Nicotinic activity depresses synaptic potentiation in layer V pyramidal neurons of mouse insular cortex

Sato, Hajime; Kawano, Takahito; Yin, Dong; Kato, Takafumi; Toyoda, Hiroki

doi:10.1016/j.neuroscience.2017.06.031

Cited by 18 publications

(56 citation statements)

References 55 publications

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“…B), although the contribution of nAChR‐expressing neurons in other cortical layers cannot be excluded (see below). These results are similar to the findings observed in layer 5 pyramidal neurons (Sato et al ., ). The activation of nAChRs moderately increased both glutamatergic and GABAergic synaptic inputs onto layer 6 pyramidal neurons, and nicotine enhanced synaptic potentiation in layer 6 pyramidal neurons.…”

Section: Discussionmentioning

confidence: 97%

“…This result supports the observation that glutamatergic inputs onto layer 2/3 pyramidal neurons in the insular cortex were not modulated by nAChRs. In addition, in layer 3 of the insular cortex, the nearly half of FS interneurons expressed α7 nAChRs and the majority of non‐FS interneurons expressed α7‐ and/or β2‐containing nAChRs, similar to the observations found in layers 2/3 and 5 of the prefrontal cortex (Couey et al ., ; Poorthuis et al ., ) and in layer 5 of the insular cortex (Sato et al ., ). The GABAergic synaptic transmission onto layer 3 pyramidal neurons was strongly increased by activation of nAChRs, mainly via activation of β2‐containing nAChRs and to a minor extent via activation of α7‐containing nAChRs.…”

Section: Discussionmentioning

confidence: 97%

“…The layer 5 pyramidal neurons in the insular cortex express α7‐containing nAChRs, and glutamatergic synaptic inputs onto layer 5 pyramidal neurons are enhanced by nAChRs. Nevertheless, activation of nAChRs suppresses synaptic potentiation through enhancing GABAergic synaptic transmission (Sato et al ., ). Similar to the findings observed in layer 5 pyramidal neurons, I demonstrated that activation of nAChRs suppressed synaptic potentiation in layer 3 pyramidal neurons.…”

Section: Discussionmentioning

confidence: 97%

“…Thus, in both humans and animals, the insular cortex is likely to be strongly involved in nicotine addiction, but the underlying cellular and synaptic mechanisms remain largely unknown. Our previous and present studies reveal how activation of nAChRs modulates synaptic potentiation in layers 3, 5 and 6 pyramidal neurons of the mouse insular cortex (Sato et al ., ). However, how the layer‐specific modulation of synaptic plasticity by nAChRs is associated with nicotine addiction remains unclear.…”

Section: Discussionmentioning

confidence: 97%

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Nicotinic activity layer specifically modulates synaptic potentiation in the mouse insular cortex

Toyoda

2018

Eur J of Neuroscience

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Nicotinic acetylcholine receptors (nAChRs) in the insular cortex play an important role in nicotine addiction, but its cellular and synaptic mechanisms underlying nicotine addiction still remain unresolved. In layer 5 pyramidal neurons of the mouse insular cortex, activation of nAChRs suppresses synaptic potentiation through enhancing GABAergic synaptic transmission via activation of β2-containing nAChRs in non-fast-spiking (non-FS) interneurons. However, it has not been addressed whether and how activation of nAChRs modulates synaptic plasticity in layers 3 and 6 pyramidal neurons of the insular cortex. In this study, I demonstrate that activation of nAChRs oppositely modulates synaptic potentiation in layers 3 and 6 pyramidal neurons of the insular cortex. In layer 3 pyramidal neurons, activation of nAChRs depressed synaptic potentiation induced by combination of presynaptic stimulation with postsynaptic depolarization (paired training) through enhancing GABAergic synaptic transmission via activation of β2-containing nAChRs in non-FS interneurons. By contrast, in layer 6 pyramidal neurons, activation of nAChRs enhanced synaptic potentiation through activating postsynaptic β2-containing nAChRs. These results indicate, in different layers of the mouse insular cortex, paired training-induced synaptic potentiation is oppositely regulated by activation of nAChRs which are located on GABAergic interneurons (layer 3) and on pyramidal neurons (layer 6). Thus, layer-specific modulation of synaptic potentiation may be involved in cellular and synaptic mechanisms of insular cortical changes in nicotine addiction.

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Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 97%

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Nicotinic activity layer specifically modulates synaptic potentiation in the mouse insular cortex

Toyoda

2018

Eur J of Neuroscience

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“…Acquisition of LiCl-induced CTA is dependent on relatively more caudal areas of the IC (Schier et al, 2016; Schier et al, 2014). Nicotine administered to the anterior IC increases GABAergic tone and ultimately results in a depression of synaptic potentiation (Sato et al, 2017), primarily at layer 5-pyramidal neurons, the primary excitatory output of the IC. The present results could reasonably be due to the ability for nicotine to enhance long-term depression in the insular cortex.…”

Section: Discussionmentioning

confidence: 99%

Nicotine pre-treatment reduces sensitivity to the interoceptive stimulus effects of commonly abused drugs as assessed with taste conditioning paradigms

Loney¹,

Meyer²

2019

Drug and Alcohol Dependence

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Background: Drug pre-exposure attenuates sensitivity to the interoceptive stimulus properties of additional subsequently administered drugs in drug-induced conditioned taste avoidance (CTA) and conditioned place preference (CPP) paradigms. Specifically, nicotine, commonly used in conjunction with other addictive substances, attenuates acquisition of ethanol and caffeine As and morphine-induced CPP. Methods: Because nicotine use is comorbid with a number of substance use disorders, we systematically examined the effects of nicotine pre-exposure on two different conditioning paradigms involving integration of the interoceptive stimulus properties of multiple commonly abused drugs, in male and female rats, designed to examine both the aversive and reinforcing properties of these drugs. Results: Nicotine dose-dependently interfered with acquisition of CTA to passively administered morphine, ethanol, and cocaine, but not lithium chloride, demonstrating that the effects of nicotine are not simply a matter of reduced orosensory processing or an inability to learn such associations. Moreover, nicotine-treated rats required higher doses of drug in order to develop CTA and did not show increased acceptance of the taste of self-administered ethanol compared with saline-treated rats. Conclusions: These data demonstrate that nicotine pre-exposure attenuates sensitivity to the stimulus effects of multiple drugs in two conditioning paradigms, in a manner which is consistent with a reduced ability to integrate the interoceptive properties of abused drugs. Through reducing these stimulus properties of drugs of abuse, concomitant nicotine use may result in a need to increase either the frequency or strength of doses during drug-taking, thus likely contributing to enhanced addiction liability in smokers.

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Interaction of nicotinic acetylcholine receptors with dopamine receptors in synaptic plasticity of the mouse insular cortex

Toyoda

2019

Synapse

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The insular cortex plays essential roles in nicotine addiction. However, much is still unknown about its cellular and synaptic mechanisms responsible for nicotine addiction. We have previously shown that in layer 5 pyramidal neurons of the mouse insular cortex, activation of the nicotinic acetylcholine receptors (nAChRs) suppresses synaptic potentiation through enhancing GABAergic synaptic transmission, although it enhances both glutamatergic and GABAergic synaptic transmission. In the present study, we examined whether dopamine receptors might contribute to the nicotine‐induced inhibition of synaptic potentiation. The nicotine‐induced inhibition of synaptic potentiation was decreased in the presence of a D1 dopamine receptor antagonist SCH23390 irrespective of the presence of a D2 dopamine receptor antagonist sulpiride, suggesting that D1 dopamine receptors are involved in nicotine‐induced inhibition. We also investigated how dopamine receptors might contribute to the nAChR‐induced enhancement of glutamatergic and GABAergic synaptic transmission. The nAChR‐induced enhancement of GABAergic synaptic transmission was decreased in the presence of SCH23390 irrespective of the presence of sulpiride, whereas that of glutamatergic synaptic transmission was not altered in the presence of SCH23390 and sulpiride. These results suggest that D1 dopamine receptors are involved in the nAChR‐induced enhancement of GABAergic synaptic transmission while dopamine receptors are not involved in that of glutamatergic synaptic transmission. These observations indicate that the interaction between nAChRs and D1 dopamine receptors plays critical roles in synaptic activities in layer 5 pyramidal neurons of the mouse insular cortex. These insular synaptic changes might be associated with nicotine addiction.

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Nicotinic activity depresses synaptic potentiation in layer V pyramidal neurons of mouse insular cortex

Cited by 18 publications

References 55 publications

Nicotinic activity layer specifically modulates synaptic potentiation in the mouse insular cortex

Nicotinic activity layer specifically modulates synaptic potentiation in the mouse insular cortex

Nicotine pre-treatment reduces sensitivity to the interoceptive stimulus effects of commonly abused drugs as assessed with taste conditioning paradigms

Interaction of nicotinic acetylcholine receptors with dopamine receptors in synaptic plasticity of the mouse insular cortex

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