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Hippocampal Theta Input to the Amygdala Shapes Feedforward Inhibition to Gate Heterosynaptic Plasticity.

Bazelot M, Bocchio M, Kasugai Y, Fischer D, Dodson PD, Ferraguti F, Capogna M - Neuron (2015)

Bottom Line: These effects are mediated by GABAB receptors and change in the Cl(-) driving force.Hence, feedforward inhibition, known to enforce temporal fidelity of excitatory inputs, dominates hippocampus-amygdala interactions to gate heterosynaptic plasticity.VIDEO ABSTRACT.

View Article: PubMed Central - PubMed

Affiliation: MRC Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford OX1 3TH, UK.

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Optical TBS of Hippocampal Axons Inhibits PNs and Triggers Firing in INs of the BA In Vivo(A) Expression of ChR2/YFP in ventral/intermediate CA1.(B) Light micrograph showing ChR2/YFP-positive axons in the amygdaloid complex. BA and BM nuclei showed densest innervation, whereas only few fibers were detectable in the LA and CeA.(C) Scheme showing experimental configuration: single unit recordings and juxtacellular labeling from neurons of the BA and photostimulation of vCA1 pyramidal cells axons through a fiber optic implanted above the BA.(D) Representative PN was inhibited by optical TBS. Superimposed traces (n = 8, top), singularly represented in rasterplot (middle), and peri-stimulus time histogram (PSTH) (50-ms bins, bottom). Note spikelet-like events during TBS are stimulation artifacts.(E) Normalized firing rates (50-ms bins) of BA PNs in response to optical TBS of hippocampal axons (baseline versus TBS, p < 0.01, n = 10).(F) Representative IN was activated by optical TBS. Superimposed traces (n = 8, top), singularly represented in raster plot (middle) and PSTH (50-ms bins, bottom). Inset: TBS evokes action potentials primarily following the first pulse of each train.(G) Normalized firing rates (50 ms bins) of BA INs in response to optical TBS of hippocampal axons (baseline versus TBS, p < 0.05, n = 7). Scale bars: (A), 350 μm; (B), 250 μm. Data are presented as means ± SEM.
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fig2: Optical TBS of Hippocampal Axons Inhibits PNs and Triggers Firing in INs of the BA In Vivo(A) Expression of ChR2/YFP in ventral/intermediate CA1.(B) Light micrograph showing ChR2/YFP-positive axons in the amygdaloid complex. BA and BM nuclei showed densest innervation, whereas only few fibers were detectable in the LA and CeA.(C) Scheme showing experimental configuration: single unit recordings and juxtacellular labeling from neurons of the BA and photostimulation of vCA1 pyramidal cells axons through a fiber optic implanted above the BA.(D) Representative PN was inhibited by optical TBS. Superimposed traces (n = 8, top), singularly represented in rasterplot (middle), and peri-stimulus time histogram (PSTH) (50-ms bins, bottom). Note spikelet-like events during TBS are stimulation artifacts.(E) Normalized firing rates (50-ms bins) of BA PNs in response to optical TBS of hippocampal axons (baseline versus TBS, p < 0.01, n = 10).(F) Representative IN was activated by optical TBS. Superimposed traces (n = 8, top), singularly represented in raster plot (middle) and PSTH (50-ms bins, bottom). Inset: TBS evokes action potentials primarily following the first pulse of each train.(G) Normalized firing rates (50 ms bins) of BA INs in response to optical TBS of hippocampal axons (baseline versus TBS, p < 0.05, n = 7). Scale bars: (A), 350 μm; (B), 250 μm. Data are presented as means ± SEM.

Mentions: We then sought to understand the influence of a theta frequency input from vCA1 pyramidal cells on the firing of BA neurons. To this aim, we transfected pyramidal cells of vCA1 with the ultrafast (E123T/T159C) Channelrhodopsin-2 (ChR2) (Figures 2A and S2), which more efficiently evokes action potentials at high frequency stimulation compared to the common H134R variant (Berndt et al., 2011). Three to four weeks after viral injection, ChR2+ axons densely innervated the BA and BM, together with the external and intermediate capsules surrounding the BLA, whereas only sparse fibers were observed in the LA (Figure 2B). This pattern of innervation was consistent with previous tracing studies in rodents (Kishi et al., 2006; Müller et al., 2012).


Hippocampal Theta Input to the Amygdala Shapes Feedforward Inhibition to Gate Heterosynaptic Plasticity.

Bazelot M, Bocchio M, Kasugai Y, Fischer D, Dodson PD, Ferraguti F, Capogna M - Neuron (2015)

Optical TBS of Hippocampal Axons Inhibits PNs and Triggers Firing in INs of the BA In Vivo(A) Expression of ChR2/YFP in ventral/intermediate CA1.(B) Light micrograph showing ChR2/YFP-positive axons in the amygdaloid complex. BA and BM nuclei showed densest innervation, whereas only few fibers were detectable in the LA and CeA.(C) Scheme showing experimental configuration: single unit recordings and juxtacellular labeling from neurons of the BA and photostimulation of vCA1 pyramidal cells axons through a fiber optic implanted above the BA.(D) Representative PN was inhibited by optical TBS. Superimposed traces (n = 8, top), singularly represented in rasterplot (middle), and peri-stimulus time histogram (PSTH) (50-ms bins, bottom). Note spikelet-like events during TBS are stimulation artifacts.(E) Normalized firing rates (50-ms bins) of BA PNs in response to optical TBS of hippocampal axons (baseline versus TBS, p < 0.01, n = 10).(F) Representative IN was activated by optical TBS. Superimposed traces (n = 8, top), singularly represented in raster plot (middle) and PSTH (50-ms bins, bottom). Inset: TBS evokes action potentials primarily following the first pulse of each train.(G) Normalized firing rates (50 ms bins) of BA INs in response to optical TBS of hippocampal axons (baseline versus TBS, p < 0.05, n = 7). Scale bars: (A), 350 μm; (B), 250 μm. Data are presented as means ± SEM.
© Copyright Policy - CC BY
Related In: Results  -  Collection

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fig2: Optical TBS of Hippocampal Axons Inhibits PNs and Triggers Firing in INs of the BA In Vivo(A) Expression of ChR2/YFP in ventral/intermediate CA1.(B) Light micrograph showing ChR2/YFP-positive axons in the amygdaloid complex. BA and BM nuclei showed densest innervation, whereas only few fibers were detectable in the LA and CeA.(C) Scheme showing experimental configuration: single unit recordings and juxtacellular labeling from neurons of the BA and photostimulation of vCA1 pyramidal cells axons through a fiber optic implanted above the BA.(D) Representative PN was inhibited by optical TBS. Superimposed traces (n = 8, top), singularly represented in rasterplot (middle), and peri-stimulus time histogram (PSTH) (50-ms bins, bottom). Note spikelet-like events during TBS are stimulation artifacts.(E) Normalized firing rates (50-ms bins) of BA PNs in response to optical TBS of hippocampal axons (baseline versus TBS, p < 0.01, n = 10).(F) Representative IN was activated by optical TBS. Superimposed traces (n = 8, top), singularly represented in raster plot (middle) and PSTH (50-ms bins, bottom). Inset: TBS evokes action potentials primarily following the first pulse of each train.(G) Normalized firing rates (50 ms bins) of BA INs in response to optical TBS of hippocampal axons (baseline versus TBS, p < 0.05, n = 7). Scale bars: (A), 350 μm; (B), 250 μm. Data are presented as means ± SEM.
Mentions: We then sought to understand the influence of a theta frequency input from vCA1 pyramidal cells on the firing of BA neurons. To this aim, we transfected pyramidal cells of vCA1 with the ultrafast (E123T/T159C) Channelrhodopsin-2 (ChR2) (Figures 2A and S2), which more efficiently evokes action potentials at high frequency stimulation compared to the common H134R variant (Berndt et al., 2011). Three to four weeks after viral injection, ChR2+ axons densely innervated the BA and BM, together with the external and intermediate capsules surrounding the BLA, whereas only sparse fibers were observed in the LA (Figure 2B). This pattern of innervation was consistent with previous tracing studies in rodents (Kishi et al., 2006; Müller et al., 2012).

Bottom Line: These effects are mediated by GABAB receptors and change in the Cl(-) driving force.Hence, feedforward inhibition, known to enforce temporal fidelity of excitatory inputs, dominates hippocampus-amygdala interactions to gate heterosynaptic plasticity.VIDEO ABSTRACT.

View Article: PubMed Central - PubMed

Affiliation: MRC Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford OX1 3TH, UK.

Show MeSH