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. 2017 Nov 7;21(6):1426-1433.
doi: 10.1016/j.celrep.2017.10.046.

Prefrontal Cortex Drives Distinct Projection Neurons in the Basolateral Amygdala

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Free PMC article

Prefrontal Cortex Drives Distinct Projection Neurons in the Basolateral Amygdala

Laura M McGarry et al. Cell Rep. .
Free PMC article

Abstract

The prefrontal cortex (PFC) regulates emotional behavior via top-down control of the basolateral amygdala (BLA). However, the influence of PFC inputs on the different projection pathways within the BLA remains largely unexplored. Here, we combine whole-cell recordings and optogenetics to study these cell-type specific connections in mouse BLA. We characterize PFC inputs onto three distinct populations of BLA neurons that project to the PFC, ventral hippocampus, or nucleus accumbens. We find that PFC-evoked synaptic responses are strongest at amygdala-cortical and amygdala-hippocampal neurons and much weaker at amygdala-striatal neurons. We assess the mechanisms for this targeting and conclude that it reflects fewer connections onto amygdala-striatal neurons. Given the similar intrinsic properties of these cells, this connectivity allows the PFC to preferentially activate amygdala-cortical and amygdala-hippocampal neurons. Together, our findings reveal how PFC inputs to the BLA selectively drive feedback projections to the PFC and feedforward projections to the hippocampus.

Keywords: basolateral amygdala; circuit; prefrontal cortex; projection neuron; synapse.

Conflict of interest statement

The authors have no financial conflicts of interest.

Figures

Figure 1
Figure 1. PFC axons overlap with multiple projection neurons in the BLA
A) Left, Injections into the PL PFC to label axons and AC neurons in the BLA. Axes apply to all images. Right, Injection of AAV-mCherry (red) and CTB-488 (green) in the PL PFC (top left) labels PFC axons (red) and AC neurons (green) in the BLA (bottom middle), with expanded view (far right). DAPI staining in grey. B) Average PFC-evoked AMPA-R EPSC at AC neurons before (green) and after (black) wash-in of NBQX. Arrowhead indicates time of light pulse. C) Left, Dual injections of CTB into the PFC and NAc. Right, Labeling of AC (green) and AS (purple) neurons in the BLA. D) Left, Dual injections of CTB into the PFC and vHPC. Right, Labeling of AC (green) and AH (orange) neurons in the BLA. E) Left, Average PFC-evoked AMPA-R EPSC at pairs of AS neurons located in the medial (purple) and lateral (black) BLA. Right, Summary of EPSC amplitudes at AS neurons located in medial (M) or lateral (L) BLA. F) Left, Average PFC-evoked AMPA-R EPSC at AH neurons located in the medial (orange) and lateral (black) BLA. Right, Summary of EPSC amplitudes at AH neurons located in medial (M) or lateral (L) BLA.
Figure 2
Figure 2. PFC inputs are strongest onto AC and AH neurons
A) Dendritic reconstructions of AC (green), AS (purple) and AH (orange) neurons located in the medial BLA. B) Summary of dendritic Sholl analysis for the five types of neurons. C) Average PFC-evoked AMPA-R and NMDA-R EPSCs at pairs of neighboring AC (green) and AS (purple) neurons. D) Summary of AS/AC amplitude ratio (left), and AMPA/NMDA ratio (right) for PFC-evoked EPSCs at AC and AS neurons. E–F) Similar to (C–D) for AC (green) and AH (orange) neurons. * = p < 0.05.
Figure 3
Figure 3. Differential synaptic strength reflects number of connections
A) Top, PFC-evoked qEPSCs recorded in the presences of strontium (Sr2+) at AS (purple), AC (green) and AH (orange) neurons, where asterisks indicate detected qEPSCs. Arrowheads indicate time of light pulses. Bottom, Histograms for example cells showing detected post-stimulation qEPSCs across all trials. B) Summary of PFC-evoked qEPSC ∆ frequency (left) and amplitude (right) at AS, AC and AH neurons. Lines indicate pairs of recorded neurons. C) Summary of AS/AC (left) and AH/AC (right) ratios for PFC-evoked qEPSC ∆ frequency and amplitude. D) Left, Average PFC-evoked AMPA-R EPSCs evoked by trains of inputs (5 pulses at 20 Hz) at AC (green) and AS (purple) neurons. Right, Summary of paired pulse ratio (PPR = EPSCN/EPSC1) during trains. E) Similar to (D) for AC (green) and AH (orange) neurons. * = p < 0.05.
Figure 4
Figure 4. PFC inputs preferentially drive firing of AC and AH neurons
A) AP firing and hyperpolarization of AC (green), AS (purple) and AH (orange) neurons located in the medial BLA in response to +200 pA and −50 pA current steps in the presence of synaptic blockers. B) Firing vs current (F–I) curves for the five types of neurons. C) Left, PFC-evoked EPSPs and APs at neighboring AC (green) and AS (purple) neurons. Example traces to light duration of 4 ms shown. Arrowhead indicates time of light pulse. Right, Probability of AP firing versus light duration. D) Similar to (C) for AC (green) and AH (orange) neurons. E) Left, PFC-evoked EPSPs and APs at neighboring AC (green) and AS (purple) neurons in response to trains (5 pulses at 20 Hz). Example traces to 4 ms light duration shown. Right, Probability of AP firing versus pulse number. F) Similar to (E) for AC (green) and AH (orange) neurons. * = p < 0.05.

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