Metabotropic glutamate receptors modulate glutamatergic and GABAergic synaptic transmission in the central nucleus of the inferior colliculus

Farazifard, Rasoul; Wu, Shu Hui

doi:10.1016/j.brainres.2010.02.021

Cited by 24 publications

(18 citation statements)

References 64 publications

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“…A similar decrease of GABAergic neurotransmission by presynaptic mGluRs has been observed in other brain regions (Chen and Bonham 2005;Farazifard and Wu 2010;Hanania and Johnson 1999;Hayashi et al 1993;Jones et al 1998;Jouvenceau et al 1995;Liu et al 1993;Neale and Salt 2006;Salt and Eaton 1995;Salt and Turner 1998). However, our data demonstrate for the first time the effects of mGluR activation on specific intracortical GABAergic pathways in V1 and A1.…”

Section: Discussionsupporting

confidence: 89%

“…However, studies that tested this idea have produced a range of results. Activation of group II mGluRs has been shown to suppress GABAergic responses in hippocampus (Jouvenceau et al 1995;Liu et al 1993), thalamus (Salt and Eaton 1995;Salt and Turner 1998), olfactory bulb (Hayashi et al 1993), striatum (Hanania and Johnson 1999), tectum (Farazifard and Wu 2010;Neale and Salt 2006), and parts of brain stem (Chen and Bonham 2005;Jones et al 1998). However, group I mGluR activation appears to have no significant effect in most brain regions with the exception of striatum (Hanania and Johnson 1999;Wang et al 1996) and some parts of brain stem (Jones et al 1998), where it increases GABA release.…”

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confidence: 99%

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Modulatory effects of activation of metabotropic glutamate receptors on GABAergic circuits in the mouse cortex

Liu

Petrof

Sherman

2014

Journal of Neurophysiology

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Liu T, Petrof I, Sherman SM. Modulatory effects of activation of metabotropic glutamate receptors on GABAergic circuits in the mouse cortex. J Neurophysiol 111: 2287-2297, 2014. First published March 12, 2014 doi:10.1152/jn.00730.2013.-Metabotropic glutamate receptors (mGluRs) have a ubiquitous distribution in the central nervous system and often serve to regulate the release of neurotransmitters. We have previously shown that activation of both presynaptic and postsynaptic mGluRs can affect the gain of glutamatergic inputs in both thalamus and cortex. In the present study, we sought to determine the effect of mGluR activation on GABAergic inputs in cortex. Using whole cell recordings in a mouse slice preparation of either primary visual or auditory cortex (V1 or A1), we tested the effects on mGluRs by applying various agonists to the slice. Two pathways were tested in each area: the GABAergic inputs in layers 2/3 activated from layer 4 and the GABAergic inputs in layer 4 activated from adjacent layer 4. In both of these pathways, we found that activation of mGluRs significantly reduced the amplitude of the evoked inhibitory postsynaptic currents. Because the effects were not blocked by the addition of GDP␤S to the recording electrode, and because mGluR agonists did not affect responses to photostimulation of GABA in a low-Ca 2ϩ and high-Mg 2ϩ bathing solution, we concluded this reduction was due to activation of presynaptic mGluRs. Furthermore, using specific mGluR agonists, we found that group II mGluRs, but not group I mGluRs, were involved in these modulatory effects. Because similar results were found in both pathways in V1 and A1, a possible cortical pattern for these effects is suggested. cortical circuit; GABA; IPSC; mGluR; modulation METABOTROPIC GLUTAMATE RECEPTORS (mGluRs) are G proteincoupled receptors found in many areas of the mammalian brain (Hollmann and Heinemann 1994). Previous work from our laboratory has shown that activation of mGluRs either by agonist application or by stimulation of certain glutamatergic inputs reduces the gain of synaptic transmission in other glutamatergic inputs. Both presynaptic and postsynaptic mGluRs have been implicated in this phenomenon in various combinations [reviewed in Sherman (2014)].Recent studies have indicated the existence of mGluRs on GABAergic terminals, suggesting the possibility that activation of these receptors can modulate GABA release (Cartmell and Schoepp 2000;Pinheiro and Mulle 2008;Schoepp 2001). However, studies that tested this idea have produced a range of results. Activation of group II mGluRs has been shown to suppress GABAergic responses in hippocampus (Jouvenceau et al. 1995;Liu et al. 1993 Given the importance of GABAergic circuitry in cortex (Anderson et al. 2000;DeFelipe 1993;Ferster and Miller 2000;Haglund et al. 1992; Hamberger and van Gelder 1993;Hirsch and Martinez 2006;Marco et al. 1996;Monier et al. 2003;Sherwin 1999;Wood et al. 1979) and given the widespread presence of mGluRs in cortex, we sought to investigate the effects of...

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Section: Discussionsupporting

confidence: 89%

mentioning

confidence: 99%

Modulatory effects of activation of metabotropic glutamate receptors on GABAergic circuits in the mouse cortex

Liu

Petrof

Sherman

2014

Journal of Neurophysiology

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“…Antagonism but not activation of group II mGluRs also increases firing of IC neurons in vivo (Voytenko and Galazyuk, 2011), suggesting suppression of cellular excitability by endogenous activity of group II mGluRs. Using whole-cell patch recordings in brains slices, Farazifard and Wu (2010) showed that activation of group II mGluRs suppresses both EPSCs and inhibitory postsynaptic currents (IPSCs) in IC neurons, and the effects are mediated by presynaptic actions. In contrast, activation of group I or III mGluRs modulates neither the synaptic responses nor the intrinsic properties (Farazifard and Wu, 2010).…”

Section: Anatomy and Physiology Of Mglurs In Mammalian Auditory Midbrainmentioning

confidence: 99%

Metabotropic glutamate receptors in auditory processing

2014

Neuroscience

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As the major excitatory neurotransmitter used in the vertebrate brain, glutamate activates ionotropic and metabotropic glutamate receptors (mGluRs), which mediate fast and slow neuronal actions, respectively. Important modulatory roles of mGluRs have been shown in many brain areas, and drugs targeting mGluRs have been developed for treatment of brain disorders. Here, I review the studies on mGluRs in the auditory system. Anatomical expression of mGluRs in the cochlear nucleus has been well characterized, while data for other auditory nuclei await more systematic investigations at both the light and electron microscopy levels. The physiology of mGluRs has been extensively studied using in vitro brain slice preparations, with a focus on the lower auditory brainstem in both mammals and birds. These in vitro physiological studies have revealed that mGluRs participate in neurotransmission, regulate ionic homeostasis, induce synaptic plasticity, and maintain the balance between excitation and inhibition in a variety of auditory structures. However, very few in vivo physiological studies on mGluRs in auditory processing have been undertaken at the systems level. Many questions regarding the essential roles of mGluRs in auditory processing still remain unanswered and more rigorous basic research is warranted.

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“…mGlu2/3 receptors are members of the group II family of mGluRs. These G i -coupled receptors function as autoreceptors; regulating presynaptic neurotransmitter release (Baskys and Malenka, 1991;Liu et al, 1993;Macek et al, 1996;Marek et al, 2000;Molinaro et al, 2009;Farazifard and Wu, 2010). As such, activation of mGlu2/3 receptors decreases the synaptic availability of glutamate, allowing for 'refinement' of glutamatergic neurotransmission (Schoepp, 2001;Pinheiro and Mulle, 2008).…”

Section: Introductionmentioning

confidence: 99%

Activation of Group II Metabotropic Glutamate Receptors Inhibits the Discriminative Stimulus Effects of Alcohol via Selective Activity Within the Amygdala

Cannady

Grondin

Fisher

et al. 2011

Neuropsychopharmacol

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Metabotropic glutamate receptor subtypes (mGlu2/3) regulate a variety of alcohol-associated behaviors, including alcohol reinforcement, and relapse-like behavior. To date, the role of mGlu2/3 receptors in modulating the discriminative stimulus effects of alcohol has not been examined. Given that the discriminative stimulus effects of drugs are determinants of abuse liability and can influence drug seeking, we examined the contributions of mGlu2/3 receptors in modulating the discriminative stimulus effects of alcohol. In male Long-Evans rats trained to discriminate between alcohol (1 g/kg, IG) and water, the mGlu2/3 agonist LY379268 (0.3-10 mg/kg) did not produce alcohollike stimulus effects. However, pretreatment with LY379268 (1 and 3 mg/kg; in combination with alcohol) inhibited the stimulus effects of alcohol (1 g/kg). Systemic LY379268 (3 mg/kg, i.p.) was associated with increases in neuronal activity within the amygdala, but not the nucleus accumbens, as assessed by c-Fos immunoreactivity. Intra-amygdala activation of mGlu2/3 receptors by LY379268 (6 mg) inhibited the discriminative stimulus effects of alcohol, without altering response rate. In contrast, intra-accumbens LY379268 (3 mg) profoundly reduced response rate; however, at lower LY379268 doses (0.3, 1 mg), the discriminative stimulus effects of alcohol and response rate were not altered. These data suggest that amygdala mGlu2/3 receptors have a functional role in modulating the discriminative stimulus properties of alcohol and demonstrate differential motor sensitivity to activation of mGlu2/3 receptors in the amygdala and the accumbens. Understanding the neuronal mechanisms that underlie the discriminative stimulus effects of alcohol may prove to be important for future development of pharmacotherapies for treating alcoholism.

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Metabotropic glutamate receptors modulate glutamatergic and GABAergic synaptic transmission in the central nucleus of the inferior colliculus

Cited by 24 publications

References 64 publications

Modulatory effects of activation of metabotropic glutamate receptors on GABAergic circuits in the mouse cortex

Modulatory effects of activation of metabotropic glutamate receptors on GABAergic circuits in the mouse cortex

Metabotropic glutamate receptors in auditory processing

Activation of Group II Metabotropic Glutamate Receptors Inhibits the Discriminative Stimulus Effects of Alcohol via Selective Activity Within the Amygdala

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