GABA-induced long-term potentiation in the guinea-pig superior colliculus
Introduction
γ-Aminobutyric acid (GABA) receptors can be divided into three subclasses: GABA-A, -B and -C receptors. Bicuculline-sensitive GABA-A and bicuculline-insensitive GABA-C receptors are associated with an ion channel selectively permeable for chloride (Cl−) and bicarbonate (HCO3−), whereas GABA-B receptors couple to Ca2+ and K+ channels via G-proteins and intracellular second messenger systems (Bormann, 1988, Bormann and Feigenspann, 1995). The GABA-C receptor has only recently been studied at the molecular level and has, so far, been investigated in detail only in the retina (Quian and Dowling, 1993, Quian and Dowling, 1995) and in expression systems such as oocytes (Kusama et al., 1993a, Kusama et al., 1993b).
Although GABA is the main inhibitory neurotransmitter in the central nervous system it can also depolarise neurones under certain conditions for instance in the hippocampus of neonatal rats (Cherubini et al., 1991, Strata and Cherubini, 1994, Martina et al., 1995, Ben-Ari et al., 1997). In this context, GABA was found to increase intracellular calcium via the activation of voltage-dependent calcium channels (VDCCs, Reichling et al., 1994, Leinekugel et al., 1995, Obrietan and van den Pol, 1995) which appears to play a major role in early development (Cherubini et al., 1991, LoTurco et al., 1995, Obrietan and van den Pol, 1996), but also after neuronal injury (Van den Pol et al., 1996). In addition, strong activation of GABA-A receptors was reported to cause a biphasic inhibitory/excitatory response in distal dendrites of the mature hippocampus (Alger and Nicoll, 1979, Andersen et al., 1980, Lambert et al., 1991) which could also be observed after 200 Hz stimulation (Grover et al., 1993).
The superior colliculus (SC) is a multi-layered midbrain nucleus which shows various forms of plasticity such as tetanus-induced long-term potentiation (LTP, Miyamoto et al., 1990) habituation (Platt and Withington, 1997a) and paired-pulse depression (Platt and Withington, 1997c). GABA has been described as a major transmitter beside the excitatory neurotransmitter glutamate. In fact, approximately 50% of SC neurones show GABA-labelling and highest concentrations of GABA and glutamate decarboxylase, the GABA synthesising enzyme are found in this brain area (Mize, 1992). Three different types of GABA-labelled neurones have been identified in the SC, with the densest distribution of GABA receptors found in the superficial layers (Mize, 1992, Okada, 1992). Application of GABA was described to cause both an enhancement and depression of evoked postsynaptic potentials in SC slices of adult guinea-pigs, depending on the concentration used (Arakawa and Okada, 1988). Interestingly, GABA-mediated excitation could also be induced by applying the GABA-uptake inhibitor nipecotic acid. In this paper, the authors attributed the excitatory action of GABA to GABA-A and the inhibitory action to GABA-B receptor activation. However, application of GABA-A antagonists caused clear signs of disinhibition in SC slices (Arakawa and Okada, 1988, Platt and Withington, 1997a, Platt and Withington, 1997c) and tetanus-induced in vivo LTP could only be induced in the presence of GABA-A antagonists (Hirai and Okada, 1993) suggesting inhibitory rather than excitatory GABA-A mediated responses. In the frog optic tectum (the homologue of the SC in amphibians), an excitatory action of GABA was reported which was insensitive to the specific GABA-A antagonist bicuculline (Nistri and Sivilotti, 1985, Sivilotti and Nistri, 1989). Similar evidence for bicuculline- and baclofen-insensitive excitatory GABA receptors in early postnatal life was provided for instance in the hippocampal slice preparation (Strata and Cherubini, 1994, Martina et al., 1995).
The aim of the present study was to characterise pharmacologically the unusual excitatory action of GABA in SC slices of adult guinea pigs, and the consequences of GABA-induced excitation on synaptic transmission. A preliminary report of some of the data presented here has already appeared in abstract form (Platt and Withington, 1997b).
Section snippets
Methods
A detailed description of the experimental procedures can be found elsewhere (Platt and Withington, 1997c). Briefly, anaesthetised adult guinea-pigs (>50 days) were decapitated and the brains were quickly transferred into ice-cold Ringer solution (composition in mM: NaCl 125, KCl 5, MgCl2 1.3, CaCl2 2.5, KH2PO4 1.2, glucose 10, NaHCO3 25; saturated with 95% O2/5% CO2, pH 7.4,). Sagittal SC slices (400 μm) were prepared using a vibratome. After 60 min of equilibration at 32°C, slices were placed
GABA causes a long-lasting enhancement of synaptic transmission
During superfusion of GABA (300 μM–3 mM) an enhancement of the fEPSP recorded in the SGL of the SC (see Fig. 1A for experimental design) was seen which is in agreement with the reports of others (Arakawa and Okada, 1988, Okada, 1992).
When GABA was applied for 7 min, however, the enhancement of the fEPSP was found to be sustained and lasted for at least 1 h after washout. We propose that this type of long-lasting increase of synaptic efficacy, termed `GABA-induced long-term potentiation' (LTPG),
The excitatory action of GABA is not mediated through GABA-A or -B receptors
Our data show that application of GABA (≤3 mM) caused an enhancement of evoked fEPSPs in the superficial layers of the SC leading to a novel form of long-term potentiation, LTPG. For the 3 mM group, the increase of the slope was maintained after removal of GABA while it declined partially when induced by 500 μM indicating the concentration-dependence of LTPG. The enhancement of the fEPSP slope during superfusion of 3 mM GABA was slightly weaker than the one observed during application of 500 μM
Acknowledgements
BP was supported by the European Community, DJW is a senior MRC Research Fellow.
References (46)
- et al.
Muscimol-induced long-term depression in the hippocampus: lack of dependence of extracellular calcium
Neuroscience
(1996) - et al.
Excitatory and inhibitory action of GABA on synaptic transmission in slices of guinea-pig superior colliculus
Eur. J. Pharmacol.
(1988) - et al.
GABAA, NMDA and AMPA receptors: a developmentally regulated `menage à trois'
Trends Neurosci.
(1997) Electrophysiology of GABAA and GABAB receptor subtypes
Trends Neurosci.
(1988)- et al.
GABAC receptors
Trends Neurosci.
(1995) - et al.
GABA: an excitatory transmitter in early postnatal life
Trends Neurosci.
(1991) Calcium signaling
Cell
(1995)Diversity of GABA receptors in the vertebrate outer retina
Trends Neurosci.
(1995)- et al.
Ca2+-dependent routes to Ras: mechanisms for neuronal survival, differentiation, and plasticity?
Neuron
(1996) - et al.
Ipsilateral corticotectal pathway inhibits the formation of long-term potentiation (LTP) in the rat superior colliculus through GABAergic mechanism
Brain Res.
(1993)
Inhibitory effect of GABA (γ-aminobutyric acid) on the induction of long-term potentiation in guinea-pig superior colliculus slices
Neurosci. Lett.
GABA ρ2 receptor pharmacological profile: GABA recognition site similarities to ρ1
Eur. J. Pharmacol.
GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis
Neuron
Masking effect of NMDA receptor antagonists on the formation of long-term potentiation (LTP) in superior colliculus slices from the guinea pig
Brain Res.
The distribution and function of gamma-aminobutyric acid (GABA) in the superior colliculus
Prog. Brain Res.
Response habituation in the superficial layers of the guinea-pig superior colliculus in vitro
Neurosci. Lett.
Pharmacology of a novel effect of γ-aminobutyric acid on the frog optic tectum
Eur. J. Pharmacol.
GABA-mediated biphasic inhibitory responses in hippocampus
Nature
Two different responses of hippocampal pyramidal cells to application of gamma-aminobutyric acid
J. Physiol.
A synaptic model for memory: long-term potentiation in the hippocampus
Nature
Expression of GABA receptor ρ subunits in rat brain
J. Neurochem.
Role of excitatory amino acid receptors in synaptic transmission in area CA1 of rat hippocampus
Proc. R. Soc. Lond.
Role of HCO3- ions in depolarizing GABAA receptor mediated responses in pyramidal cells of rat hippocampus
J. Neurophysiol.
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