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Research Articles, Systems/Circuits

Differential Regulation of Prelimbic and Thalamic Transmission to the Basolateral Amygdala by Acetylcholine Receptors

Sarah C. Tryon, Joshua X. Bratsch-Prince, James W. Warren, Grace C. Jones, Alexander J. McDonald and David D. Mott
Journal of Neuroscience 1 February 2023, 43 (5) 722-735; DOI: https://doi.org/10.1523/JNEUROSCI.2545-21.2022
Sarah C. Tryon
Department of Pharmacology, Physiology & Neuroscience, University of South Carolina School of Medicine, Columbia, South Carolina 29208
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Joshua X. Bratsch-Prince
Department of Pharmacology, Physiology & Neuroscience, University of South Carolina School of Medicine, Columbia, South Carolina 29208
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James W. Warren
Department of Pharmacology, Physiology & Neuroscience, University of South Carolina School of Medicine, Columbia, South Carolina 29208
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Grace C. Jones
Department of Pharmacology, Physiology & Neuroscience, University of South Carolina School of Medicine, Columbia, South Carolina 29208
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Alexander J. McDonald
Department of Pharmacology, Physiology & Neuroscience, University of South Carolina School of Medicine, Columbia, South Carolina 29208
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David D. Mott
Department of Pharmacology, Physiology & Neuroscience, University of South Carolina School of Medicine, Columbia, South Carolina 29208
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Abstract

The amygdalar anterior basolateral nucleus (BLa) plays a vital role in emotional behaviors. This region receives dense cholinergic projections from basal forebrain which are critical in regulating neuronal activity in BLa. Cholinergic signaling in BLa has also been shown to modulate afferent glutamatergic inputs to this region. However, these studies, which have used cholinergic agonists or prolonged optogenetic stimulation of cholinergic fibers, may not reflect the effect of physiological acetylcholine release in the BLa. To better understand these effects of acetylcholine, we have used electrophysiology and optogenetics in male and female mouse brain slices to examine cholinergic regulation of afferent BLa input from cortex and midline thalamic nuclei. Phasic ACh release evoked by single pulse stimulation of cholinergic terminals had a biphasic effect on transmission at cortical input, producing rapid nicotinic receptor-mediated facilitation followed by slower mAChR-mediated depression. In contrast, at this same input, sustained ACh elevation through application of the cholinesterase inhibitor physostigmine suppressed glutamatergic transmission through mAChRs only. This suppression was not observed at midline thalamic nuclei inputs to BLa. In agreement with this pathway specificity, the mAChR agonist, muscarine more potently suppressed transmission at inputs from prelimbic cortex than thalamus. Muscarinic inhibition at prelimbic cortex input required presynaptic M4 mAChRs, while at thalamic input it depended on M3 mAChR-mediated stimulation of retrograde endocannabinoid signaling. Muscarinic inhibition at both pathways was frequency-dependent, allowing only high-frequency activity to pass. These findings demonstrate complex cholinergic regulation of afferent input to BLa that is pathway-specific and frequency-dependent.

SIGNIFICANCE STATEMENT Cholinergic modulation of the basolateral amygdala regulates formation of emotional memories, but the underlying mechanisms are not well understood. Here, we show, using mouse brain slices, that ACh differentially regulates afferent transmission to the BLa from cortex and midline thalamic nuclei. Fast, phasic ACh release from a single optical stimulation biphasically regulates glutamatergic transmission at cortical inputs through nicotinic and muscarinic receptors, suggesting that cholinergic neuromodulation can serve precise, computational roles in the BLa. In contrast, sustained ACh elevation regulates cortical input through muscarinic receptors only. This muscarinic regulation is pathway-specific with cortical input inhibited more strongly than midline thalamic nuclei input. Specific targeting of these cholinergic receptors may thus provide a therapeutic strategy to bias amygdalar processing and regulate emotional memory.

  • amygdala
  • cholinergic
  • muscarinic
  • nicotinic
  • prelimbic
  • thalamus

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The Journal of Neuroscience: 43 (5)
Journal of Neuroscience
Vol. 43, Issue 5
1 Feb 2023
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Differential Regulation of Prelimbic and Thalamic Transmission to the Basolateral Amygdala by Acetylcholine Receptors
Sarah C. Tryon, Joshua X. Bratsch-Prince, James W. Warren, Grace C. Jones, Alexander J. McDonald, David D. Mott
Journal of Neuroscience 1 February 2023, 43 (5) 722-735; DOI: 10.1523/JNEUROSCI.2545-21.2022

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Differential Regulation of Prelimbic and Thalamic Transmission to the Basolateral Amygdala by Acetylcholine Receptors
Sarah C. Tryon, Joshua X. Bratsch-Prince, James W. Warren, Grace C. Jones, Alexander J. McDonald, David D. Mott
Journal of Neuroscience 1 February 2023, 43 (5) 722-735; DOI: 10.1523/JNEUROSCI.2545-21.2022
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Keywords

  • amygdala
  • cholinergic
  • muscarinic
  • nicotinic
  • prelimbic
  • thalamus

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