Distinct Roles of GABAA and GABAB Receptors in Balancing and Terminating Persistent Cortical Activity

Mann, Edward O.; Köhl, Michael; Paulsen, Ole

doi:10.1523/jneurosci.6162-08.2009

Cited by 189 publications

(248 citation statements)

References 34 publications

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“…While co-antagonism of GABA A and GABA B receptors induced paroxysmal depolarizing shift, blocking either GABA A or GABA B receptors alone did not cause catastrophic depolarization. GABA A and GABA B receptors have a complementary role in reducing neural excitation (Mann et al, 2009). GZ significantly reduced conductance and reversed the anoxic depolarization; however, GABA B receptors might prevent the release of excitatory neurotransmitters and excitotoxic cell death even when GABA A receptors are inactive.…”

Section: Discussionmentioning

confidence: 99%

Stellate and pyramidal neurons in goldfish telencephalon respond differently to anoxia and GABA receptor inhibition

Hossein-Javaheri¹,

Wilkie²,

Lado

et al. 2016

Journal of Experimental Biology

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With oxygen deprivation, the mammalian brain undergoes hyperactivity and neuronal death while this does not occur in the anoxiatolerant goldfish (Carassius auratus). Anoxic survival of the goldfish may rely on neuromodulatory mechanisms to suppress neuronal hyper-excitability. As γ-aminobutyric acid (GABA) is the major inhibitory neurotransmitter in the brain, we decided to investigate its potential role in suppressing the electrical activity of goldfish telencephalic neurons. Utilizing whole-cell patch-clamp recording, we recorded the electrical activities of both excitatory ( pyramidal) and inhibitory (stellate) neurons. With anoxia, membrane potential (V m ) depolarized in both cell types from −72.2 mV to −57.7 mV and from −64.5 mV to −46.8 mV in pyramidal and stellate neurons, respectively. While pyramidal cells remained mostly quiescent, action potential frequency (AP f ) of the stellate neurons increased 68-fold. Furthermore, the GABA A receptor reversal potential (E GABA ) was determined using the gramicidin perforated-patch-clamp method and found to be depolarizing in pyramidal (−53.8 mV) and stellate neurons (−42.1 mV). Although GABA was depolarizing, pyramidal neurons remained quiescent as E GABA was below the action potential threshold (−36 mV pyramidal and −38 mV stellate neurons). Inhibition of GABA A receptors with gabazine reversed the anoxiamediated response. While GABA B receptor inhibition alone did not affect the anoxic response, co-antagonism of GABA A and GABA B receptors (gabazine and CGP-55848) led to the generation of seizure-like activities in both neuron types. We conclude that with anoxia, V m depolarizes towards E GABA which increases AP f in stellate neurons and decreases AP f in pyramidal neurons, and that GABA plays an important role in the anoxia tolerance of goldfish brain.

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Section: Discussionmentioning

confidence: 99%

Stellate and pyramidal neurons in goldfish telencephalon respond differently to anoxia and GABA receptor inhibition

Hossein-Javaheri¹,

Wilkie²,

Lado

et al. 2016

Journal of Experimental Biology

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“…The inhibition controls the firing of regular-spiking neurons; inhibitory conductances are always larger than excitatory ones except before an action potential (Hasenstaub et al 2005;Rudolph et al 2007). Furthermore, GABA A conductances have been shown to be important to maintain activity within the network during the active state; the removal of this inhibition shortens the active state's duration and induces epileptiform burst (Mann et al 2009;Sanchez-Vives et al 2010). If inhibition controls the firing of neurons, a strong and synchronous recruitment of interneurons would have the consequence that inhibition would silence neurons and cause a disfacilitation resulting into a full silent state.…”

Section: Discussionmentioning

confidence: 99%

Neocortical inhibitory activities and long-range afferents contribute to the synchronous onset of silent states of the neocortical slow oscillation

Lemieux

Chauvette

Timofeev

2015

Journal of Neurophysiology

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Lemieux M, Chauvette S, Timofeev I. Neocortical inhibitory activities and long-range afferents contribute to the synchronous onset of silent states of the neocortical slow oscillation. J Neurophysiol 113: 768-779, 2015. First published November 12, 2014 doi:10.1152/jn.00858.2013.-During slowwave sleep, neurons of the thalamocortical network are engaged in a slow oscillation (Ͻ1 Hz), which consists of an alternation between the active and the silent states. Several studies have provided insights on the transition from the silent, which are essentially periods of disfacilitation, to the active states. However, the conditions leading to the synchronous onset of the silent state remain elusive. We hypothesized that a synchronous input to local inhibitory neurons could contribute to the transition to the silent state in the cat suprasylvian gyrus during natural sleep and under ketamine-xylazine anesthesia. After partial and complete deafferentation of the cortex, we found that the silent state onset was more variable among remote sites. We found that the transition to the silent state was preceded by a reduction in excitatory postsynaptic potentials and firing probability in cortical neurons. We tested the impact of chloride-mediated inhibition in the silent-state onset. We uncovered a long-duration (100 -300 ms) inhibitory barrage occurring about 250 ms before the silent state onset in 3-6% of neurons during anesthesia and in 12-15% of cases during natural sleep. These inhibitory activities caused a decrease in cortical firing that reduced the excitatory drive in the neocortical network. That chain reaction of disfacilitation ends up on the silent state. Electrical stimuli could trigger a network silent state with a maximal efficacy in deep cortical layers. We conclude that long-range afferents to the neocortex and chloride-mediated inhibition play a role in the initiation of the silent state. slow oscillation; long-range afferents; chloride-mediated inhibition; intracellular recordings SLOW OSCILLATION IS THE HALLMARK of the slow-wave sleep but also of several anesthetics, including ketamine-xylazine (Contreras and Steriade 1995; Steriade et al.

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“…Up states have been observed both in vivo (Li et al 2009;Wilson and Kawaguchi 1996) and in vitro (McCormick et al 2003) and typically occur spontaneously. Up states in cortical pyramidal cells are due to intrinsic cortical dynamics but can be triggered by thalamic input (Maclean et al 2005) and are controlled in a complex manner by GABAergic inhibition (Mann et al 2009). It has been difficult to establish a clear link between Up states and external triggering events, and their function remains unknown.…”

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confidence: 99%

Stimulus-induced up states in the dorsal pallium of a weakly electric fish

Elliott

Maler

2015

Journal of Neurophysiology

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Elliott SB, Maler L. Stimulus-induced up states in the dorsal pallium of a weakly electric fish. J Neurophysiol 114: [2071][2072][2073][2074][2075][2076] 2015.First published August 5, 2015; doi:10.1152/jn.00666.2015.-We investigated the response of putative novelty-detecting neurons in the pallium of an electric fish to electrosensory and acoustic stimuli. Extracellular and whole cell patch recordings were made from neurons in the dorsal pallial nucleus (DD) of Apteronotus leptorhynchus. DD neurons were typically quiescent and exhibited hyperpolarized resting membrane potentials. Stimulation induced, with a variable long latency, rapid though transient depolarization and spike discharge. The transition between resting and depolarized/spiking states resembled the transition to Up states seen in mammalian telencephalic neurons. electrophysiology; up states; weakly electric fish; dorsal pallium ELECTROPHYSIOLOGICAL RECORDINGS from mammalian cortex and striatum have revealed the existence of Up states: the normally quiescent and hyperpolarized membrane potential is interrupted by a brief period of depolarization, increased membrane potential variance, and spike discharge. Up states have been observed both in vivo (Li et al. 2009;Wilson and Kawaguchi 1996) and in vitro (McCormick et al. 2003) and typically occur spontaneously. Up states in cortical pyramidal cells are due to intrinsic cortical dynamics but can be triggered by thalamic input (Maclean et al. 2005) and are controlled in a complex manner by GABAergic inhibition (Mann et al. 2009). It has been difficult to establish a clear link between Up states and external triggering events, and their function remains unknown.Our work focused on Apteronotus leptorhynchus, a weakly electric fish that utilizes its sinusoidal electric organ discharge (EOD) and electroreceptors to communicate, navigate, and locate prey (Chacron et al. 2011;Krahe and Maler 2014;Marsat et al. 2012). The Apteronotus EOD is a constant high-frequency sinusoid, and when two fish are in proximity, their EODs interfere to generate an amplitude modulation (AM) or beat with a frequency equal to the difference of their EOD frequencies. Apteronotus is very sensitive to such AMs and can remember specific beat frequencies for at least 3 days (Harvey-Girard et al. 2010).We recorded from neurons in the dorsal pallium (DD). Neurons in DD have been shown to respond to initial electrosensory beat stimuli and acoustic stimuli with dramatic delayed increases in immediate early gene expression (Egr-1; HarveyGirard et al. 2010). Egr-1 expression also increases in other pallial regions, but to a lesser extent. Egr-1 expression in DD declines to undetectable levels as the fish habituates to a repeatedly presented beat frequency, and expression again increases when novel beat frequencies are presented. This led us to hypothesize that DD was involved in detecting novel stimuli and initiating long-term memory storage of the beat frequency in the large dorsolateral pallium (DL). DD receives glutamergic input from DL...

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Distinct Roles of GABAA and GABAB Receptors in Balancing and Terminating Persistent Cortical Activity

Cited by 189 publications

References 34 publications

Stellate and pyramidal neurons in goldfish telencephalon respond differently to anoxia and GABA receptor inhibition

Stellate and pyramidal neurons in goldfish telencephalon respond differently to anoxia and GABA receptor inhibition

Neocortical inhibitory activities and long-range afferents contribute to the synchronous onset of silent states of the neocortical slow oscillation

Stimulus-induced up states in the dorsal pallium of a weakly electric fish

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