Synapse-specific opioid modulation of thalamo-cortico-striatal circuits

The medial thalamus (MThal), anterior cingulate cortex (ACC) and striatum play important roles in affective-motivational pain processing and reward learning. Opioids affect both pain and reward through uncharacterized modulation of this circuitry. This study examined opioid actions on glutamate tran...

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Bibliographic Details
Published in:eLife 2019-05, Vol.8
Main Authors: Birdsong, William T, Jongbloets, Bart C, Engeln, Kim A, Wang, Dong, Scherrer, Grégory, Mao, Tianyi
Format: Article
Language:English
Subjects:
Agonists
Analgesics, Opioid - metabolism
Animals
Brain
Corpus Striatum - drug effects
cortex
Cortex (cingulate)
Experiments
feed-forward inhibition
GABA
Glutamate
Gyrus Cinguli - drug effects
Interneurons
Learning - drug effects
Legal fees
Mice
Narcotics
Neostriatum
Nerve Net - drug effects
Neurons
Neuroscience
Neurosciences
opioid
opioid receptor
Opioid receptors (type delta)
Opioid receptors (type mu)
Opioids
Pain
Parvalbumin
Physiological aspects
Prefrontal cortex
Pyramidal cells
Receptors, Opioid, delta - agonists
Receptors, Opioid, mu - agonists
Reinforcement
Software
Spiny neurons
Statistical analysis
Striatum
Synapses
Synapses - drug effects
Thalamus
Thalamus - drug effects
γ-Aminobutyric acid
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Summary:The medial thalamus (MThal), anterior cingulate cortex (ACC) and striatum play important roles in affective-motivational pain processing and reward learning. Opioids affect both pain and reward through uncharacterized modulation of this circuitry. This study examined opioid actions on glutamate transmission between these brain regions in mouse. Mu-opioid receptor (MOR) agonists potently inhibited MThal inputs without affecting ACC inputs to individual striatal medium spiny neurons (MSNs). MOR activation also inhibited MThal inputs to the pyramidal neurons in the ACC. In contrast, delta-opioid receptor (DOR) agonists disinhibited ACC pyramidal neuron responses to MThal inputs by suppressing local feed-forward GABA signaling from parvalbumin-positive interneurons. As a result, DOR activation in the ACC facilitated poly-synaptic (thalamo-cortico-striatal) excitation of MSNs by MThal inputs. These results suggest that opioid effects on pain and reward may be shaped by the relative selectivity of opioid drugs to the specific circuit components.
ISSN:2050-084X
2050-084X
DOI:10.7554/elife.45146