Opposite effects of mu and delta opioid receptor agonists on excitatory propagation induced in rat somatosensory and insular cortices by dental pulp stimulation

Yokota, Eiko; Koyanagi, Yuko; Nakamura, Hiroko; Horinuki, Eri; Oi, Yoshiyuki; Kobayashi, Masayuki

doi:10.1016/j.neulet.2016.05.065

Cited by 14 publications

(7 citation statements)

References 40 publications

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“…These results complement a previous study in which DOR activation resulted in increased activity in the rat insular cortex following dental pulp stimulation, while MOR activation decreased the insular cortex activity (Yokota et al, 2016a). A follow-up study found that inhibitory transmission from fast-spiking interneurons to pyramidal neurons was inhibited by DOR activation (Yokota et al, 2016b). The current results extend these findings to the mouse ACC and identify that specifically, PV interneurons are a target of DOR inhibition.…”

Section: Discussionmentioning

confidence: 99%

“…The ACC in turn projects to the DMS, forming a circuit connecting the MThal and the ACC, both of which provide convergent glutamate inputs to the DMS. This thalamo-cortico-striatal circuit has been demonstrated to be involved in pain processing, in particular, affective pain perception (Rainville et al, 1997; Price, 2000; Fields, 2004; Zhang et al, 2015; Yokota et al, 2016b).…”

Section: Introductionmentioning

confidence: 99%

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

Birdsong

Jongbloets

Engeln

et al. 2019

eLife

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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.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Birdsong

Jongbloets

Engeln

et al. 2019

eLife

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“…The role of delta-opioid receptors is less well understood. Recent studies suggest that selective delta-opioid receptor agonists have opposite effects as mu agonists on electrophysiological responses to somatosensory stimulation (Yokota et al 2016) and selective knockouts of either mu or delta receptors result in opposite emotional behavioral responses (Filliol et al 2000). Consistent with the hypothesis that blockade of delta-opioid receptors could increase motivation for exercise is that mice lacking delta-opioid receptors have been reported to be hyperactive (Filliol et al 2000).…”

Section: Candidate Pharmaceuticals To Increase Motivation For Exercisementioning

confidence: 94%

“…Endogenous opioids have long been hypothesized to play a role in mediating the euphoria derived from voluntary exercise (Boecker et al 2008). Recent studies suggest that selective delta-opioid receptor agonists have opposite effects as mu agonists on electrophysiological responses to somatosensory stimulation (Yokota et al 2016) and selective knockouts of either mu or delta receptors result in opposite emotional behavioral responses (Filliol et al 2000). The role of delta-opioid receptors is less well understood.…”

Section: Candidate Pharmaceuticals To Increase Motivation For Exercisementioning

confidence: 99%

High motivation for exercise is associated with altered chromatin regulators of monoamine receptor gene expression in the striatum of selectively bred mice

Saul¹,

Majdak

Perez

et al. 2016

Genes Brain and Behavior

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Although exercise is critical for health, many lack the motivation to exercise, and it is unclear how motivation might be increased. To uncover the molecular underpinnings of increased motivation for exercise, we analyzed the transcriptome of the striatum in four mouse lines selectively bred for high voluntary wheel running and four non-selected control lines. The striatum was dissected and RNA was extracted and sequenced from four individuals of each line. We found multiple genes and gene systems with strong relationships to both selection and running history over the previous 6 days. Among these genes were Htr1b, a serotonin receptor subunit and Slc38a2, a marker for both glutamatergic and γ-aminobutyric acid (GABA)-ergic signaling. System analysis of the raw results found enrichment of transcriptional regulation and kinase genes. Further, we identified a splice variant affecting the Wnt-related Golgi signaling gene Tmed5. Using coexpression network analysis, we found a cluster of interrelated coexpression modules with relationships to running behavior. From these modules, we built a network correlated with running that predicts a mechanistic relationship between transcriptional regulation by nucleosome structure and Htr1b expression. The Library of Integrated Network-Based Cellular Signatures identified the protein kinase C δ inhibitor, rottlerin, the tyrosine kinase inhibitor, Linifanib and the delta-opioid receptor antagonist 7-benzylidenenaltrexone as potential compounds for increasing the motivation to run. Taken together, our findings support a neurobiological framework of exercise motivation where chromatin state leads to differences in dopamine signaling through modulation of both the primary neurotransmitters glutamate and GABA, and by neuromodulators such as serotonin.

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“…We performed optical imaging using a VSD (RH1691, Optical Imaging) as previously described (Horinuki et al, 2015, 2016; Nakamura et al, 2015, 2016; Fujita et al, 2016, 2017; Yokota et al, 2016; Kobayashi and Horinuki, 2017) to observe IANX-induced changes in the spatiotemporal profiles of the excitatory propagation induced by electrical stimulation of the dental pulps at the macroscopic level (Figs. 1-3).…”

Section: Methodsmentioning

confidence: 99%

Trigeminal Nerve Transection-Induced Neuroplastic Changes in the Somatosensory and Insular Cortices in a Rat Ectopic Pain Model

Fujita

Yamamoto

Kobayashi

2019

eNeuro

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The primary sensory cortex processes competitive sensory inputs. Ablation of these competitive inputs induces neuroplastic changes in local cortical circuits. However, information concerning cortical plasticity induced by a disturbance of competitive nociceptive inputs is limited. Nociceptive information from the maxillary and mandibular molar pulps converges at the border between the ventral secondary somatosensory cortex (S2) and insular oral region (IOR); therefore, S2/IOR is a suitable target for examining the cortical changes induced by a disturbance of noxious inputs, which often causes neuropathic pain and allodynia. We focused on the plastic changes in S2/IOR excitation in a model of rats subjected to inferior alveolar nerve transection (IANX). Our optical imaging using a voltage-sensitive dye (VSD) revealed that the maxillary molar pulp stimulation-induced excitatory propagation was expanded one to two weeks after IANX at the macroscopic level. At the cellular level, based on Ca2+ imaging using two-photon microscopy, the amplitude of the Ca2+ responses and the number of responding neurons in S2/IOR increased in both excitatory and inhibitory neurons. The in vitro laser scanning photostimulation (LSPS) revealed that Layer II/III pyramidal and GABAergic fast-spiking neurons in S2/IOR received larger excitatory inputs from Layer IV in the IANX models, which supports the findings obtained by the macroscopic and microscopic optical imaging. Furthermore, the inhibitory postsynaptic inputs to the pyramidal neurons were decreased in the IANX models, suggesting suppression of inhibitory synaptic transmission onto excitatory neurons. These results suggest that IANX induces plastic changes in S2/IOR by changing the local excitatory and inhibitory circuits.

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Opposite effects of mu and delta opioid receptor agonists on excitatory propagation induced in rat somatosensory and insular cortices by dental pulp stimulation

Cited by 14 publications

References 40 publications

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

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

High motivation for exercise is associated with altered chromatin regulators of monoamine receptor gene expression in the striatum of selectively bred mice

Trigeminal Nerve Transection-Induced Neuroplastic Changes in the Somatosensory and Insular Cortices in a Rat Ectopic Pain Model

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