Excitatory projections from the amygdala to neurons in the nucleus pontis oralis in the rat: an intracellular study

Abstract There is a consensus that active (REM) sleep (AS) is controlled by cholinergic projections from the laterodorsal and pedunculopontine tegmental nuclei (LDT/PPT) to neurons in the nucleus pontis oralis (NPO) that generate AS (i.e. AS-Generator neurons). The present study was designed to prov...

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Published in:Neuroscience 2011-12, Vol.197, p.181-190
Main Authors: Xi, M, Fung, S.J, Sampogna, S, Chase, M.H
Format: Article
Language:English
Subjects:
amygdala
Amygdala - cytology
Amygdala - physiology
Animals
Biological and medical sciences
Brain Stem - cytology
Brain Stem - physiology
electrical stimulation
Excitatory Postsynaptic Potentials - physiology
Fundamental and applied biological sciences. Psychology
Male
Membrane Potentials - physiology
Neural Pathways - cytology
Neural Pathways - physiology
Neurology
Neuronal Plasticity - physiology
Neurons - cytology
Neurons - physiology
nucleus pontis oralis
Rats
Rats, Sprague-Dawley
REM sleep
Sleep, REM - physiology
Sleep. Vigilance
synaptic potentials
Vertebrates: nervous system and sense organs
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Summary:Abstract There is a consensus that active (REM) sleep (AS) is controlled by cholinergic projections from the laterodorsal and pedunculopontine tegmental nuclei (LDT/PPT) to neurons in the nucleus pontis oralis (NPO) that generate AS (i.e. AS-Generator neurons). The present study was designed to provide evidence that other projections to the NPO, such as those from the amygdala, are also capable of inducing AS. Accordingly, the responses of neurons, recorded intracellularly in the NPO, were examined following stimulation of the ipsilateral central nucleus of the amygdala (CNA) in urethane-anesthetized rats. Single pulse stimulation in the CNA produced an early, fast depolarizing potential (EPSP) in neurons within the NPO. The mean latency to the onset of these excitatory postsynaptic potentials (EPSPs) was 3.6±0.2 ms. A late, small-amplitude inhibitory synaptic potential (IPSP) was present following EPSPs in a portion of the NPO neurons. Following stimulation of the CNA with a train of 8–10 pulses, NPO neurons exhibited a sustained depolarization (5–10 mV) of their resting membrane potential. When single subthreshold intracellular depolarizing current pulses were delivered to NPO neurons, CNA-induced EPSPs were sufficient to promote the discharge of these cells. Stimulation of the CNA with a short train of stimuli induced potent temporal facilitation of EPSPs in NPO neurons. Two forms of synaptic plasticity were revealed by the patterns of response of NPO neurons following stimulation of the CNA: paired-pulse facilitation (PPF) and post-tetanic potentiation (PTP). Six of recorded NPO neurons were identified morphologically with neurobiotin. They were medium to large, multipolar cells with diameters >20 μM, which resemble AS-on cells in the NPO. The present results demonstrate that amygdalar projections are capable of exerting a powerful excitatory postsynaptic drive that activates NPO neurons. Therefore, we suggest that the amygdala is capable of inducing AS via direct projections to AS-Generator neurons in the NPO.
ISSN:0306-4522
1873-7544
DOI:10.1016/j.neuroscience.2011.09.029