to express all genes needed for release of more than one neurotransmitter; off-target Cre expression in mouse lines can lead to misinterpretation, and in situ transcriptional plus electrophysiological confirmation is critical.
- Stated: classical minimal stimulation is confounded when axons from many presynaptic neuron types overlap; optogenetic targeting helps but requires careful spatiotemporal calibration to stimulate individual axons/synapses.
- Stated and evident: many mechanistic questions remain unresolved, including how transporters are trafficked to separate vesicle pools, how multitransmitter properties are maintained through the vesicle cycle, how postsynaptic receptors are organized at GABA/glutamate synapses, and the identity of the hypothetical error signal for LHb value learning; as a review, it reports no new primary data.
Model-written summary. Check it against the paper before relying on it.
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Claims the paper makes
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- Interpretationnone given
Mammalian neurons often release more than one neurotransmitter onto postsynaptic cells, rather than only a single transmitter.
“Neurons in the mammalian brain are not limited to releasing a single neurotransmitter but often release multiple neurotransmitters onto postsynaptic cells.”
Quote in the paperSubstantial claim - Premisecitation
New studies show that many neuronal subtypes in the brain have the molecular machinery needed to release more than one neurotransmitter.
“exciting new studies exemplify the diverse array of neuronal subtypes in the brain that have the molecular machinery necessary to release more than one neurotransmitter.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [5][6][7][8][9]
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- Premisecitation
In multitransmitter neurons, differential sensitivity of vesicular transporters to intravesicular pH or membrane potential is important for co-packaging.
“In multitransmitter neurons, where vesicular packaging of more than one neurotransmitter occurs, it is important to consider how vesicular transporters are differentially sensitive to intravesicular factors such as pH or membrane potential.16”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [16] source
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- Study design and conductreasoning
Concluding that a neuron can corelease requires confirmation that both neurotransmitter accumulation and vesicular packaging occur.
“Therefore, concluding that a neuron can only release one or more neurotransmitters (i.e., that it can corelease), requires confirmation that both steps occur.”
Quote in the paperSubstantial claim- Rests on an assumption: Vesicular release of a neurotransmitter requires presynaptic accumulation of the signaling molecule to a concentration sufficient for packaging into a vesicle and release.
- Premisereasoning
Each component of accumulation and packaging can be independently modulated to restrict or enhance release of a transmitter.
“Each of these components can also be independently modulated or modified to restrict or enhance release of a transmitter, underscoring their importance to neurotransmission.”
Quote in the paperSubstantial claim
- Premisecitation
Optical quantal analysis found that unitary responses from EP release sites are consistent only with co-packaging of GABA and glutamate into the same synaptic vesicle.
“Optical quantal analysis determined that the statistical properties of unitary responses resulting from activation of cotransmitting EP release sites were consistent only with copackaging of GABA and glutamate into the same synaptic vesicle 25 (Figure 2).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [25] source
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- Premisecitation
Immunogold EM and immunoprecipitation of LHb synaptic vesicles found vesicles largely vGluT2 or vGAT positive, rarely copositive, suggesting GABA and glutamate are typically packaged into separate vesicles in LHb.
“Finally, immunogold EM and immunoprecipitation of synaptic vesicles from LHb found that vesicles were largely vGluT2 or vGAT positive, but rarely copositive, suggesting that GABA and glutamate are typically packaged into separate vesicles in the LHb.33”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [33] source
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- Premisecitation
Synaptic vesicles are acidified by V-ATPases that pump protons into the vesicle lumen.
“Synaptic vesicles are acidified by vacuolar H+-dependent adenosine triphosphatases (V-ATPases) that pump protons into the vesicle lumen.17”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [17] source
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- Premisenone given
vGAT transports neutral zwitterions.
“In contrast, the vesicular GABA/glycine transporter (vGAT) transports neutral zwitterions.”
Quote in the paperSubstantial claim - Study design and conductnone given
Cotransmission by most recently identified GABA/glutamate cell types has not yet been physiologically confirmed.
“However, cotransmission by most of these recently identified cell types has yet to be physiologically confirmed”
Quote in the paperSubstantial claim - Interpretationcitation
The postsynaptic LHb neuron may determine whether VTA input is primarily excitatory or inhibitory, likely through differential insertion of ionotropic GABA and glutamate receptors.
“suggesting that the postsynaptic LHb neuron, presumably by differential insertion of ionotropic GABA and glutamate receptors, may determine whether the input is primarily excitatory or inhibitory.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [32] source
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- Interpretationreasoning
vGAT on synaptic vesicles may have little impact on other transporters on the same vesicle because it depends on both gradients and minimally affects either.
“Therefore, the presence of vGAT on synaptic vesicles may have little impact on the activity of other transporters on the same vesicle, with little effect on their function due to its codependence on DpH and DJ and its minimal effect on either gradient.”
Quote in the paperSubstantial claim0 of 2 sources checked - Premisecitation
GABA/glycine cotransmission has been observed in the auditory brainstem and cerebellum.
“GABA/glycine cotransmission has since been observed in other areas, including the auditory brainstem and cerebellum.[45][46][47]”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [45][46][47]
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- Interpretationreasoning
Complementary dependencies may explain observed synergies between vGluT and VAChT or vGluT and ZnT3 on the same synaptic vesicle.
“These complementary dependencies may explain the observed synergies between vGluT and VAChT or vGluT and the vesicular zinc transporter (ZnT3) when these are localized to the same synaptic vesicle.5,21,22”
Quote in the paperSubstantial claim0 of 3 sources checked - Premisecitation
Optogenetic activation of SuM terminals in dentate gyrus produces monosynaptic short-latency release of both GABA and glutamate onto granule cells and interneurons.
“Furthermore, optogenetic activation of SuM terminals in the DG produces monosynaptic, short-latency release of both GABA and glutamate onto postsynaptic granule cells and interneurons.29”
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- Premisecitation
The resulting pH gradient and vesicle membrane potential can power neurotransmitter uptake by vesicular transporters.
“This creates a pH gradient (DpH) and a vesicular membrane potential (DJ), both of which can power the uptake of neurotransmitters by vesicular transporters (Table 1).16”
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- Premisecitation
In vivo optogenetic excitation of VTA input to LHb causes excitation, inhibition, or both in extracellularly recorded LHb neurons.
“In vivo optogenetic excitation of VTA input to the LHb (using either Slc17a6-IRES-Cre or Slc32a1-IRES-Cre mice) results in either excitation, inhibition, or both of extracellularly recorded LHb neurons”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [32] source
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- Premisecitation
LHb-projecting EP neurons have single axon terminals that make both symmetric and asymmetric synapses, as determined by EM.
“Similar to LHb-projecting VTA neurons, LHb-projecting EP neurons have single axon terminals that make both symmetric (GABAergic) and asymmetric (glutamatergic) synapses, as determined by EM. 33”
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- Premisecitation
A screen found that 30 brain regions contain neurons expressing genes required for vesicular packaging of both GABA and glutamate.
“a screen for GABA/glutamate coreleasing neurons revealed that 30 different brain regions have neurons that express the genes required for synaptic vesicle packaging of both GABA (vGAT; Slc32a1) and glutamate (vGluT2/3; Slc17a6/Slc17a8).8”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [8] source
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- Premisecitation
These VTA neurons are distributed mostly in medial subregions including the interfascicular, paranigral, and rostral linear raphe nuclei.
“These neurons are distributed mostly in the medial subregions of the VTA, including the interfascicular nucleus, paranigral nucleus, and rostral linear nucleus of the raphe.33”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [33] source
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- Premisecitation
Studies from the 1990s demonstrated cotransmission of GABA and glycine from inhibitory interneurons in the spinal cord.
“Studies from the 1990s demonstrated cotransmission of GABA and glycine from inhibitory interneurons in the spinal cord.44”
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- Premisecitation
A VTA neuronal subtype coexpresses genes for the vesicular GABA transporter and vesicular glutamate transporter 2.
“One of the VTA neuronal subtypes is distinguished by coexpression of the genes encoding the vesicular transporters for GABA (Slc32a1) and glutamate (Slc17a6).32”
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- Premisereasoning
vGluT1/2/3 transport glutamate primarily depending on membrane potential.
“Conversely, the transport of glutamate by vGluT1/2/3 depends primarily on DJ.”
Quote in the paperSubstantial claim - Interpretationcitation
Even though VTA axons express both vGluT2 and vGAT, synaptic vesicles and transporters are largely segregated into distinct pools for release rather than released together at the same synapse.
“Together, these studies suggest that even though individual axons from the VTA express both vGluT2 and vGAT, synaptic vesicles and vesicular transporters are largely segregated into distinct pools for release, rather than released together at the same synapse.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [33] source
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- Premisecitation
EM studies of dentate gyrus axon terminals found anatomical evidence for GABAergic and glutamatergic vesicular transporters in the same axon.
“Electron microscopy (EM) studies of axon terminals in the dentate gyrus (DG) have demonstrated anatomical evidence for the existence of GABAergic and glutamatergic vesicular transporters in the same axon.27”
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- Premisecitation
Chemogenetic manipulation of SuM-to-dentate gyrus projections indicates this circuit regulates arousal.
“Studies using chemogenetic manipulation of projections from the SuM to DG reveal that this circuit is involved in the regulation of arousal. 30”
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- Premisecitation
These studies were among the first to describe co-packaging, in which two neurotransmitters are loaded into individual synaptic vesicles.
“These studies were some of the first to describe the ''co-packaging'' phenomenon, where two different neurotransmitters are loaded into individual synaptic vesicles.”
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- Interpretationcitation
GABA/glutamate cotransmission may be more widespread than previously thought.
“These findings indicated that GABA/glutamate cotransmission may be more widespread than previously thought.”
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- Premisecitation
A subset of serotonergic neurons in the dorsal and median raphe nuclei express vGluT3.
“To add to this complexity, it is now clear that a subset of serotonergic neurons in the dorsal and median raphe nuclei express vGluT3 (Slc17a8).[75][76][77]”
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- Interpretationcitation
Ach and GABA are segregated into different synaptic vesicles and/or axonal boutons to endow single SACs with spatial selectivity over cotransmission.
“These studies suggest that Ach and GABA are segregated into different synaptic vesicles and/or axonal boutons to endow single SACs with spatial selectivity over cotransmission of neurotransmitters.”
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- Premisecitation
Paired recordings from neighboring retinal neurons demonstrated monosynaptic transmission of both Ach and GABA from SACs to direction-sensitive retinal ganglion cells.
“More recently, an elegant study employing paired recordings from neighboring retinal neurons demonstrated monosynaptic transmission of both Ach and GABA from SACs to direction-sensitive retinal ganglion cells (DSGCs).86”
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- Premisecitation
Array tomography of cortical axons from pallidal Ach/GABA neurons revealed physically separate sites of vGAT and vAChT labeling, suggesting distinct vesicular pools.
“Additional array tomography studies of cortical axons projecting from pallidal Ach/GABA neurons revealed physically separate sites of vGAT and vAChT labeling, suggesting distinct vesicular pools for the two neurotransmitters.90”
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- Premisecitation
Functional and immunohistochemical studies identified starburst amacrine cells as the sole source of Ach in the retina.
“Functional and immunohistochemical studies identified starburst amacrine cells (SACs) as the sole source of Ach in the retina.82,83”
Quote in the paperSubstantial claim0 of 2 sources checked - Premisecitation
GABA and glycine compete for packaging into synaptic vesicles because both are transported by vGAT.
“Notably, GABA and glycine compete for packaging into synaptic vesicles as both are transported by the same vesicular transporter vGAT 50 (Figure 1A).”
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- Interpretationnone given
Evidence from retina, basal forebrain/globus pallidus, and cortex points to distinct pools of synaptic vesicles containing either Ach or GABA, which may be released at separate sites.
“Here, we review Ach/GABA-releasing neurons from the retina, basal forebrain/globus pallidus, and cortex, where evidence points to distinct pools of synaptic vesicles containing either Ach or GABA, which may be released at separate sites.”
Quote in the paperNot a substantial claim - Premisecitation
Packaging GABA and/or glycine into vesicles largely depends on their intracellular intraaxonal concentrations, controlled by GAD1/2 synthesis or GlyT1/2 transporters.
“Therefore, packaging GABA and/or glycine into vesicles is largely dependent on their intracellular (intraaxonal) concentration, which are controlled by either intracellular synthesis (glutamate decarboxylase [GAD] 1/2) or plasma membrane transporters (GlyT1/2), respectively.51”
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- Premisecitation
Immunogold EM and immunoprecipitation suggest that vGluT and VAChT co-package glutamate and ACh into the same synaptic vesicle in mHb-IPN and striatal cholinergic-to-SPN synapses.
“Immunogold EM and immunoprecipitation experiments suggest that vGluT and VAChT co-package glutamate and ACh into the same synaptic vesicle in both mHb to IPN synapses and striatal cholinergic to medium spiny neuron synapses 21,22,56 (Figure 1A).”
Quote in the paperSubstantial claim0 of 3 sources checked - Premisecitation
Striatal cholinergic interneurons cotransmit Ach and glutamate locally onto spiny projection neurons and dopaminergic axonal terminals.
“Striatal cholinergic interneurons (CINs) cotransmit Ach and glutamate locally onto spiny projection neurons (SPNs) 60 and dopaminergic axonal terminals.[61][62][63]”
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- Interpretationreasoning
Vesicular transporter synergism/antagonism is important for neurons that co-package two neurotransmitters into synaptic vesicles.
“Together, these examples illustrate the importance of vesicular transporter synergism/antagonism for neurons that copackage two neurotransmitters into synaptic vesicles.”
Quote in the paperSubstantial claim - Interpretationreasoning
GABA/glycine cotransmission allows two transmitters to hyperpolarize postsynaptic cells with different kinetics, giving the presynaptic neuron tight control over postsynaptic firing rates.
“Together, these studies frame an interesting role for cotransmission, where two transmitters provide hyperpolarization of the postsynaptic cell with different kinetics, allowing the presynaptic neuron tight control over postsynaptic firing rates.”
Quote in the paperSubstantial claim - Premisecitation
Median raphe 5-HT/vGluT3+ neurons activate CA1 inhibitory interneurons to disynaptically inhibit CA1 pyramidal neurons.
“Compounding the diverse and extensive functions of 5-HT neurons, median raphe 5-HT/vGluT3+ neurons also activate CA1 inhibitory interneurons to disynaptically inhibit CA1 pyramidal neurons.81”
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- Premisecitation
Medial habenula axon terminals to the interpeduncular nucleus contain both vGluT1/2 and VAChT and cotransmit glutamate and Ach onto individual IPN neurons.
“Axon terminals from mHb to the interpeduncular nucleus (IPN) contain both vGluT1/2 and VAChT and cotransmit both glutamate and Ach onto individual neurons in the IPN.56”
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- Premisecitation
Optogenetic activation of cortically projecting Ach/GABA-releasing neurons evoked monosynaptic GABA-mediated inhibitory currents and Ach-mediated nicotinic excitatory currents in layer 1 interneurons.
“Optogenetic activation of cortically projecting Ach/GABA-releasing neurons evoked monosynaptic GABAmediated inhibitory currents and Ach-mediated nicotinic excitatory currents in layer 1 interneurons.”
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- Interpretationreasoning
Assumptions that postsynaptic receptors saturate after single vesicle fusion may not hold at synapses with high competition for vesicular transport.
“Therefore, assumptions regarding saturation of postsynaptic receptors following single vesicle fusion may not hold at these or other synapses, where competition for vesicular transport is high.”
Quote in the paperSubstantial claim - Premisecitation
Many cholinergic neurons also contain vGluT1/2/3 coexpressed with Ach synthesis, packaging, and release machinery in the striatum, basal forebrain, and medial habenula.
“However, many of these neurons also contain the vesicular glutamate transporters (vGluT1/2/3) that are coexpressed with molecular machinery for Ach synthesis, vesicular packaging, and release in multiple brain regions, including the striatum, basal forebrain, and medial habenula (mHb).22,56,57”
Quote in the paperSubstantial claim0 of 3 sources checked - Interpretationreasoning
These findings contrast with GABA/glycine co-packaging, which shows an antagonistic relationship.
“These findings lie in contrast to those described above for neurons that co-package GABA and glycine, which show an antagonistic relationship with regard to co-packaging.”
Quote in the paperNot a substantial claim - Premisecitation
Synergism has been reported between vGluT3 and vMAT2, by which vGluT3 promotes vesicular loading of 5-HT via vMAT2.
“In support of co-packaging, synergism has been reported between vGluT3 and vMAT2, by which vGluT3 promotes vesicular loading of 5-HT via vMAT2.80”
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- Premisecitation
Ach is the primary transmitter when the postsynaptic neuron is a layer 1 interneuron or another VIP/Chat+ neuron and the receptors are nAchRs.
“Ach is the primary transmitter when the postsynaptic neuron is a layer 1 interneuron or another VIP/Chat+ neuron and the postsynaptic receptors are nAchRs.”
Quote in the paperSubstantial claim0 of 2 sources checked - Premisecitation
vGluT3+ retinal amacrine cells release both glycine and glutamate onto separate populations of retinal ganglion cells.
“a class of vGluT3+ retinal amacrine cells was recently found to release both the inhibitory neurotransmitter glycine and excitatory neurotransmitter glutamate onto distinct populations of retinal ganglion cells (RGCs).99,100”
Quote in the paperSubstantial claim0 of 2 sources checked - Premisecitation
Reducing GABA cotransmission from DANs by genetic deletion of Aldh1a1 increases ethanol intake and preference in mice.
“reducing GABA cotransmission from DANs by genetic deletion of Aldh1a1 increases ethanol intake and preference in mice”
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- Premisecitation
Ach/glutamate release from the mHb to the IPN has frequency-dependent effects on postsynaptic cells.
“Investigations into Ach/glutamate release from the mHb to the IPN revealed frequency-dependent effects of cotransmission on postsynaptic cells.”
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- Premisecitation
Transcriptomically similar VIP/ChAT+ subpopulations have been identified by large-scale single-cell sequencing of motor and visual cortex in mouse, marmosets, and humans.
“Transcriptomically similar neuronal subpopulations (VIP/ChAT+) have also been identified with largescale single-cell sequencing of the motor and visual cortex in mouse, marmosets, and humans.6,[94][95][96]”
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Glutamatergic synapses from vGluT3+ amacrine cells target OFF alpha ganglion cells and other retinal cell types but avoid suppressed-by-contrast RGCs.
“Glutamatergic synapses from vGluT3+ retinal amacrine cells are more promiscuous and target OFF alpha ganglion cells and other retinal cell types but avoid suppressed by contrast RGCs.99”
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- Premisecitation
Selective deletion of Slc17a6 from DA neurons in vivo abolishes glutamate release.
“selective deletion of Slc17a6 from DA neurons in vivo abolished glutamate release”
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Dopamine neurons projecting to ventral and dorsal striatum that express vGluT2 release glutamate onto striatal SPNs and CINs.
“dopamine neurons in the ventral midbrain projecting to ventral and dorsal striatum expressing the vGluT2 were confirmed, using optogenetic stimulation in brain slices, to release glutamate onto striatal SPNs and CINs.[108][109][110]”
Quote in the paperSubstantial claim0 of 3 sources checked - Premisecitation
Ach and glutamate are copackaged into the same synaptic vesicles at the mHb-to-IPN synapse.
“Several groups have found evidence for Ach and glutamate being copackaged into the same synaptic vesicles at this synapse 21,22,56,124”
Quote in the paperSubstantial claim0 of 4 sources checked - Interpretationreasoning
Much like cholinergic neurons in the basal forebrain and globus pallidus, VIP/ChAT+ neurons appear to have distinct vesicle populations for Ach and GABA release.
“This suggests, much like the cholinergic neurons in the basal forebrain and globus pallidus, that there are distinct vesicle populations for Ach and GABA release (Figure 1B).”
Quote in the paperSubstantial claim - Premisecitation
The net effect of VIP/Chat+ activity on the cortical microcircuit is disinhibition of excitatory pyramidal neurons by engaging multiple cell types across the cortical column.
“The net effect of VIP/Chat+ activity on the cortical microcircuit is disinhibition of excitatory pyramidal neurons by engaging multiple cell types across the cortical column.97,98”
Quote in the paperSubstantial claim0 of 2 sources checked - Premisecitation
Optogenetic excitation of VIP/ChAT+ neurons in motor and visual cortex revealed GABAergic output primarily to other interneuron subtypes, with a bias toward Sst+ cortical interneurons.
“Optogenetic excitation of VIP/Chat+ neurons in the motor and visual cortex revealed GABAergic output primarily to other interneuron subtypes, with a bias toward the Sst+ cortical interneurons.”
Quote in the paperSubstantial claim0 of 2 sources checked - Interpretationreasoning
All DANs that express GAT1 are likely capable of releasing GABA in addition to DA throughout the striatum.
“Therefore, it is likely that all DANs that express GAT1 are capable of GABA release, in addition to DA, throughout striatum.”
Quote in the paperNot a substantial claim - Premisecitation
Selective deletion of Slc17a6 from DA neurons decreases DA release in the ventral striatum.
“decreased DA release in the ventral striatum”
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Striatal GABA release from DANs does not require vGAT.
“striatal GABA release from DANs does not require its typical cognate vesicular transporter vGAT.115”
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- Premisecitation
These studies confirmed that this cortical subtype expresses all genes required for synthesis and release of both GABA and Ach.
“These studies also confirmed that this cortical subtype expresses all the required genes for synthesis and release of both GABA and Ach.”
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- cites [94][95][96]
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Glycinergic synapses from vGluT3+ amacrine cells are selective and shape contrast and size selectivity of suppressed-by-contrast RGCs by reducing tonic firing.
“Glycinergic synapses are highly selective and shape contrast and size selectivity of postsynaptic ''suppressed by contrast'' RGCs by depressing tonic firing.100”
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vGAT is not expressed in vGluT3+ retinal amacrine cells or their axon terminals.
“vGAT is not expressed in vGluT3+ retinal amacrine cells or axon terminals, 102”
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- Premisecitation
GABA is the primary transmitter when the postsynaptic neuron is a Sst+, PV+, or 5HT3aR+ interneuron.
“But GABA is the primary transmitter when the postsynaptic neuron is a Sst+, PV+, or 5HT3aR+ interneuron.”
Quote in the paperSubstantial claim0 of 2 sources checked - Premiseown data
Immunohistochemical analysis supported independent trafficking of vGAT and vAChT in VIP/ChAT+ axon terminals.
“Immunohistochemical analysis also supported independent trafficking of vGAT and vAChT in VIP/Chat+ axon terminals.”
Quote in the paperSubstantial claim - Premisecitation
Optogenetic inhibition of mPFC VIP/ChAT+ neurons after the cue in a 5-choice serial reaction time task reduced correct responses.
“optogenetically inhibiting this population following the cue in a 5-choice serial reaction time task reduced correct responses.98”
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- Interpretationcitation
DA and GABA may be segregated into not fully overlapping and potentially separate vesicle populations, despite both depending on vMAT2 for vesicular loading.
“These findings suggest that DA and GABA may be segregated into not fully overlapping and potentially separate vesicle populations, despite both depending on vMAT2 for vesicular loading.119”
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Individual synaptic vesicles from EP Sst neurons in the LHb contain both GABA and glutamate.
“individual synaptic vesicles from EP Sst neurons in the LHb contain both GABA and glutamate”
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- Interpretationcitation
GABA and Ach coreleased in cortex may act in parallel on different targets to achieve a common function, such as placing cortex in a more excitable and pro-plasticity state.
“GABA and Ach coreleased in the cortex may act in parallel on different targets to achieve a single common function, such as placing the cortex in a more excitable and pro-plasticity state by simultaneously inhibiting Sst+ interneurons with GABA while using Ach release to excite disinhibitory interneurons and activate muscarinic receptors on pyramidal cells.90,97,98,140,141”
Quote in the paperNot a substantial claim0 of 5 sources checked - Interpretationreasoning
During reward-reinforced behaviors, LHb neurons learn to calculate the negative expected value of specific actions or contexts.
“Thus, the neurons of LHb, during reward-reinforced behaviors, learn to calculate the negative expected value of specific actions or contexts.”
Quote in the paperSubstantial claim - Interpretationreasoning
Activity-dependent insertion and removal of GABA and glutamate ionotropic receptors at postsynaptic terminals opposed to GABA/glutamate coreleasing synapses provides a mechanism for LHb neurons to learn to calculate expected value from diverse inputs.
“The activity-dependent insertion and removal of GABA and glutamate ionotropic receptors from postsynaptic terminals opposed to GABA/glutamate coreleasing synapses provides a mechanism for LHb neurons to learn to calculate expected value from information about sensory state, past experience, motor action, and other variables received from diverse brain areas, including EP.”
Quote in the paperSubstantial claim - Interpretationcitation
Dopamine, GABA, and glutamate released by DANs may elicit prolonged waves of postsynaptic effects, from millisecond excitability changes to tens-of-seconds biochemical signaling and excitability.
“the dopamine, GABA, and glutamate released by DANs may elicit prolonged waves of postsynaptic effects, cascading from the millisecond changes in excitability triggered by ionotropic receptors, to the tens of seconds on biochemical signaling and excitability 109,115,122,123 (Figure 3A).”
Quote in the paperNot a substantial claim0 of 4 sources checked - Study design and conductcitation
Most analyses in these single-cell sequencing studies are performed on populations of neurons.
“An important caveat to these findings is that most analyses performed in these studies are performed on populations of neurons.”
Quote in the paperSubstantial claim0 of 5 sources checked - Premisecitation
Non-DA neurons within the VTA encode experienced value.
“As a recent study reported that non-DA neurons within VTA encode experienced value, 127”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [127] source
Not checked in the free run.
- Premisecitation
Single-cell sequencing studies in the brain have shown that neuron types with the genetic constituents required for releasing more than one neurotransmitter are ubiquitous.
“These studies have also shown the ubiquity of neuron types that have the genetic constituents required for the release of more than one neurotransmitter.6,7,9,40,131”
Quote in the paperSubstantial claim0 of 5 sources checked - Study design and conductnone given
Classical minimal stimulation approaches using extracellular stimulation are confounded when axons from many different presynaptic neuron types overlap, making it impossible to determine whether one axon is being stimulated.
“classical minimal stimulation approaches using extracellular stimulation are confounded when axons from many different types of presynaptic neurons are overlapping, making it impossible to determine whether one axon is being stimulated”
Quote in the paperSubstantial claim - Interpretationreasoning
VTA DA neurons could calculate reward-prediction error by subtracting the predicted value provided by the LHb from the experienced value provided by non-DA VTA neurons.
“VTA DA neurons could simply calculate RPE by subtracting the predicted value (provided by LHb) from the experienced value (provided by non-DA VTA neurons).”
Quote in the paperSubstantial claim- Rests on an assumption: VTA DA neurons compute reward-prediction error as the experienced value of an activity minus its predicted value.
- May combine two claims. 49
- Classified as probably not a substantial claim. 4
May combine two claims.
InterpretationreasoningNeuroscience can now confidently identify when and where cotransmission occurs and reveal its contribution to normal and pathological brain function.
“We conclude that neuroscience is now at a stage where we can confidently identify when and where cotransmission oc-curs in the brain, as well as reveal its contribution to normal and pathological brain function.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim.
Premisenone givenRecent technological advances have made it possible to identify new multitransmitter neurons and study their synaptic properties.
“We highlight recent technological innovations that have made the identification of new multitransmitter neurons and the study of their synaptic properties possible.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisereasoningKnowledge of these components allows precise genetic perturbation of corelease by manipulating each neurotransmitter individually.
“Finally, knowledge of these components allows precise genetic perturbation of corelease by manipulating each neurotransmitter individually.”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationIntersectional genetic and viral tools allow manipulation of specific neuronal populations suspected of neurotransmitter corelease and enable functional analysis of cotransmitting neurons in vitro and in vivo.
“new ''intersectional'' genetic and viral tools permit manipulation of specific neuronal populations suspected of neurotransmitter corelease 10 and enable functional analysis of cotransmitting neurons in vitro and in vivo.11,12”
Quote in the paperSubstantial claim0 of 3 sources checkedMay combine two claims.
PremisecitationImmunogold EM indicates that single axon terminals make both symmetric and asymmetric synapses, suggesting segregation of vesicles into GABAergic and glutamatergic synapses within the same axon and bouton.
“Interestingly, immunogold EM also indicated that single axon terminals make both symmetric (GABAergic) and asymmetric (glutamatergic) synapses (see Figure 5 in Root et al. 33 ), suggesting segregation of synaptic vesicles into glutamatergic and GABAergic synapses within the same axon and bouton.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [33] source
Not checked in the free run.
May combine two claims.
PremisecitationLHb-projecting EP/GPi neurons were later found to transmit both glutamate and GABA and to be capable of exciting and inhibiting LHb neurons.
“Later, they were found to simultaneously transmit both glutamate and GABA and to be capable of both exciting and inhibiting LHb neurons 40,26 (Figure 1A).”
Quote in the paperSubstantial claim0 of 2 sources checkedMay combine two claims.
PremisecitationGlutamate is an anion at neutral pH, and its loading into vesicles produces charge and proton changes opposite to vMAT and VAChT.
“Glutamate is an anion at neutral pH, and loading of glutamate into vesicles produces a change in charge and H+ opposite to vMAT and VAChT.20”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [20] source
Not checked in the free run.
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PremisecitationGlycine receptor kinetics are faster than GABA receptor kinetics, producing IPSCs with fast and slow components.
“The kinetics of glycine receptors are faster than those of GABA receptors, resulting in an inhibitory post synaptic current (IPSC) with fast and slow components.44,45,49”
Quote in the paperNot a substantial claim0 of 3 sources checkedMay combine two claims.
PremisecitationThese terminals arose from long-range supramammillary projections, and GABAergic and glutamatergic vesicles segregated into distinct pools and presynaptic terminals.
“These studies found that these terminals arose from long-range projections from the SuM and provided evidence that the GABAergic and glutamatergic vesicles segregated into distinct pools and occupied distinct presynaptic terminals.28”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [28] source
Not checked in the free run.
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PremisecitationImmunogold EM shows that more than 60% of VTA axon terminals in LHb are positive for both vGAT and vGluT2, with smaller subsets positive for one transporter.
“Immunogold EM indicates that >60% of the axon terminals in LHb from VTA are positive for both vGAT and vGluT2, while smaller subsets label for one or the other transporter.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [33] source
Not checked in the free run.
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PremisecitationThe structure, organization, and regulation of postsynaptic receptors and related molecular constituents of GABA/glutamate synapses remain unknown but appear specialized within LHb due to low PSD-95 expression.
“The structure, organization, and regulation of the postsynaptic receptors and related molecular constituents of GABA/glutamate synapses remain unknown but appear specialized within LHb due to low expression of the glutamatergic postsynaptic-terminal-associated MAGUK PSD-95.25”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [25] source
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PremisecitationEP/GPi has diverse neuronal populations and functions, primarily via dense projections targeting the LHb.
“However, EP/GPi has diverse neuronal populations and functions, the latter primarily via its dense projections targeting the LHb.[35][36][37]”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [35][36][37]
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Interpretationown dataThese results support a model in which individual synaptic vesicles express both vGAT and vGluT2 and release GABA and glutamate simultaneously to activate postsynaptic receptors across the cleft.
“These results support a model in which individual synaptic vesicles express both vGAT and vGluT2, and GABA/glutamate are released simultaneously to activate postsynaptic receptors across the synaptic cleft.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [25] source
Not checked in the free run.
May combine two claims.
PremisecitationThese VTA neurons monosynaptically connect to lateral habenula neurons and cotransmit GABA and glutamate onto individual LHb neurons.
“They monosynaptically connect to neurons within the lateral habenula (mostly medial subregions) and cotransmit Cotransmission: process by which two (or more) neurotransmitters are synaptically released in response to an action potential and detected by receptors on the postsynaptic”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [32] source
Not checked in the free run.
May combine two claims.
InterpretationcitationThe excitatory/inhibitory ratio at each synapse can be adjusted independently by regulating vesicular transporter activity or postsynaptic receptor composition.
“The excitatory/ inhibitory ratio at each synapse can be adjusted independently by regulating the activity of the vesicular transporters 26,41 or adjusting the composition of postsynaptic receptors.”
Quote in the paperSubstantial claim0 of 2 sources checkedMay combine two claims.
PremisecitationLHb-projecting EP/GPi neurons were first suggested to be glutamatergic, purely excitatory, and to signal aversive/negative outcomes.
“Due to immunohistochemical and behavioral findings, LHb-projecting EP/GPi neurons were first suggested to be glutamatergic, purely excitatory, and signal aversive/negative outcomes.38,39”
Quote in the paperNot a substantial claim0 of 2 sources checkedMay combine two claims.
PremisecitationGABA/glutamate coreleasing neurons in mouse EP and human GPi are marked by Sst expression, enabling specific targeting.
“GABA/glutamate coreleasing neurons in the EP of mice and GPi in humans were found to be marked by expression of Sst, facilitating specific targeting of these neurons in functional studies.40”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [40] source
Not checked in the free run.
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PremisecitationBy adulthood, GABA and glycine are both inhibitory, activating chloride-permeable ligand-gated ion channels and hyperpolarizing postsynaptic targets.
“By adulthood, both transmitters are inhibitory, activating their cognate chloride permeable ligand-gated ion channels, and hyperpolarizing their postsynaptic targets.48”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [48] source
Not checked in the free run.
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PremisecitationvGAT acts as a GABA/H+ antiporter rather than a GABA/Cl cotransporter and depends on both pH gradient and membrane potential.
“Studies conclude that vGAT acts as a GABA/H+ antiporter rather than a GABA/ClÀ cotransporter and depends on both DpH and DJ.23,24”
Quote in the paperSubstantial claim0 of 2 sources checkedMay combine two claims.
PremisecitationvMAT1/2 and VAChT transport positively charged neurotransmitters in exchange for two protons and depend more on the pH gradient than on membrane potential.
“Vesicular transporters for monoamines (vMAT1/2) and Ach (VAChT) transport positively charged neurotransmitters in exchange for 2H+ and are more dependent on DpH than DJ.18,19”
Quote in the paperSubstantial claim0 of 2 sources checkedMay combine two claims.
InterpretationreasoningData suggest a complementary or synergistic relationship between glutamate and 5-HT release from 5-HT/vGluT3+ neurons, with direct effects on cortical and midbrain structures.
“Together, these data suggest a complementary or synergistic relationship between glutamate and 5-HT release from 5-HT/vGluT3+ neurons, with direct effects on cortical and midbrain structures.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationGlutamate release onto SPNs activates ionotropic glutamate receptors with distinct AMPA/NMDA ratios compared with cortico-striatal synapses, suggesting distinct plasticity rules.
“Glutamate release onto SPNs activates postsynaptic ionotropic glutamate receptors with distinct AMPA/NMDA ratios compared with cortico-striatal synapses, suggesting distinct plasticity rules from these disparate inputs.60”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [60] source
Not checked in the free run.
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PremisecitationSingle-cell sequencing and ISH confirmed that these medial habenula neurons reside in the ventral and ventrolateral subregion and form a genetically distinct subtype.
“Single-cell sequencing and in-situ hybridization (ISH) studies confirmed that these neurons reside in the ventral and ventrolateral subregion of the mHb and form a genet-ically distinct subtype.58,59”
Quote in the paperNot a substantial claim0 of 2 sources checkedMay combine two claims.
PremisecitationFurther studies suggested that SACs also express GABA synthetic enzymes and can release GABA.
“Further studies suggested that these cells also express GABA synthetic enzymes and are capable of releasing GABA.84,85”
Quote in the paperSubstantial claim0 of 2 sources checkedMay combine two claims.
Premisecitation5-HT/vGluT3+ neurons from the dorsal raphe target the VTA, make asymmetric synapses, and monosynaptically release glutamate to excite accumbal-projecting dopamine neurons.
“5-HT/vGluT3+ neurons from the dorsal raphe also target the VTA, where they make asymmetric synapses and monosynaptically release glutamate to excite accumbal-projecting dopamine neurons.79”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [79] source
Not checked in the free run.
May combine two claims.
PremisecitationGABA release from SACs is restricted to dendrites of postsynaptic DSGCs' null direction, whereas Ach release is not spatially restricted.
“Release of GABA from SACs is restricted to the dendrites of the postsynaptic DSGCs' null direction, whereas release of Ach is not spatially restricted.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [86] source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationThese axonally induced action potentials can drive DA release in vitro and have been hypothesized to locally control DA release within the striatum.
“These axonally induced APs are capable of driving DA release in vitro 61 and have been hypothesized to act as a mechanism for local control of DA release within the striatum.[64][65][66][67][68]”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [61] source
Not checked in the free run.
- cites [64][65][66][67][68]
Not checked in the free run.
May combine two claims.
InterpretationreasoningCompetition for vesicular transport may be a general feature of co-packaging multitransmitter neurons, likely lowering the amount of each neurotransmitter loaded per vesicle compared with one-transmitter vesicles.
“This may be a general feature of multitransmitter neurons that exhibit co-packaging, as it likely puts a lower limit on the amount of each neurotransmitter loaded into a single vesicle when compared with one vesicle with one transmitter.”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationDeletion of either Tph1 or vGluT3 from 5-HT/vGluT3+ neurons increases anxiety-like behaviors, suggesting that disrupting signaling from either transmitter has similar consequences.
“In addition, deletion of either serotonin synthetic enzyme tryptophan hydroxylase 1 (Tph1) or vGluT3 (Slc18a8) from 5-HT/vGluT3+ neurons results in increased anxiety-like behaviors, suggesting that disrupting signaling from either transmitter has similar consequences.78,80”
Quote in the paperSubstantial claim0 of 2 sources checkedMay combine two claims.
PremisecitationThe proportion of postsynaptic layer 1 interneurons receiving an EPSC or an IPSC differed significantly, and most received only one type of input.
“The proportion of postsynaptic layer 1 interneurons receiving an EPSC or an IPSC differed significantly, and most received only one type of input.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [89] source
Not checked in the free run.
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Interpretationnone givenSeparate neuronal subpopulations can cotransmit Ach and GABA; these Ach-releasing neurons form nonoverlapping populations, reside in different brain regions, and use distinct synaptic mechanisms for corelease.
“In contrast to neurons that cotransmit Ach and glutamate, separate neuronal subpopulations are capable of cotransmitting Ach and GABA.These two types of Ach-releasing neurons form nonoverlapping neuronal populations, reside in different brain regions, and have distinct synaptic mechanisms for corelease of neurotransmitters.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationAt mHb-IPN synapses, AMPA and NMDA receptors are activated by single action potentials, but nicotinic Ach receptors are activated only slowly after prolonged 50 Hz 5 s stimulation, indicating different transmission modes for glutamate and Ach.
“Although postsynaptic AMPA and NMDA receptors are activated by single action potentials (APs) in the presynaptic axon, nicotinic Ach receptors (nAchRs) were only activated slowly following prolonged (50 Hz, 5 s) stimulation of inputs, indicating that glutamate and Ach have different transmission modes.56”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [56] source
Not checked in the free run.
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PremisecitationDorsal raphe 5-HT/vGluT3+ neurons project widely throughout the cortex and increase or decrease their activity to reward and punish, respectively.
“Those in the dorsal raphe project widely throughout the cortex and increase or decrease their activity to reward and punish, respectively.76,78”
Quote in the paperNot a substantial claim0 of 2 sources checkedMay combine two claims.
PremisecitationDirect recordings from DA axon terminals in the striatum determined that Ach release from CINs onto dopamine axons primarily activates nAchRs and can locally induce action potentials.
“Heroic electrophysiological experiments that intracellularly recorded directly from DA axon terminals in the striatum unambiguously determined that synaptic release of Ach from CINs onto dopamine axons primarily activates nAchRs and is even capable of locally inducing APs.62”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [62] source
Not checked in the free run.
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InterpretationreasoningSynaptic potency depends not only on postsynaptic receptor number but also on presynaptic transmitter concentrations and vesicular loading.
“These results suggest that the potency of a synapse depends not only on the number of postsynaptic receptors but also on the concentrations of presynaptic transmitter and how much transmitter is loaded into the vesicle.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [51] source
Not checked in the free run.
May combine two claims.
PremisecitationSeveral groups found that vGluT and VAChT function synergistically, and depletion of one transporter or neurotransmitter also depletes loading and release of the other.
“Interestingly, several groups have found that vGluT and VAChT function synergistically and that depletion of one transporter or neurotransmitter also depletes loading and release of the other.21,22,63,69”
Quote in the paperNot a substantial claim0 of 4 sources checkedMay combine two claims.
PremisecitationAch and GABA release from SACs are differentially sensitive to calcium concentration and calcium channel antagonists, suggesting separate vesicle populations.
“Ach and GABA release are differentially sensitive to calcium concentration and calcium channel antagonists, suggesting separate vesicle populations.86”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [86] source
Not checked in the free run.
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PremisecitationThe GABA-mediated IPSC was ablated by selective genetic deletion of Slc32a1 in Chat-Cre+ neurons, while the nicotinic EPSC persisted, indicating that Ach loading did not depend on GABA vesicular transport.
“The GABA-mediated IPSC could be ablated by selective genetic deletion of Slc32a1 (vGAT) in Chat-Cre+ neurons, while the nicotinic excitatory postsynaptic current (EPSC) persisted, indicating that the loading of Ach did not depend on GABA vesicular transport.89”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [89] source
Not checked in the free run.
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PremisecitationIn mouse and rat medial prefrontal cortex, cholinergic transmission from VIP/ChAT+ neurons onto layer 1 interneurons occurs with higher probability and evokes larger postsynaptic responses.
“as cholinergic output from VIP/ChAT+ neurons to layer 1 interneurons in the mouse and rat medial prefrontal cortex occurs at a higher probability and produces a larger postsynaptic response.97,98”
Quote in the paperNot a substantial claim0 of 2 sources checkedMay combine two claims.
PremisecitationDA release affects postsynaptic cells much more slowly, with about a 500-ms delay, than GABA or glutamate synaptic currents, which last 2-4 ms.
“DA release affects the postsynaptic cell considerably more slowly ($500-ms delay) than the synaptic currents generated by either cotransmitted GABA or glutamate (2-4 ms).115,123”
Quote in the paperSubstantial claim0 of 2 sources checkedMay combine two claims.
PremisecitationvGluT2+ and vMAT2+ vesicles segregate into distinct vesicle populations and separate axonal boutons or microdomains.
“Immunogold EM studies and immunoprecipitation experiments suggest that vGluT2+ and vMAT2+ vesicles segregate into distinct vesicle populations and even separate axonal boutons/microdomains, 111”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [111] source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
InterpretationcitationThe regional differences in VIP/ChAT+ transmission may arise from a distinct population of VIP-negative cholinergic interneurons in mPFC.
“However, these differences may be due to the existence of a unique population of VIPÀ CINs in this region.97”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [97] source
Not checked in the free run.
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InterpretationreasoningvGluT3+ retinal amacrine cells simultaneously excite contrast-activated cells and inhibit contrast-suppressed cells, giving them a dual role in retinal circuits.
“Therefore, vGluT3+ retinal amacrine cells simultaneously excite cells activated by contrast and inhibit cells suppressed by contrast, performing a dual role in retinal circuits.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationvGluT2 can stimulate monoamine uptake into synaptic vesicles by vMAT2 by lowering intravesicular pH, providing a mechanism for reduced DA release when vGluT2 is absent.
“vGluT2 was capable of stimulating monoamine uptake into synaptic vesicles by vMAT2 by lowering the intravesicular pH, providing a mechanism for reduced DA release in the absence of vGluT2.113”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [113] source
Not checked in the free run.
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PremisecitationBipolar cortical interneurons expressing VIP and ChAT were first identified by immunohistochemistry in rodents and account for about one third of all VIP+ cortical neurons.
“Bipolar cortical interneurons expressing vasoactive intestinal polypeptide (VIP) and ChAT were first identified using immunohistochemistry in rodents and account for $1/3 of all VIP+ cortical neurons.92,93”
Quote in the paperNot a substantial claim0 of 2 sources checkedMay combine two claims.
InterpretationreasoningAt the mHb-to-IPN synapse, glutamate acts as a temporally precise point-to-point transmitter, while Ach acts as a volume transmitter that activates postsynaptic receptors mainly at high firing rates.
“therefore, glutamate acts as the temporally precise, point-to-point transmitter, while Ach acts as a volume transmitter, only accumulating enough to activate postsynaptic receptors at high presynaptic firing rates.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationOlfactory-bulb-projecting cholinergic neurons from the basal forebrain cotransmit GABA and Ach onto deep short axon cells within the internal plexiform layer, reinforcing pervasive GABA cotransmission from this population.
“More recently, olfactorybulb-projecting cholinergic neurons from the basal forebrain were also shown to cotransmit GABA and Ach onto deep, short axon cells within the internal plexiform layer of the bulb, reinforcing the pervasive nature of GABA cotransmission from this population of cholinergic neurons throughout the brain.91”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [91] source
Not checked in the free run.
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PremisecitationGAT1 is both necessary and sufficient to sustain GABA release in DANs.
“only the GABA transporter, GAT1, is both necessary and sufficient to sustain GABA release in DANs”
Quote in the paperSubstantial claim0 of 2 sources checkedMay combine two claims.
PremisecitationCholinergic EPSCs from VIP/ChAT+ neurons were sparse but primarily detected in layer 1 interneurons and other VIP cells.
“Cholinergic EPSCs were sparse, but primarily detected in layer 1 interneurons and other VIP cells.97”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [97] source
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PremisecitationVentral midbrain dopamine neurons are diverse, project to different regions, and can release neurotransmitters besides dopamine.
“Dopamine neurons of the ventral midbrain (DANs) comprise a diverse population of neurons targeting different regions and capable of releasing multiple neurotransmitters in addition to dopamine.31,103,104”
Quote in the paperSubstantial claim0 of 3 sources checkedMay combine two claims.
PremisecitationDA release, via cAMP regulation, controls PKA activity in SPNs over tens of seconds, with differential effects on D1 and D2 receptor-expressing neurons.
“Real-time monitoring of the kinase activity in behaving animals indicates that DA release, via regulation of intracellular cAMP production, controls the activity of protein kinase A (PKA) in SPNs over the timescale of tens of seconds, with differential effects on neurons that express type 1 or type 2 dopamine receptors.122”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [122] source
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PremisecitationLHb neurons increase their activity when adverse outcomes occur or are predicted and provide disynaptic inhibitory input to VTA DANs.
“LHb neurons increase their activity when adverse outcomes occur or are predicted and provide a disynaptic inhibitory (-GABAergic) input to VTA DANs.125,126”
Quote in the paperSubstantial claim0 of 2 sources checked
The paper relies on this without support.
Many, if not all, neurons release more than one neurotransmitter.
“as many, if not all, neurons release more than one neurotransmitter.”
The paper relies on this without support.
Vesicular release of a neurotransmitter requires presynaptic accumulation of the signaling molecule to a concentration sufficient for packaging into a vesicle and release.
“Vesicular release of a neurotransmitter requires a neuron to accumulate the signaling molecule in the presynaptic terminal to a concentration that permits it to be packaged into a vesicle and released.”
The paper relies on this without support.
Neurons can take up and package neurotransmitters through atypical pathways, making corelease determination sometimes difficult.
“Importantly, neurons can uptake and package neurotransmitters using atypical pathways, making this process sometimes difficult.”
The paper relies on this without support.
VTA DA neurons compute reward-prediction error as the experienced value of an activity minus its predicted value.
“VTA DAN neurons calculate reward-prediction error (RPE)-the difference between the experienced value of an activity and that which had been predicted.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
It is known that in many midbrain dopamine neurons (VTA and SNc), Aldh1a1 is used for synthesizing GABA in the absence of Gad1 or Gad2, and Slc18a2 is used for co-release of dopamine and GABA in the absence of Slc32a1.
“It is known that in many midbrain dopamine neurons (in VTA and SNc), Aldh1a1 is used for synthesizing GABA in the absence of Gad1 or Gad2, and Slc18a2 is used for co-release of dopamine and GABA in the absence of Slc32a157.”
From A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain (2023) · cites this paper as [57]
The DA/GABA section (page not provided) says dopamine neurons release GABA without canonical GAD65/67 synthesis or vGAT packaging, and that vMAT2 packages GABA into vesicles. But it does not establish that Aldh1a1 synthesizes GABA within those neurons: it says that mechanism was proposed, while cell-type-specific evidence points to an effect in non-dopaminergic cells instead. (LLM, conf=0.91)
Experimental — accuracy not yet measuredMany neurotransmitter co-release patterns had been documented previously.
“Although many of these neurotransmitter co-release patterns had been documented previously55–57”
From A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain (2023) · cites this paper as [57]
The assignment of neurotransmitter types based on synthesizing enzymes and transporter genes is conservative; there may be even more diversity in neurotransmitter co-release patterns if other unconventional transmitter release routes are considered.
“Of note, our assignment of neurotransmitter types based on synthesizing enzymes and transporter genes is conservative; there may be even more diversity in neurotransmitter co-release patterns if other unconventional transmitter release routes are considered57,118.”
From A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain (2023) · cites this paper as [57]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Two different gene names are given for vGluT3
MinorThe serotonin section identifies the gene for vGluT3 as Slc18a8, but an earlier passage identifies it as Slc17a8. Table 1 also lists Slc17a8 for vGluT3.
“deletion of either serotonin synthetic enzyme tryptophan hydroxylase 1 (Tph1) or vGluT3 (Slc18a8) from 5-HT/vGluT3+ neurons”
“glutamate (vGluT2/3; Slc17a6/Slc17a8)”
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Molecular diversity and specializations among the cells of the adult mouse brain
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Shared and distinct transcriptomic cell types across neocortical areas
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A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain
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Ventral tegmental area: cellular heterogeneity, connectivity and behaviour
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VGLUT2 Trafficking Is Differentially Regulated by Adaptor Proteins AP-1 and AP-3
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Analytical approaches to examine gamma-aminobutyric acid and glutamate vesicular co-packaging
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Self-citation
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A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain
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Mechanisms of neuromodulatory volume transmission
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A neurotransmitter atlas of C. elegans males and hermaphrodites
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A neurotransmitter atlas of C. elegans males and hermaphroditesPreprint
Wang, C., Vidal, B., Sural, S., Loer, C. M., Aguilar, G. R., Merritt, D. M., Toker, I. A., Vogt, M. C., Cros, C., & Hobert, O. (2024) · eLife · doi:10.7554/elife.95402 · Cited by 22 · see citing works
The behavioral relevance of a modular organization in the lateral habenula
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Widespread co-release of glutamate and GABA throughout the mouse brain
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Temperature effects on the neuronal dynamics and Hamilton energy
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A connectomic resource for neural cataloguing and circuit dissection of the larval zebrafish brainPreprint
Petkova, M. D., Januszewski, M., Blakely, T. M., Herrera, K. J., Schuhknecht, G. F. P., Tiller, R., Choi, J., Schalek, R. L., Boulanger-Weill, J., Peleg, A., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.06.10.658982 · Cited by 14 · see citing works
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Hidden in the white matter: Current views on interstitial white matter neurons
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Self-citationAxonal neurotransmitter release in the regulation of myelination
Marshall-Phelps, K. L., & Almeida, R. (2024) · Bioscience Reports · doi:10.1042/bsr20231616 · Cited by 6 · see citing works
A call for a unified and multimodal definition of cellular identity in the enteric nervous system
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Neuropeptides as transmitters and regulators of the locus coeruleus noradrenergic system
Becker, L. J., Martin, M. M., Hughes, A. C., Mulvey, B., Kuo, C., Piantadosi, S. C., Bruchas, M. R., Martinowich, K., Meye, F. J., Schwarz, L. A., et al. (2025) · Pharmacological Reviews · doi:10.1016/j.pharmr.2025.100081 · Cited by 5 · see citing works
Diverse perceptual biases emerge from Hebbian plasticity in a recurrent neural network model
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Role of adaptor protein complexes in generating functionally distinct synaptic vesicle pools
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Qiu, X., Wu, Y., Liu, Y., Zhuo, M., Chen, K., Takai, Y., Kang, I., Shimasaki, Y., & Oshima, Y. (2026) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2026.112027 · Cited by 4 · see citing works
A neurotransmitter atlas of C. elegans males and hermaphroditesPreprint
Wang, C., Vidal, B., Sural, S., Loer, C. M., Aguilar, G. R., Merritt, D. M., Toker, I. A., Vogt, M. C., Cros, C., & Hobert, O. (2024) · eLife · doi:10.7554/elife.95402.2 · Cited by 4 · see citing works
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A neurotransmitter atlas of the nervous system of C. elegans males and hermaphroditesPreprint
Wang, C., Vidal, B., Sural, S., Merritt, D. M., Toker, I. A., Vogt, M. C., Cros, C., & Hobert, O. (2024) · eLife · doi:10.7554/elife.95402.1 · Cited by 3 · see citing works
Bi-Modal Synapse Based on a Short-Channel Ferroelectric van der Waals Heterostructure
Ram, A., Fusil, S., Masood, S. B., Rajak, N. K., Samanta, G., Soliman, M., Taniguchi, T., Watanabe, K., Doudin, B., Ouerghi, A., et al. (2025) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.5c16593 · Cited by 2 · see citing works
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Synaptic summation shapes information transfer in GABA-glutamate co-transmission
Krubitski, B., Ceballos, C. C., Roachford, T., & Pena, R. F. O. (2025) · Cognitive Neurodynamics · doi:10.1007/s11571-025-10383-2 · Cited by 1 · see citing works
Aleman, A., & Donlea, J. M. (2026) · SLEEP · doi:10.1093/sleep/zsag153 · Cited by 1 · see citing works
Hirai, H., Konno, K., Yamasaki, M., Watanabe, M., Sakaba, T., & Hashimotodani, Y. (2024) · eLife · doi:10.7554/elife.99711.2 · Cited by 1 · see citing works
Locantore, J., Liu, Y., White, J., Wallace, J. B., Beron, C. C., Kraft, E., Sabatini, B. L., & Wallace, M. L. (2025) · eLife · doi:10.7554/elife.100488.2 · Cited by 1 · see citing works
Self-citationGABA-glutamate corelease is a mechanism for state-dependent neurotransmissionPreprint
Warlow, S. M., Dowlat, D. S., Hollon, N. G., Faget, L. C., Oriol, L., Zell, V., Zweifel, L. S., & Hnasko, T. S. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.19.689286 · Cited by 1 · see citing works
Evolutionary principles underlying neuron subtype encoding and diversification in animalsPreprint
Hehmeyer, J., Harris, D., Lowe, C. J., & Marlow, H. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.04.13.718258 · Cited by 1 · see citing works
Gender diversity; parvalbumin interneurons; flawed clinical trials
Adams, J. U. (2023) · The Transmitter · doi:10.53053/cqol4376
Characterization of Identified Dopaminergic Neurons in the Mouse Olfactory Bulb and MidbrainPreprint
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Characterization of Identified Dopaminergic Neurons in the Mouse Forebrain and MidbrainPreprint
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Self-citationFan, L., Deng, B., Hao, X., Qiu, X., & Liu, Y. (2024) · Neuroscience Letters · doi:10.1016/j.neulet.2024.138034
Locantore, J., Liu, Y., White, J., Wallace, J. B., Beron, C. C., Kraft, E., Sabatini, B. L., & Wallace, M. L. (2025) · eLife · doi:10.7554/elife.100488.3.sa4
Self-citationDivergent excitatory and inhibitory signaling in a head direction circuitPreprint
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Local Glutamate-Glutamine Cycling Underlies Presynaptic ATP Homeostasis
Maex, R. (2026) · Neural Computation · doi:10.1162/neco.a.1490
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Characterizing neuronal cell bodies in white matter tracts of the human brain
VanderBerg, D., Perlman, K., Davoli, M. A., Turecki, G., & Mechawar, N. (2026) · Brain Structure and Function · doi:10.1007/s00429-026-03112-w
Neurotransmitter co-transmission: synaptic architectures, functional logic, and emerging tools
Tunc‐Ozcan, E. (2026) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2026.1862021
Gutierrez, G. J., Baas-Thomas, N., & Marder, E. E. (2026) · Journal of Neurophysiology · doi:10.1152/jn.00196.2026
Varga, A. G., Reid, B. T., Maletz, S. N., Dossat, A. M., & Levitt, E. S. (2026) · Journal of Neuroscience · doi:10.1523/jneurosci.2199-25.2026
Pathania, I., Mourya, A. K., Sharma, A., Kumar, A., & Singh, I. P. (2026) · Journal of Pharmacy and Pharmacology · doi:10.1093/jpp/rgag081
Neurotransmitter Systems and Systemic Resilience in the Healthy Aging Brain
Ramı́rez-Expósito, M. J., Martı́nez-Martos, J. M., & Cueto‐Ureña, C. (2026) · Applied Biosciences · doi:10.3390/applbiosci5040098
- Authors
- Wallace, M. L., & Sabatini, B. L.
- Affiliations
- Boston University (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Wallace, Michael L.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2023-10
- Volume
- 111
- Issue
- 19
- Pages
- 2969-2983
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC10592565
- OpenAlex
- W4384564286
- Cited by
- 59
- References
- 141
- Citations by year
- 2026: 13 · 2025: 13 · 2024: 29 · 2023: 4
- FWCI
- 2.27
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 369 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Whitehall Foundation
- NINDS (R01NS103226)
- National Institutes of Health
- Brain and Behavior Research Foundation
- National Alliance for Research on Schizophrenia and Depression (IG256AX89O, R01NS103226)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Keywords
- synaptic vesicles, axon terminals, brain circuits, synaptic properties, central nervous system, neuromodulation, neurotoxicity
- MeSH terms
- Animals, Brain, Central Nervous System, Mammals, Synaptic Transmission, Neurons, Neurotransmitter Agents, Glutamic Acid
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-09.
Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-09.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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