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Cited by 136Neuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on BehaviorMemory and Neural Mechanisms

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Control of Amygdala Circuits by 5-HT Neurons via 5-HT and Glutamate Cotransmission

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Sengupta, Ayesha, Bocchio, Marco, Bannerman, David M., Sharp, Trevor, Capogna, Marco·2017·The Journal of Neuroscience
DOI 10.1523/jneurosci.2238-16.2016PMC PMC5320609
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Abstract

The serotonin (5-HT) system and the amygdala are key regulators of emotional behavior. Several lines of evidence suggest that 5-HT transmission in the amygdala is implicated in the susceptibility and drug treatment of mood disorders. Therefore, elucidating the physiological mechanisms through which midbrain 5-HT neurons modulate amygdala circuits could be pivotal in understanding emotional regulation in health and disease. To shed light on these mechanisms, we performed patch-clamp recordings from basal amygdala (BA) neurons in brain slices from mice with channelrhodopsin genetically targeted to 5-HT neurons. Optical stimulation of 5-HT terminals at low frequencies (≤1 Hz) evoked a short-latency excitation of BA interneurons (INs) that was depressed at higher frequencies. Pharmacological analysis revealed that this effect was mediated by glutamate and not 5-HT because it was abolished by ionotropic glutamate receptor antagonists. Optical stimulation of 5-HT terminals at higher frequencies (10–20 Hz) evoked both slow excitation and slow inhibition of INs. These effects were mediated by 5-HT because they were blocked by antagonists of 5-HT2Aand 5-HT1Areceptors, respectively. These fast glutamate- and slow 5-HT-mediated responses often coexisted in the same neuron. Interestingly, fast-spiking and non-fast-spiking INs displayed differential modulation by glutamate and 5-HT. Furthermore, optical stimulation of 5-HT terminals did not evoke glutamate release onto BA principal neurons, but inhibited these cells directly via activation of 5-HT1Areceptors and indirectly via enhanced GABA release. Collectively, these findings suggest that 5-HT neurons exert a frequency-dependent, cell-type-specific control over BA circuitry via 5-HT and glutamate co-release to inhibit the BA output. SIGNIFICANCE STATEMENTThe modulation of the amygdala by serotonin (5-HT) is important for emotional regulation and is implicated in the pathogenesis and treatment of affective disorders. Therefore, it is essential to determine the physiological mechanisms through which 5-HT neurons in the dorsal raphe nuclei modulate amygdala circuits. Here, we combined optogenetic, electrophysiological, and pharmacological approaches to study the effects of activation of 5-HT axons in the basal nucleus of the amygdala (BA). We found that 5-HT neurons co-release 5-HT and glutamate onto BA neurons in a cell-type-specific and frequency-dependent manner. Therefore, we suggest that theories on the contribution of 5-HT neurons to amygdala function should be revised to incorporate the concept of 5-HT/glutamate cotransmission.

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Figure 1. Expression of ChR2 in DRN 5-HT neurons. A, Cre-dependent expression of ChR2/YFP in the DRN of SERT-Cre mice. B, Overlap between ChR2/YFP and 5-HT expression in the DRN and lack of ChR2/YFP expression in the median raphe nucleus (MRN). C, Maximum-intensity projection (z-stack: 4.2 μm, 0.21 μm optical sections) showing expression of ChR2/YFP in the membrane of 5-HT+ DRN neurons. D, Light pulses (5 ms) delivered at 20 Hz evoke inward currents in voltage clamp (top) and action potentials in current clamp (bottom) in a DRN neuron expressing ChR2/YFP. E, ChR2/YFP+ axons innervating the anterior (E1) and posterior BLA (E2); the BA shows a denser innervation than the LA. AP, Anteroposterior distance from bregma. F, Overlap between 5-HT and ChR2/YFP expression in the BLA. G, Representative image showing a 5-HT+ axon in the BA that also expresses ChR2/YFP.
Figure 1. Expression of ChR2 in DRN 5-HT neurons. A, Cre-dependent expression of ChR2/YFP in the DRN of SERT-Cre mice. B, Overlap between ChR2/YFP and 5-HT expression in the DRN and lack of ChR2/YFP expression in the median raphe nucleus (MRN). C, Maximum-intensity projection (z-stack: 4.2 μm, 0.21 μm optical sections) showing expression of ChR2/YFP in the membrane of 5-HT+ DRN neurons. D, Light pulses (5 ms) delivered at 20 Hz evoke inward currents in voltage clamp (top) and action potentials in current clamp (bottom) in a DRN neuron expressing ChR2/YFP. E, ChR2/YFP+ axons innervating the anterior (E1) and posterior BLA (E2); the BA shows a denser innervation than the LA. AP, Anteroposterior distance from bregma. F, Overlap between 5-HT and ChR2/YFP expression in the BLA. G, Representative image showing a 5-HT+ axon in the BA that also expresses ChR2/YFP.CC BY · PubMed Central
Figure 2. 5-HT neurons release glutamate onto BA INs. A, Representative biocytin-filled BA IN showing a dense local axon (left) and a spiny dendrite (right). B, Example of a voltage-clamp (−70 mV) trace from a BA IN showing a fast EPSC evoked by a single light pulse (3 ms) activation of DRN axons (top); the fast EPSC is blocked by AMPA/kainate and the NMDA receptor antagonists NBQX (10 μm) and APV (50 μm; bottom). Black traces are the average of 10 individual traces, which are shown in gray. Inset, Firing pattern of a BA IN exhibiting the light-evoked fast EPSC. C, Fast EPSC evoked in BA INs is blocked by NBQX and APV. (Wilcoxon matched-pairs signed-rank test, p = 0.0039, n = 9). D, Example of a voltage-clamp (−70 mV) trace from a BA IN showing frequency-dependent depression of the fast glutamatergic EPSCs evoked by light trains (5 s) at 1 Hz (left), 10 Hz (middle), and 20 Hz (right). Traces shown are an average of five individual traces. E, Stimulation-frequency-dependent depression of the second and last fast glutamatergic EPSC amplitudes normalized to the first EPSC amplitude for each cell. The depression of the last EPSC increases with higher stimulation frequencies (repeated-measures two-way ANOVA, main effect of light pulse no. p < 0.0001, main effect of stimulation frequency p = 0.0008; light pulse no. × stimulation frequency interaction p < 0.0001; Bonferroni's post hoc comparisons: at 1 Hz stimulation frequency, first vs second light pulse p < 0.0001, first vs last light pulse p < 0.0001; at 10 Hz stimulation frequency, first vs second light pulse p < 0.0001, first vs last light pulse p < 0.0001; at 20 Hz stimulation frequency, first vs second light pulse p < 0.0001, second vs last light pulse p < 0.0001, first vs last light pulse p < 0.0001; last light pulse, 20 Hz vs 10 Hz p = 0.0027, 10 Hz vs 1 Hz p = 0.0013, 20 Hz vs 1 Hz p < 0.0001; n = 7). F, Maximum intensity projection (z-stack: 5.18 μm) showing sparse expression of VGLUT3 in 5-HT neuron axons (YFP+) in the BA. Arrows highlight YFP+/VGLUT3+ boutons. G, Magnification of the area framed in F. Single optical section (0.43 μm thickness) showing two YFP+ boutons immunopositive for VGLUT3. Data are expressed as means ± SEM. *p < 0.05; **p < 0.01; ***p < 0.0001.
Figure 2. 5-HT neurons release glutamate onto BA INs. A, Representative biocytin-filled BA IN showing a dense local axon (left) and a spiny dendrite (right). B, Example of a voltage-clamp (−70 mV) trace from a BA IN showing a fast EPSC evoked by a single light pulse (3 ms) activation of DRN axons (top); the fast EPSC is blocked by AMPA/kainate and the NMDA receptor antagonists NBQX (10 μm) and APV (50 μm; bottom). Black traces are the average of 10 individual traces, which are shown in gray. Inset, Firing pattern of a BA IN exhibiting the light-evoked fast EPSC. C, Fast EPSC evoked in BA INs is blocked by NBQX and APV. (Wilcoxon matched-pairs signed-rank test, p = 0.0039, n = 9). D, Example of a voltage-clamp (−70 mV) trace from a BA IN showing frequency-dependent depression of the fast glutamatergic EPSCs evoked by light trains (5 s) at 1 Hz (left), 10 Hz (middle), and 20 Hz (right). Traces shown are an average of five individual traces. E, Stimulation-frequency-dependent depression of the second and last fast glutamatergic EPSC amplitudes normalized to the first EPSC amplitude for each cell. The depression of the last EPSC increases with higher stimulation frequencies (repeated-measures two-way ANOVA, main effect of light pulse no. p < 0.0001, main effect of stimulation frequency p = 0.0008; light pulse no. × stimulation frequency interaction p < 0.0001; Bonferroni's post hoc comparisons: at 1 Hz stimulation frequency, first vs second light pulse p < 0.0001, first vs last light pulse p < 0.0001; at 10 Hz stimulation frequency, first vs second light pulse p < 0.0001, first vs last light pulse p < 0.0001; at 20 Hz stimulation frequency, first vs second light pulse p < 0.0001, second vs last light pulse p < 0.0001, first vs last light pulse p < 0.0001; last light pulse, 20 Hz vs 10 Hz p = 0.0027, 10 Hz vs 1 Hz p = 0.0013, 20 Hz vs 1 Hz p < 0.0001; n = 7). F, Maximum intensity projection (z-stack: 5.18 μm) showing sparse expression of VGLUT3 in 5-HT neuron axons (YFP+) in the BA. Arrows highlight YFP+/VGLUT3+ boutons. G, Magnification of the area framed in F. Single optical section (0.43 μm thickness) showing two YFP+ boutons immunopositive for VGLUT3. Data are expressed as means ± SEM. *p < 0.05; **p < 0.01; ***p < 0.0001.CC BY · PubMed Central
Figure 3. 5-HT neurons modulate BA INs bidirectionally via 5-HT release. A, Example of a voltage-clamp (−70 mV) trace from a BA IN showing a slow EPSC evoked by 30 s optical stimulation at 20 Hz of DRN axons. The slow EPSC is blocked by the 5-HT2A receptor antagonist MDL 100907 (150 nm). Recordings were performed in the presence of the generic glutamate receptor blocker kynurenic acid (3 mm) to isolate slow responses. Inset, Example of a firing pattern of a BA IN exhibiting the light-evoked slow EPSC. B, Slow EPSC evoked in BA INs is blocked by the 5-HT2A receptor antagonist MDL 100907 (1 μm; paired t test, p = 0.0018, n = 9). C, Slow EPSC amplitude is increased significantly by higher stimulation frequencies. Slow EPSC amplitudes are normalized to the amplitude evoked at 20 Hz stimulation frequency for each cell (one-way ANOVA, p < 0.0001; Bonferroni's post hoc comparisons, 1 Hz vs 10 Hz p = 0.0368, 10 Hz vs 20 Hz p = 0.0139, 1 Hz vs 20 Hz p = 0.0020; n = 6). D, Example of a voltage-clamp (−70 mV) trace from a BA IN showing a slow IPSC evoked by 30 s optical stimulation at 20 Hz of DRN axons. The slow IPSC is blocked by the 5-HT1A receptor antagonist WAY 100635 (1 μm). Recordings were performed in the presence of the generic glutamate receptor blocker kynurenic acid (3 mm) to isolate slow responses. Inset, Example of a firing pattern of a BA IN exhibiting the light-evoked slow IPSC. E, Slow IPSC evoked in BA INs is blocked by the 5-HT1A receptor antagonist WAY 100635 (1 μm; paired t test, p = 0.0391, n = 7). F, Slow IPSC amplitude is significantly increased by higher stimulation frequencies. Slow IPSC amplitudes are normalized to the amplitude evoked at 20 Hz stimulation frequency for each cell (one-way ANOVA, p = 0.0043; Bonferroni's post hoc comparisons, 1 Hz vs 20 Hz p = 0.0274; n = 5). G, Representative voltage-clamp (−70 mV) traces from a BA IN showing simultaneous fast EPSCs and a slow IPSC evoked by optical stimulation at 20 Hz (left), at short (first 10 light pulses, top traces) and long (entire 20 Hz train, bottom traces) time scales. The fast EPSCs are blocked by AMPA/kainate and NMDA receptor antagonists NBQX (10 μm) and APV (50 μm; middle). Both the fast EPSCs and the slow IPSC are blocked by a combination of NBQX, APV, and WAY 100635 (right). H, Light-evoked fast EPSCs and slow IPSC cooccurring in BA INs (left, n = 3) are blocked by glutamate receptor (middle, n = 2) and 5-HT1A antagonists (right, n = 2), respectively. Data are expressed as means ± SEM. *p < 0.05; **p < 0.01.
Figure 3. 5-HT neurons modulate BA INs bidirectionally via 5-HT release. A, Example of a voltage-clamp (−70 mV) trace from a BA IN showing a slow EPSC evoked by 30 s optical stimulation at 20 Hz of DRN axons. The slow EPSC is blocked by the 5-HT2A receptor antagonist MDL 100907 (150 nm). Recordings were performed in the presence of the generic glutamate receptor blocker kynurenic acid (3 mm) to isolate slow responses. Inset, Example of a firing pattern of a BA IN exhibiting the light-evoked slow EPSC. B, Slow EPSC evoked in BA INs is blocked by the 5-HT2A receptor antagonist MDL 100907 (1 μm; paired t test, p = 0.0018, n = 9). C, Slow EPSC amplitude is increased significantly by higher stimulation frequencies. Slow EPSC amplitudes are normalized to the amplitude evoked at 20 Hz stimulation frequency for each cell (one-way ANOVA, p < 0.0001; Bonferroni's post hoc comparisons, 1 Hz vs 10 Hz p = 0.0368, 10 Hz vs 20 Hz p = 0.0139, 1 Hz vs 20 Hz p = 0.0020; n = 6). D, Example of a voltage-clamp (−70 mV) trace from a BA IN showing a slow IPSC evoked by 30 s optical stimulation at 20 Hz of DRN axons. The slow IPSC is blocked by the 5-HT1A receptor antagonist WAY 100635 (1 μm). Recordings were performed in the presence of the generic glutamate receptor blocker kynurenic acid (3 mm) to isolate slow responses. Inset, Example of a firing pattern of a BA IN exhibiting the light-evoked slow IPSC. E, Slow IPSC evoked in BA INs is blocked by the 5-HT1A receptor antagonist WAY 100635 (1 μm; paired t test, p = 0.0391, n = 7). F, Slow IPSC amplitude is significantly increased by higher stimulation frequencies. Slow IPSC amplitudes are normalized to the amplitude evoked at 20 Hz stimulation frequency for each cell (one-way ANOVA, p = 0.0043; Bonferroni's post hoc comparisons, 1 Hz vs 20 Hz p = 0.0274; n = 5). G, Representative voltage-clamp (−70 mV) traces from a BA IN showing simultaneous fast EPSCs and a slow IPSC evoked by optical stimulation at 20 Hz (left), at short (first 10 light pulses, top traces) and long (entire 20 Hz train, bottom traces) time scales. The fast EPSCs are blocked by AMPA/kainate and NMDA receptor antagonists NBQX (10 μm) and APV (50 μm; middle). Both the fast EPSCs and the slow IPSC are blocked by a combination of NBQX, APV, and WAY 100635 (right). H, Light-evoked fast EPSCs and slow IPSC cooccurring in BA INs (left, n = 3) are blocked by glutamate receptor (middle, n = 2) and 5-HT1A antagonists (right, n = 2), respectively. Data are expressed as means ± SEM. *p < 0.05; **p < 0.01.CC BY · PubMed Central
Figure 4. 5-HT neurons differentially modulate BA INs. A, Relative distribution (as a percentage) of response types in BA INs evoked by either single pulses (fast EPSC) or trains (slow EPSC and IPSC) of optical stimulation of DRN axons (n = 59). B, No correlation between amplitudes of the fast EPSC and slow EPSC responses evoked in BA INs (Pearson correlation coefficient, n = 59; left). Positive correlation between amplitudes of the fast EPSC and slow IPSC responses evoked in BA INs (Pearson correlation coefficient, n = 59; right). C, Example of voltage-clamp (−70 mV) traces showing a larger fast EPSC evoked in a fast-spiking (left) than in a non-fast-spiking (right) BA IN by a single light pulse (3 ms) activation of DRN axons. Inset, Example of firing patterns of a fast-spiking (left) and a non-fast-spiking (right) BA IN. D, Mean voltage-clamp (−70 mV) traces from fast-spiking and non-fast-spiking BA INs showing similar amplitudes of the slow EPSC but different amplitudes of the slow IPSC evoked by 30 s optical stimulation at 20 Hz of DRN axons (fast-spiking n = 21, non-fast-spiking n = 36). E, Amplitudes of the fast EPSC and the slow IPSC, but not the slow EPSC, are greater in fast-spiking than in non-fast-spiking BA INs (fast EPSC, Mann–Whitney test, p = 0.0114; slow EPSC, Mann–Whitney test, p = 0.4922, fast-spiking n = 21, non-fast-spiking n = 36; slow IPSC, Mann–Whitney test, p = 0.0090; fast-spiking n = 21, non-fast-spiking n = 36). Data are expressed as means ± SEM. *p < 0.05; **p < 0.01.
Figure 4. 5-HT neurons differentially modulate BA INs. A, Relative distribution (as a percentage) of response types in BA INs evoked by either single pulses (fast EPSC) or trains (slow EPSC and IPSC) of optical stimulation of DRN axons (n = 59). B, No correlation between amplitudes of the fast EPSC and slow EPSC responses evoked in BA INs (Pearson correlation coefficient, n = 59; left). Positive correlation between amplitudes of the fast EPSC and slow IPSC responses evoked in BA INs (Pearson correlation coefficient, n = 59; right). C, Example of voltage-clamp (−70 mV) traces showing a larger fast EPSC evoked in a fast-spiking (left) than in a non-fast-spiking (right) BA IN by a single light pulse (3 ms) activation of DRN axons. Inset, Example of firing patterns of a fast-spiking (left) and a non-fast-spiking (right) BA IN. D, Mean voltage-clamp (−70 mV) traces from fast-spiking and non-fast-spiking BA INs showing similar amplitudes of the slow EPSC but different amplitudes of the slow IPSC evoked by 30 s optical stimulation at 20 Hz of DRN axons (fast-spiking n = 21, non-fast-spiking n = 36). E, Amplitudes of the fast EPSC and the slow IPSC, but not the slow EPSC, are greater in fast-spiking than in non-fast-spiking BA INs (fast EPSC, Mann–Whitney test, p = 0.0114; slow EPSC, Mann–Whitney test, p = 0.4922, fast-spiking n = 21, non-fast-spiking n = 36; slow IPSC, Mann–Whitney test, p = 0.0090; fast-spiking n = 21, non-fast-spiking n = 36). Data are expressed as means ± SEM. *p < 0.05; **p < 0.01.CC BY · PubMed Central
Figure 5. 5-HT neurons inhibit BA PNs via 5-HT1A receptors and enhanced GABA release. A, Representative biocytin-filled PN showing a sparse axon with long-projecting branches (left) and spiny dendrites (right). B, Example of a voltage-clamp (−50 mV) trace from a BA PN showing a slow IPSC evoked by 30 s optical stimulation at 20 Hz of DRN axons, blocked by the 5-HT1A receptor antagonist WAY 100635 (1 μm). Inset, Stereotypical firing pattern of a BA PN exhibiting the light-evoked slow IPSC. C, Slow IPSC evoked in BA PNs is blocked by the 5-HT1A receptor antagonist WAY 100635 (1 μm; Wilcoxon matched-pairs signed-rank test, p = 0.0313, n = 7), but not by the GABAA and GABAB receptor antagonists SR 95531 (50 μm) and CGP54626 (5 μm; Wilcoxon matched-pairs signed-rank test, p = 0.6250, n = 5). D, Relative distribution (as a percentage) of response types in BA PNs evoked by optical stimulation of 5-HT axons (n = 13). E, Example of a voltage-clamp (−50 mV) trace from a BA PN showing an increase in sIPSC frequency during 20 Hz optical stimulation of DRN axons (top). Mean PSTH showing an increase in sIPSC frequency in BA PNs during 30 s optical stimulation at 20 Hz of DRN axons (n = 14; bottom) is shown. F, Increase in sIPSC frequency in BA PNs is blocked by the GABAA and GABAB receptor antagonists SR 95531 (50 μm) and CGP54626 (5 μm), but not the 5-HT1A antagonist WAY100635 (1 μm; control, Wilcoxon matched-pairs signed-rank test, p = 0.0254, n = 13; WAY 100635, paired t test, p = 0.0609, n = 7; SR 95531 and CGP54626, Wilcoxon matched-pairs signed-rank test, p > 0.9999, n = 5). G, Top, Example of a current-clamp trace from a BA PN. Rheobase-positive current was constantly injected to evoke baseline firing. Thirty seconds of optical stimulation at 20 Hz of 5-HT axons reduced the firing rate. Bottom, Firing rate of BA PNs is significantly reduced by optical stimulation at 20 Hz of 5-HT axons (repeated-measures one-way ANOVA, main effect of stimulation time p = 0.0371; Dunnett's multiple-comparisons test, baseline vs 5 s p = 0.0261, baseline vs 10 s p = 0.0456, baseline vs 15 s p = 0.0410, n = 8). Data are expressed as means ± SEM. *p < 0.05.
Figure 5. 5-HT neurons inhibit BA PNs via 5-HT1A receptors and enhanced GABA release. A, Representative biocytin-filled PN showing a sparse axon with long-projecting branches (left) and spiny dendrites (right). B, Example of a voltage-clamp (−50 mV) trace from a BA PN showing a slow IPSC evoked by 30 s optical stimulation at 20 Hz of DRN axons, blocked by the 5-HT1A receptor antagonist WAY 100635 (1 μm). Inset, Stereotypical firing pattern of a BA PN exhibiting the light-evoked slow IPSC. C, Slow IPSC evoked in BA PNs is blocked by the 5-HT1A receptor antagonist WAY 100635 (1 μm; Wilcoxon matched-pairs signed-rank test, p = 0.0313, n = 7), but not by the GABAA and GABAB receptor antagonists SR 95531 (50 μm) and CGP54626 (5 μm; Wilcoxon matched-pairs signed-rank test, p = 0.6250, n = 5). D, Relative distribution (as a percentage) of response types in BA PNs evoked by optical stimulation of 5-HT axons (n = 13). E, Example of a voltage-clamp (−50 mV) trace from a BA PN showing an increase in sIPSC frequency during 20 Hz optical stimulation of DRN axons (top). Mean PSTH showing an increase in sIPSC frequency in BA PNs during 30 s optical stimulation at 20 Hz of DRN axons (n = 14; bottom) is shown. F, Increase in sIPSC frequency in BA PNs is blocked by the GABAA and GABAB receptor antagonists SR 95531 (50 μm) and CGP54626 (5 μm), but not the 5-HT1A antagonist WAY100635 (1 μm; control, Wilcoxon matched-pairs signed-rank test, p = 0.0254, n = 13; WAY 100635, paired t test, p = 0.0609, n = 7; SR 95531 and CGP54626, Wilcoxon matched-pairs signed-rank test, p > 0.9999, n = 5). G, Top, Example of a current-clamp trace from a BA PN. Rheobase-positive current was constantly injected to evoke baseline firing. Thirty seconds of optical stimulation at 20 Hz of 5-HT axons reduced the firing rate. Bottom, Firing rate of BA PNs is significantly reduced by optical stimulation at 20 Hz of 5-HT axons (repeated-measures one-way ANOVA, main effect of stimulation time p = 0.0371; Dunnett's multiple-comparisons test, baseline vs 5 s p = 0.0261, baseline vs 10 s p = 0.0456, baseline vs 15 s p = 0.0410, n = 8). Data are expressed as means ± SEM. *p < 0.05.CC BY · PubMed Central

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Metadata

Authors
Sengupta, A., Bocchio, M., Bannerman, D. M., Sharp, T., & Capogna, M.
Affiliations
  • University of Oxford (GB)
  • Aarhus University (DK)
Corresponding author
  • Sharp, Trevor
  • Capogna, Marco
ORCID
Venue
The Journal of Neuroscience
Publisher
Society for Neuroscience
Published
2017-01-13
Volume
37
Issue
7
Pages
1785-1796
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
DOI
10.1523/jneurosci.2238-16.2016
PMC
PMC5320609
OpenAlex
W2573649328
Cited by
136
References
52
Citations by year
2026: 15 · 2025: 9 · 2024: 18 · 2023: 13 · 2022: 9 · 2021: 19 · 2020: 21 · 2019: 18 · 2018: 11 · 2017: 3
FWCI
7.10
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Neuroscience (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Durham Research Online (Durham University) (submittedVersion, cc-by)
  • Scopus (Elsevier) (submittedVersion)
  • Newcastle University ePrints (Newcastle Univesity) (cc-by)
Funders
  • Wellcome Trust
  • University of Oxford
  • National Institutes of Health
  • Medical Research Council
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 › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
serotonin, glutamate co-release, amygdala, basal amygdala, dorsal raphe nucleus, 5-HT1A receptor, 5-HT2A receptor, interneurons, principal neurons, emotion regulation, mood disorders, GABA release, optogenetics, channelrhodopsin, ionotropic glutamate receptors, fast-spiking interneurons
MeSH terms
Channelrhodopsins, Amygdala, Animals, Animals, Newborn, Female, Luminescent Proteins, Male, Mice, Inbred C57BL, Mice, Transgenic, Nerve Net, Synaptic Transmission, Neurons, Piperazines, Pyridines, Receptors, Serotonin, Serotonin, Serotonin Antagonists, Excitatory Amino Acid Agents, Glutamic Acid, GABA Antagonists, Serotonin Plasma Membrane Transport Proteins, Mice

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