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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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Differential Firing Frequencies of PNs and INs during Theta Epochs(A) In vivo single unit recording from a representative PN of the BA during SWA and theta oscillations recorded from CA1 HPC and TeA cortex (ctx). This cell became silent at the onset of theta oscillations. Insets show 2 s of CA1 LFP trace band-pass filtered between 2 and 3 Hz (SWA, left) and 3 and 6 Hz (theta oscillations, right).(B) Juxtacellularly labeled PN displaying immunoreactivity for CaMKIIα.(C) PNs fired at higher frequencies during cortical and hippocampal SWA (0.52 ± 0.08 Hz) and at significantly lower frequencies during theta oscillations (0.04 ± 0.02 Hz, ∗∗∗∗p < 0.0001 n = 16).(D) In vivo single unit recording from an IN of the BA during SWA and theta oscillations recorded from CA1 HPC and TeA. The firing frequency increased during theta oscillations. Insets: 2 s of CA1 LFP trace band-pass filtered between 2 and 3 Hz (SWA, left) and 3 and 6 Hz (theta oscillations, right).(E) Juxtacellularly labeled GABAergic IN displaying axonal immunoreactivity for VGAT.(F) INs fired at lower frequencies during cortical and hippocampal SWA (5.42 ± 1.35 Hz) and at significantly higher frequencies during theta oscillations (8.35 ± 1.48 Hz, ∗p < 0.05, n = 20). Scale bars: (B), 20 μm; (E), 10 μm. Data are presented as means ± SEM.
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fig1: Differential Firing Frequencies of PNs and INs during Theta Epochs(A) In vivo single unit recording from a representative PN of the BA during SWA and theta oscillations recorded from CA1 HPC and TeA cortex (ctx). This cell became silent at the onset of theta oscillations. Insets show 2 s of CA1 LFP trace band-pass filtered between 2 and 3 Hz (SWA, left) and 3 and 6 Hz (theta oscillations, right).(B) Juxtacellularly labeled PN displaying immunoreactivity for CaMKIIα.(C) PNs fired at higher frequencies during cortical and hippocampal SWA (0.52 ± 0.08 Hz) and at significantly lower frequencies during theta oscillations (0.04 ± 0.02 Hz, ∗∗∗∗p < 0.0001 n = 16).(D) In vivo single unit recording from an IN of the BA during SWA and theta oscillations recorded from CA1 HPC and TeA. The firing frequency increased during theta oscillations. Insets: 2 s of CA1 LFP trace band-pass filtered between 2 and 3 Hz (SWA, left) and 3 and 6 Hz (theta oscillations, right).(E) Juxtacellularly labeled GABAergic IN displaying axonal immunoreactivity for VGAT.(F) INs fired at lower frequencies during cortical and hippocampal SWA (5.42 ± 1.35 Hz) and at significantly higher frequencies during theta oscillations (8.35 ± 1.48 Hz, ∗p < 0.05, n = 20). Scale bars: (B), 20 μm; (E), 10 μm. Data are presented as means ± SEM.

Mentions: First, we set out to investigate the activity of PNs and GABAergic INs of the BA when theta oscillations occur in areas interconnected with the amygdala. We recorded the firing of single neurons of the BA and the local field potential (LFP) in CA1 and/or Temporal associative cortex (TeA), two structures projecting to the BLA, in urethane-anesthetized mice. In the BA, PNs (n = 27) and INs (n = 25) could be separated on the basis of their spike waveforms and firing regularity (Figures S1A–S1C; Experimental Procedures), consistent with previous observations (Bienvenu et al., 2012). Immunoreactivity for CaMKIIα (14/14) and VGAT (10/10) was confirmed for a subset of PNs and INs juxtacellularly labeled after their recording (Figures 1B and 1E, respectively). The firing rates of the recorded neurons were cell type specific and brain state dependent, consistent with previous data obtained in awake cats (Paré and Gaudreau, 1996). Specifically, BA PNs fired at higher frequencies during cortical and hippocampal slow wave activity (SWA) (0.52 ± 0.08 Hz) and at significantly lower frequencies during theta oscillations (0.04 ± 0.02 Hz, p < 0.0001, n = 16; Figures 1A and 1C). In contrast, INs fired at lower rates during cortical and hippocampal SWA (5.42 ± 1.35 Hz) and at significantly higher rates during theta oscillations (8.35 ± 1.48 Hz, p < 0.05, n = 20; Figures 1D and 1F). Although most of the INs (16/20) increased their firing rates during theta episodes, a few (4/20) showed a reduction. These results suggest that the firing of BA PNs might be more tightly controlled by GABAergic INs during theta epochs compared to slow wave states.


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)

Differential Firing Frequencies of PNs and INs during Theta Epochs(A) In vivo single unit recording from a representative PN of the BA during SWA and theta oscillations recorded from CA1 HPC and TeA cortex (ctx). This cell became silent at the onset of theta oscillations. Insets show 2 s of CA1 LFP trace band-pass filtered between 2 and 3 Hz (SWA, left) and 3 and 6 Hz (theta oscillations, right).(B) Juxtacellularly labeled PN displaying immunoreactivity for CaMKIIα.(C) PNs fired at higher frequencies during cortical and hippocampal SWA (0.52 ± 0.08 Hz) and at significantly lower frequencies during theta oscillations (0.04 ± 0.02 Hz, ∗∗∗∗p < 0.0001 n = 16).(D) In vivo single unit recording from an IN of the BA during SWA and theta oscillations recorded from CA1 HPC and TeA. The firing frequency increased during theta oscillations. Insets: 2 s of CA1 LFP trace band-pass filtered between 2 and 3 Hz (SWA, left) and 3 and 6 Hz (theta oscillations, right).(E) Juxtacellularly labeled GABAergic IN displaying axonal immunoreactivity for VGAT.(F) INs fired at lower frequencies during cortical and hippocampal SWA (5.42 ± 1.35 Hz) and at significantly higher frequencies during theta oscillations (8.35 ± 1.48 Hz, ∗p < 0.05, n = 20). Scale bars: (B), 20 μm; (E), 10 μm. Data are presented as means ± SEM.
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fig1: Differential Firing Frequencies of PNs and INs during Theta Epochs(A) In vivo single unit recording from a representative PN of the BA during SWA and theta oscillations recorded from CA1 HPC and TeA cortex (ctx). This cell became silent at the onset of theta oscillations. Insets show 2 s of CA1 LFP trace band-pass filtered between 2 and 3 Hz (SWA, left) and 3 and 6 Hz (theta oscillations, right).(B) Juxtacellularly labeled PN displaying immunoreactivity for CaMKIIα.(C) PNs fired at higher frequencies during cortical and hippocampal SWA (0.52 ± 0.08 Hz) and at significantly lower frequencies during theta oscillations (0.04 ± 0.02 Hz, ∗∗∗∗p < 0.0001 n = 16).(D) In vivo single unit recording from an IN of the BA during SWA and theta oscillations recorded from CA1 HPC and TeA. The firing frequency increased during theta oscillations. Insets: 2 s of CA1 LFP trace band-pass filtered between 2 and 3 Hz (SWA, left) and 3 and 6 Hz (theta oscillations, right).(E) Juxtacellularly labeled GABAergic IN displaying axonal immunoreactivity for VGAT.(F) INs fired at lower frequencies during cortical and hippocampal SWA (5.42 ± 1.35 Hz) and at significantly higher frequencies during theta oscillations (8.35 ± 1.48 Hz, ∗p < 0.05, n = 20). Scale bars: (B), 20 μm; (E), 10 μm. Data are presented as means ± SEM.
Mentions: First, we set out to investigate the activity of PNs and GABAergic INs of the BA when theta oscillations occur in areas interconnected with the amygdala. We recorded the firing of single neurons of the BA and the local field potential (LFP) in CA1 and/or Temporal associative cortex (TeA), two structures projecting to the BLA, in urethane-anesthetized mice. In the BA, PNs (n = 27) and INs (n = 25) could be separated on the basis of their spike waveforms and firing regularity (Figures S1A–S1C; Experimental Procedures), consistent with previous observations (Bienvenu et al., 2012). Immunoreactivity for CaMKIIα (14/14) and VGAT (10/10) was confirmed for a subset of PNs and INs juxtacellularly labeled after their recording (Figures 1B and 1E, respectively). The firing rates of the recorded neurons were cell type specific and brain state dependent, consistent with previous data obtained in awake cats (Paré and Gaudreau, 1996). Specifically, BA PNs fired at higher frequencies during cortical and hippocampal slow wave activity (SWA) (0.52 ± 0.08 Hz) and at significantly lower frequencies during theta oscillations (0.04 ± 0.02 Hz, p < 0.0001, n = 16; Figures 1A and 1C). In contrast, INs fired at lower rates during cortical and hippocampal SWA (5.42 ± 1.35 Hz) and at significantly higher rates during theta oscillations (8.35 ± 1.48 Hz, p < 0.05, n = 20; Figures 1D and 1F). Although most of the INs (16/20) increased their firing rates during theta episodes, a few (4/20) showed a reduction. These results suggest that the firing of BA PNs might be more tightly controlled by GABAergic INs during theta epochs compared to slow wave states.

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