Activity-Dependent Layer-Specific Changes in the Extracellular Chloride Concentration and Chloride Driving Force in the Rat Hippocampus

Centre de Recherche Université Laval Robert Giffard, University Laval, Quebec, Canada.
Journal of Neurophysiology (Impact Factor: 2.89). 04/2010; 103(4):1905-14. DOI: 10.1152/jn.00497.2009
Source: PubMed


The transmembrane distribution of chloride anions (Cl⁻) determines the direction of the Cl⁻ flux through GABA(A) receptors; this establishes whether GABA(A) receptor-mediated responses are hyperpolarizing or depolarizing in neurons. Thus an activity-dependent reduction in the efficacy of inhibitory responses can be the result of an activity-induced reduction of the Cl⁻ driving force. Using Cl(-)-sensitive electrodes, we measured the extracellular Cl⁻ concentration ([Cl⁻](o)) in each layer of the hippocampus under control conditions and after stimulation. In the control condition, [Cl⁻](o) was lower within the CA1 region (112.9 ± 1.3 mM; mean ± SD) than the CA3/dentate gyrus areas (117.7 ± 1.2 mM). Stimulation of CA3 pyramidal cells led to an increase in the [Cl⁻](o). The maximum values were observed in the stratum lacunosum-moleculare (253.4 ± 51.1 mM) and in the hilus (261 ± 43.7 mM), whereas in the granular cell layer, it reached only 159.5 ± 41 mM. The stimulation-induced [Cl⁻](o) increase was followed by a period of decreasing [Cl⁻](o) that fell below the control values. The maximum undershoot (21.6 ± 0.7 mM) was observed in the s. radiatum. Systemic application of the gap junction blocker carbenoxolone significantly decreased the stimulation-induced Cl⁻ extrusion in the dentate gyrus but only slightly modified it in the CA1 area. Carbenoxolone also drastically reduced the Cl⁻ clearance. The time constant of the Cl⁻ clearance was similar between layers (83.4 ± 15.9 ms) but increased after carbenoxolone application (207.1 ± 44.4 ms). Stimulation-induced changes in the [Cl⁻](o) significantly decreased the Cl⁻ driving force and resulted in large fluctuations between layers (Δ = 9.4 mV). The lowest value was observed in the stratum radiatum of the CA1 and the hilar region (7.7 mV), whereas the highest value was calculated for the granule cell layer (16.3 mV). We suggest that a decrease of the extracellular space is mainly responsible for the rapid [Cl⁻](o) increase while the gap junction coupled astrocytic network plays a key role in the activity-dependent redistribution and clearance of Cl⁻ across layers of the hippocampus.

4 Reads
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: To understand further how oligodendrocytes regulate brain function, the mechanism of communication between oligodendrocytes and other cell types needs to be explored. An important mode of communication between various cell types in the nervous system involves gap junctions. Astroglial cells are extensively connected through gap junctions forming the glial syncytium. Although the presence of gap junctions between oligodendrocytes and astrocytes have been well documented, evidence for gap junction-mediated calcium transfer between these two glial populations is still missing. To measure functional coupling between astrocytes and oligodendrocytes and to test whether this coupling is mediated by gap junctions we used laser photostimulation and monitored Ca(2+) propagation in cultures from transgenic animals in which oligodendrocytes express enhanced green fluorescent protein (eGFP). We show that waves of Ca(2+) spread from astrocytes to oligodendrocytes and that these waves are blocked by the broad-spectrum gap junction blocker carbenoxolone, but not the neuron-specific gap junction blocker quinine. We also show that the spread of Ca(2+) waves between astrocytes and oligodendrocytes is bi-directional. Thus, increase of Ca(2+) concentration in astrocytes triggered by surrounding neuronal activity may feed back onto different neuronal populations through oligodendrocytes.
    Neuroscience 03/2010; 167(4):1032-43. DOI:10.1016/j.neuroscience.2010.03.004 · 3.36 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: This technique proposes a new approach to correlate intra- and extracellular variations of the ionic concentrations in vivo by means of tapered optical waveguides coupled to standard electrophysiological electrodes to monitor in vivo simultaneously the intracellular and extracellular K(+) concentration as well as the neighboring field potential. The optical fibers were tapered to a final diameter of approximately 10 μm and were used to guide the excitation light deep into the tissue and to collect the fluorescence emanating from the intracellular milieu. This fiber was coupled to a double barrel ion-sensitive electrode forming a micro-optrode with a final diameter around 15 μm. The method was successfully used to record the intracellular K(+) evolution with the fluorescent indicator PBFI during three states: normal sleep-like patterns, paroxysmal seizures, and coma. While we could not disclose any phasic fluctuations of the intracellular K(+) during normal sleep patterns, they were clearly present during seizures and coma. In the majority of cases (58%), paroxysmal discharges were associated with positive variations of the intracellular fluorescence of 62±5% corresponding to extracellular K(+) increases of 2.04±0.4 mM. In the remaining cases (42%) intracellular K(+) dropped by 44.4±12% for an extracellular K(+) increase of 2.62±0.47 mM. We suggest that this differential behavior might reflect different cellular populations (glia vs. neurons, respectively). Comatose states were accompanied by an extracellular drop of K(+) of 1.31±0.13 mM, which was reflected, in all cases, by an intracellular K(+) increase of 39±4%.
    Journal of Neuroscience Methods 10/2010; 194(2):206-17. DOI:10.1016/j.jneumeth.2010.10.004 · 2.05 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Acute traumatic mandibular condyle dislocations into the middle cranial fossa are rare. The diagnosis of intracranial condylar dislocation is difficult, and CT is the most effective screening tool to get early correct diagnosis. A patient with an acute traumatic dislocated condyle into the middle cranial fossa, which was treated conservatively, is presented here. After conservative treatment, the patient restored to normal function of jaw movement, and the fractures of the middle cranial fossa completely healed and the condyle was in the reconstruction stage. The anatomic features, clinical features, and mechanism of injury for this rare type of condylar dislocation were discussed to help recognize this easily overlooked injury and avoid disastrous complications.
    Asian Journal of Oral and Maxillofacial Surgery 01/2013; 25(1). DOI:10.1016/j.ajoms.2011.10.004
Show more

Similar Publications