Presynaptic GABAB receptors differentially modulate GABA release from cholecystokinin and parvalbumin interneurons onto CA1 pyramidal neurons: A cell type-specific labeling and activating study

Shao, Chen; Dong, Jiaxue; Zhao, Mingwei; Liu, Shenhao; Wang, Xue; Yu, Yang; Fang, Lingyan; Zhu, Ziying; Chen, Qian; Xu, Xin; Zhang, Weining; Yang, Kun

doi:10.1016/j.neulet.2022.136448

Cited by 8 publications

(3 citation statements)

References 15 publications

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“…Other studies that used electrophysiological recordings and freeze-fracture replica-based quantitative immunogold electron microscopy have revealed the presence of presynaptic GABAbRs on hippocampal CCK and PV-INs 14 . Fast, GABAaR inhibition from PV to Pyr neurons is weakly reduced by presynaptic GABAbRs in the hippocampus 14 , 37 , 38 ; however, these effects may be region-specific since GABAa-mediated inhibition from L5 fast-spiking (presumably PV) interneurons was strongly modulated by GABAbRs 39 . In developing gerbil auditory cortex, GABAaR-mediated inhibition from L2/3 FS (presumably PV-INs), but not from LTS (presumably SST-INs) is controlled by presynaptic GABAbRs 40 .…”

Section: Discussionmentioning

confidence: 99%

Somatostatin-expressing interneurons modulate neocortical network through GABAb receptors in a synapse-specific manner

Kanigowski

Bogaj

Barth

et al. 2023

Sci Rep

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The firing activity of somatostatin-expressing inhibitory neurons (SST-INs) can suppress network activity via both GABAa and GABAb receptors (Rs). Although SST-INs do not receive GABAaR input from other SST-INs, it is possible that SST-IN-released GABA could suppress the activity of SST-INs themselves via GABAbRs, providing a negative feedback loop. Here we characterized the influence of GABAbR modulation on SST-IN activity in layer 2/3 of the somatosensory cortex in mice. We compared this to the effects of GABAbR activation on parvalbumin-expressing interneurons (PV-INs). Using in vitro whole-cell patch clamp recordings, pharmacological and optogenetic manipulations, we found that the firing activity of SST-INs suppresses excitatory drive to themselves via presynaptic GABAbRs. Postsynaptic GABAbRs did not influence SST-IN spontaneous activity or intrinsic excitability. Although GABAbRs at pre- and postsynaptic inputs to PV-INs are modestly activated during cortical network activity in vitro, the spontaneous firing of SST-INs was not the source of GABA driving this GABAbR activation. Thus, SST-IN firing regulates excitatory synaptic strength through presynaptic GABAbRs at connections between pyramidal neurons (Pyr-Pyr) and synapses between pyramidal neurons and SST-INs (Pyr-SST), but not Pyr-PV and PV-Pyr synapses. Our study indicates that two main types of neocortical inhibitory interneurons are differentially modulated by SST-IN-mediated GABA release.

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Section: Discussionmentioning

confidence: 99%

Somatostatin-expressing interneurons modulate neocortical network through GABAb receptors in a synapse-specific manner

Kanigowski

Bogaj

Barth

et al. 2023

Sci Rep

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“…Other studies that used electrophysiological recordings and freeze-fracture replica-based quantitative immunogold electron microscopy have revealed the presence of presynaptic GABAbRs on hippocampal CCK and PV-INs (Booker et al, 2017). Fast, GABAaR inhibition from PV to Pyr neurons is weakly reduced by presynaptic GABAbRs in the hippocampus (Booker et al, 2017;Liu et al, 2019;Shao et al, 2022); however, these effects may be region-speci c since GABAamediated inhibition from L5 fast-spiking (presumably PV) interneurons was strongly modulated by GABAbRs (Kruglikov & Rudy, 2008). In developing gerbil auditory cortex, GABAaR-mediated inhibition from L2/3 FS (presumably PV-INs), but not from LTS (presumably SST-INs) is controlled by presynaptic GABAbRs (Takesian et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

SST interneurons modulate neocortical network through GABAb receptors in a synapse- specific manner

Kanigowski

Bogaj

Barth

et al. 2023

Preprint

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The firing activity of somatostatin-expressing inhibitory neurons (SST-INs) can suppress network activity via both GABAa and GABAb receptors (Rs). Although SST-INs do not receive GABAaR input from other SST-INs, it is possible that SST-IN-released GABA could suppress the activity of SST-INs themselves via GABAbRs, providing a negative feedback loop. Here we characterized the influence of GABAbR modulation on SST-IN activity in layer 2/3 of the somatosensory cortex in mice. We compared this to the effects of GABAbR activation on parvalbumin-expressing interneurons (PV-INs). Using in vitrowhole-cell patch clamp recordings, pharmacological and optogenetic manipulations, we found that the firing activity of SST-INs suppresses excitatory drive to themselves via presynaptic GABAbRs. Postsynaptic GABAbRs did not influence SST-IN spontaneous activity or intrinsic excitability. Although GABAbRs at pre- and postsynaptic inputs to PV-INs are modestly activated during cortical network activity in vitro, the spontaneous firing of SST-INs was not the source of GABA driving this GABAbR activation. Thus, SST-IN firing regulates excitatory synaptic strength through presynaptic GABAbRs at connections between pyramidal neurons (Pyr-Pyr) and synapses between pyramidal neurons and SST-INs (Pyr-SST), but not Pyr-PV and PV-Pyr synapses. Our study indicates that two main types of neocortical inhibitory interneurons are differentially modulated by SST-IN-mediated GABA release.

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“…These findings indicated that despite the inhibitory effect of MORs and DORs on the CA1 PV-expressing basket cells via suppressing GABA release by the inhibition of voltage-sensitive Ca 2+ channels, the colocalization of MORs and DORs on the PV-expressing interneurons does not necessarily imply the functional crosstalk between these two potassium channels [114]. It is worth mentioning that GABA released from the terminals of the PV-expressing interneuron onto the CA1 pyramidal neurons is extensively suppressed by MORs (Table 1) [160]. In the hippocampal CA2 region, PV-expressing interneurons express a distinct long-term depression (LTD) through feedforward inhibition of the CA3 Schaffer collateral inputs to the CA2 region which is regulated by the activity of DORs.…”

Section: Opioids and Parvalbuminmentioning

confidence: 99%

Shared Mechanisms of GABAergic and Opioidergic Transmission Regulate Corticolimbic Reward Systems and Cognitive Aspects of Motivational Behaviors

et al. 2023

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The functional interplay between the corticolimbic GABAergic and opioidergic systems plays a crucial role in regulating the reward system and cognitive aspects of motivational behaviors leading to the development of addictive behaviors and disorders. This review provides a summary of the shared mechanisms of GABAergic and opioidergic transmission, which modulate the activity of dopaminergic neurons located in the ventral tegmental area (VTA), the central hub of the reward mechanisms. This review comprehensively covers the neuroanatomical and neurobiological aspects of corticolimbic inhibitory neurons that express opioid receptors, which act as modulators of corticolimbic GABAergic transmission. The presence of opioid and GABA receptors on the same neurons allows for the modulation of the activity of dopaminergic neurons in the ventral tegmental area, which plays a key role in the reward mechanisms of the brain. This colocalization of receptors and their immunochemical markers can provide a comprehensive understanding for clinicians and researchers, revealing the neuronal circuits that contribute to the reward system. Moreover, this review highlights the importance of GABAergic transmission-induced neuroplasticity under the modulation of opioid receptors. It discusses their interactive role in reinforcement learning, network oscillation, aversive behaviors, and local feedback or feedforward inhibitions in reward mechanisms. Understanding the shared mechanisms of these systems may lead to the development of new therapeutic approaches for addiction, reward-related disorders, and drug-induced cognitive impairment.

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Presynaptic GABAB receptors differentially modulate GABA release from cholecystokinin and parvalbumin interneurons onto CA1 pyramidal neurons: A cell type-specific labeling and activating study

Cited by 8 publications

References 15 publications

Somatostatin-expressing interneurons modulate neocortical network through GABAb receptors in a synapse-specific manner

Somatostatin-expressing interneurons modulate neocortical network through GABAb receptors in a synapse-specific manner

SST interneurons modulate neocortical network through GABAb receptors in a synapse- specific manner

Shared Mechanisms of GABAergic and Opioidergic Transmission Regulate Corticolimbic Reward Systems and Cognitive Aspects of Motivational Behaviors

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