Elsevier

Brain Research

Volume 529, Issues 1–2, 8 October 1990, Pages 30-41
Brain Research

Locally evoked potentials in slices of the rat nucleus accumbens: NMDA and non-NMDA receptor mediated components and modulation by GABA

https://doi.org/10.1016/0006-8993(90)90808-OGet rights and content

Abstract

In a slice preparation of the rat nucleus accumbens (Acb), local electrical stimulation elicited a field potential composed of two negative peaks, followed by a positive wave. The early negative peak was identified as a non-synaptic compound action potential, the late negative peak as a monosynaptic population spike (PS) and the positive wave as a mixture of an excitatory and an inhibitory postsynaptic potential (PSP). Both the PS and the PSP exhibited a marked degree of paired-pulse facilitation. The quisqualate/kainate receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX; 2 μM) and the broadly acting glutamate receptor antagonist kynurenic acid (300 μM) reversibly abolished or reduced both the PS and PSP. In contrast, nicotinic, muscarinic and N-methyl-d-aspartate (NMDA) receptor antagonists had no suppressive action. Washout of Mg2+ from the superfusion medium reversibly enhanced and prolonged the PSP and this effect was blocked by the NMDA receptor antagonistd(−)-2-amino-5-phosphonopentanoic acid (d-AP-5). The γ-aminobutyric acid antagonist picrotoxin (60 μM) enhanced the PS and induced secondary spikes which were superimposed on a prolonged PSP. Most of this prolongation was abolished byd-AP-5. It is concluded that locally evoked synaptic responses in the Acb are mediated by glutamate or aspartate, and that NMDA receptor mediated activity evoked by low-frequency stimulation is substantial in Mg2+-free medium or during reduced GABAA receptor activity, but not under normal conditions.

Reference (64)

  • HornykiewiczO.

    Psychopharmacological implications of dopamine and dopamine antagonists: a critical evaluation of current evidence

    Neuroscience

    (1978)
  • JonesD.L. et al.

    Nucleus accumbens to globus pallidus GABA projection: electrophysiological and iontophoretic investigations

    Brain Research

    (1980)
  • JonesR.S.G.

    Complex synaptic responses of entorhinal cortical cells in the rat to subicular stimulation in vitro: demonstration of an NMDA receptor-mediated component

    Neurosci. Lett.

    (1987)
  • KelleyA.E. et al.

    The amygdalostriatal projection in the rat — an anatomical study by anterograde and retrograde tracing methods

    Neuroscience

    (1982)
  • MelchersB.P.C. et al.

    Quantitative correlation between tetanus-induced decreases in extracellular calcium and LTP

    Brain Research

    (1988)
  • MiljkovicZ. et al.

    Voltage-dependent block of excitatory amino acid currents by pentobarbital

    Brain Research

    (1986)
  • MogensonG.J. et al.

    From motivation to action: functional interface between the limbic system and the motor system

    Prog. Neurobiol.

    (1980)
  • NakanishiH. et al.

    An N-methyl-d-aspartate receptor mediated excitatory postsynaptic potential evoked in subthalamic neurons in an in vitro slices preparation of the rat

    Neurosci. Lett.

    (1988)
  • NautaW.J.H. et al.

    Efferent connections and nigral afferents of the nucleus accumbens septi in the rat

    Neuroscience

    (1978)
  • NeumanR.S. et al.

    Blockade of excitatory synaptic transmission by 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) in the hippocampus in vitro

    Neurosci. Lett.

    (1988)
  • ParkM.R. et al.

    Recurrent inhibition in the rat neostriatum

    Brain Research

    (1980)
  • PhillipsonO.T. et al.

    The topographic order of inputs to nucleus accumbens in the rat

    Neuroscience

    (1985)
  • RobinsonM.B. et al.

    Kynurenic acid as an antagonist of hippocampal excitatory transmission

    Brain Research

    (1984)
  • TakagiM. et al.

    Suppressing action of cholinergic agents on synaptic transmissions in the corpus striatum of rats

    Exp. Neurol.

    (1978)
  • WalaasI. et al.

    The distribution and origin of glutamate decarboxylase and choline acetyltransferase in ventral pallidum and other basal forebrain regions

    Brain Research

    (1979)
  • WalaasI. et al.

    Biochemical evidence fro gamma-aminobutyrate containing fibres from the nucleus accumbens to the substantia nigra and ventral tegmental area in the rat

    Neuroscience

    (1980)
  • WalaasI. et al.

    Biochemical evidence for glutamate as a transmitter in hippocampal efferents to the basal forebrain and hypothalamus in the rat brain

    Neuroscience

    (1980)
  • AndersenP. et al.

    Unit analysis of hippocampa population spikes

    Exp. Brain Res.

    (1971)
  • BolamJ.P.

    Synapses of identified neurons in the neostriatum

  • CollingridgeG.L. et al.

    Excitatory amino-acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus

    J. Physiol.

    (1983)
  • CordingleyG.E. et al.

    Non-cholinergic synaptic excitation in neostriatum: pharmacological evidence for mediation by a glutamate-like transmitter

    Br. J. Pharmacol.

    (1986)
  • CreagerR. et al.

    Paired-pulse and frequency facilitation in the CA1-region of the in vitro rat hippocampus

    J. Physiol.

    (1980)
  • Cited by (59)

    • Orexin type-2 receptor blockade prevents the nicotine-induced excitation of nucleus accumbens core neurons in rats: An electrophysiological perspective

      2019, Pharmacological Reports
      Citation Excerpt :

      Dopamine and glutamate inputs can influence each other [52,53] and NAc MSNs express both DA and glutamate receptors [49,50]. Glutamate inputs from some brain areas, such as the prefrontal cortex (PFC), amygdala (AMG), and hippocampus [43–45] project on and activate MSNs of NAc, and blockade of glutamate receptors causes a reduction in the excitability of NAc MSNs [54,55], and affects excitatory postsynaptic potentials [55,56]. There is an anatomical relationship between orexin and dopamine neurons in the medial PFC, AMG, and NAc [57].

    • AMPA receptor plasticity in the nucleus accumbens after repeated exposure to cocaine

      2010, Neuroscience and Biobehavioral Reviews
      Citation Excerpt :

      This review will focus specifically on cocaine-induced alterations in glutamate transmission and plasticity involving α-amino-3-hydroxy-5-methylisoxazole-4-propionate receptors (AMPAR) in the NAc. Glutamate inputs acutely excite NAc MSN primarily by activating AMPAR (Pennartz et al., 1990; Hu and White, 1996) and results in many animal models of addiction indicate that AMPAR activation in the NAc is necessary for drug seeking. Thus, intra-NAc infusion of AMPAR antagonists blocks cue-induced cocaine seeking after withdrawal (Conrad et al., 20081), cocaine seeking under second-order schedules of reinforcement (Di Ciano and Everitt, 20012; Di Ciano and Everitt, 20041), cue-induced reinstatement (Bäckstrom and Hyytiä, 20071), and cocaine-primed reinstatement (Cornish and Kalivas, 20003; Famous et al., 20084).

    • Analogs of JHU75528, a PET ligand for imaging of cerebral cannabinoid receptors (CB1): Development of ligands with optimized lipophilicity and binding affinity

      2009, European Journal of Medicinal Chemistry
      Citation Excerpt :

      During the recording, slices were maintained at 32–33 °C and were continuously superfused at a rate of 2 mL/min with a modified artificial cerebrospinal fluid (aCSF) consisting of (in mM) NaCl, 126; KCl, 3.0; MgCl2, 1.5; CaCl2, 2.4; NaH2PO4, 1.2; glucose, 11.0; NaHCO3, 26, and saturated with 95% O2 and 5% CO2. In order to isolate glutamate-driven synaptic potentials [51] the aCSF also contained the GABAA-receptor antagonist picrotoxin (100 μM) and the N-methyl-d-aspartate (NMDA)-type receptor antagonist APV (40 μM). Electrical stimulation was performed using a bipolar tungsten stimulating electrode placed near (<100 μm) the recording electrode, in the dorsal striatum.

    • Biological substrates of reward and aversion: A nucleus accumbens activity hypothesis

      2009, Neuropharmacology
      Citation Excerpt :

      These data provided early evidence that blockade of NMDA receptors in the NAc is sufficient for reward and, by extension, reward can be dopamine-independent. Blockade of NMDA receptors would be expected to produce an overall reduction in the excitability of NAc MSNs without affecting baseline excitatory input mediated by AMPA receptors (Uchimura et al., 1989; Pennartz et al., 1990). Importantly, rats also self-administered NMDA antagonists into deep layers of the PFC (Carlezon and Wise, 1996), which project directly to the NAc (see Kelley, 2004) and have been conceptualized as a part of an inhibitory (STOP!)

    View all citing articles on Scopus
    View full text