Gap junctions on GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus (CA1 region)

Katsumaru, Hironobu; Kosaka, Toshio; Heizmann, Claus W.; Hama, Kiyoshi

doi:10.1007/bf00250257

Cited by 67 publications

(66 citation statements)

References 18 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Gap junctions have been reported among granule cells, although very rarely (MacVicar and Dudek, 1982). Anatomical studies have only reported gap junctions among intemeurons (Katsumaru et al, 1988).…”

Section: Discussionmentioning

confidence: 99%

EPSPs of dentate gyrus granule cells during epileptiform bursts of dentate hilar "mossy" cells and area CA3 pyramidal cells in disinhibited rat hippocampal slices

Scharfman

1994

J. Neurosci.

View full text Add to dashboard Cite

When hippocampal slices are exposed to GABAA antagonists, area CA3 pyramidal cells and dentate hilar “mossy” cells discharge in synchronized epileptiform bursts (Muller and Misgeld, 1991; Scharfman, 1994b). Dentate interneurons are excited simultaneously, but the degree of discharge varies (Scharfman, 1994b). This study primarily examined the activity of dentate granule cells simultaneous to the epileptiform bursts of pyramidal cells and mossy cells. EPSPs followed by large GABAB receptor-mediated IPSPs were generated in granule cells during all epileptiform bursts of pyramidal cells and mossy cells, regardless of whether they were evoked or spontaneous. By simultaneous recording it was determined that granule cell EPSPs began several milliseconds after the start of pyramidal cell bursts (n = 48 simultaneous recordings) and immediately after the first action potential of a mossy cell burst (n = 77). Interneurons were similar to granule cells in the timing of their depolarizations relative to the onset of pyramidal cell (n = 24; Scharfman, 1994b) and mossy cell (n = 9) bursts. All excitatory activity was blocked by bath application of the glutamatergic AMPA/kainate receptor antagonist CNQX (5 microM, n = 5), but not the NMDA receptor antagonist D-APV (25–50 microM, n = 9). Granule cell EPSPs were decreased after focal application of CNQX to the molecular layer at a site close to the impaled granule cell (n = 5), whereas D-APV had no effect (n = 3). EPSPs also decreased after focal application of CNQX to the hilus, in two of four slices tested. The extracellularly recorded EPSP of granule cells was maximal in the inner molecular layer (n = 33), the site of the mossy cell axonal plexus. Severing the junction of the dentate gyrus and area CA3 blocked all spontaneous and evoked activity of dentate neurons without affecting burst discharges in area CA3a and CA3b (n = 6). None of the excitatory activity of any cell type was affected by cholinergic antagonists (atropine and mecamylamine, 25 microM each, n = 5; pirenzipine and dihydro-beta-erythroidine, 25 microM each, n = 5). The results suggest that there is a glutamatergic, AMPA/kainate receptor- mediated, excitatory pathway from area CA3 to the dentate gyrus in disinhibited slices. The pharmacological results, analyses of latency, as well as the known axonal projections of the sampled cells, suggest that the excitatory pathway begins within area CA3 and leads to granule cells via mossy cells. The data also suggest that dentate interneurons are excited by mossy cells, and possibly by pyramidal cells as well.(ABSTRACT TRUNCATED AT 400 WORDS)

show abstract

Section: Discussionmentioning

confidence: 99%

EPSPs of dentate gyrus granule cells during epileptiform bursts of dentate hilar "mossy" cells and area CA3 pyramidal cells in disinhibited rat hippocampal slices

Scharfman

1994

J. Neurosci.

View full text Add to dashboard Cite

show abstract

“…23,87 Moreover, they are coupled via electrical synapses, thus forming functional interneuron networks. 49,[93][94][95][96][97][98] This special feature is well suited to synchronize basket cell spiking with high temporal fidelity in the hippocampus as well as in the neocortex. 8,16,24,99 In brief, an action potential exerts a shortlasting depolarization of electrically coupled basket cells, which is immediately curtailed by the subsequent strong IPSP.…”

Section: Hippocampal Gamma Oscillations and Fast-spiking Inhibitory Imentioning

confidence: 99%

Highly Energized Inhibitory Interneurons are a Central Element for Information Processing in Cortical Networks

Kann

Papageorgiou

Draguhn

2014

J Cereb Blood Flow Metab

236

235

View full text Add to dashboard Cite

Gamma oscillations (B30 to 100 Hz) provide a fundamental mechanism of information processing during sensory perception, motor behavior, and memory formation by coordination of neuronal activity in networks of the hippocampus and neocortex. We review the cellular mechanisms of gamma oscillations about the underlying neuroenergetics, i.e., high oxygen consumption rate and exquisite sensitivity to metabolic stress during hypoxia or poisoning of mitochondrial oxidative phosphorylation. Gamma oscillations emerge from the precise synaptic interactions of excitatory pyramidal cells and inhibitory GABAergic interneurons. In particular, specialized interneurons such as parvalbumin-positive basket cells generate action potentials at high frequency ('fast-spiking') and synchronize the activity of numerous pyramidal cells by rhythmic inhibition ('clockwork'). As prerequisites, fast-spiking interneurons have unique electrophysiological properties and particularly high energy utilization, which is reflected in the ultrastructure by enrichment with mitochondria and cytochrome c oxidase, most likely needed for extensive membrane ion transport and g-aminobutyric acid metabolism. This supports the hypothesis that highly energized fast-spiking interneurons are a central element for cortical information processing and may be critical for cognitive decline when energy supply becomes limited ('interneuron energy hypothesis'). As a clinical perspective, we discuss the functional consequences of metabolic and oxidative stress in fast-spiking interneurons in aging, ischemia, Alzheimer's disease, and schizophrenia.

show abstract

“…Electrical communication between interneurons has been demonstrated to be essential for the generation of gamma waves (Katsumaru et al, 1988;Gibson et al, 1999;Tamas et al, 2000), thereby supporting a role for interneuronal gap junctions at producing fast rhythmic synchronization in small patches of nervous tissue . Gamma oscillations are relevant in neuronal communication and synaptic plasticity (Bibbig et al, 2002), providing cues for understanding neuronal processing in both local and distributed cortical networks involved in cognitive functions (Jensen et al, 2007).…”

Section: Introductionmentioning

confidence: 96%

Role of tau protein on neocortical and hippocampal oscillatory patterns

et al. 2011

View full text Add to dashboard Cite

ABSTRACT:Tau is a neuronal microtubule-associated protein implicated in microtubules stabilization, axonal establishment and elongation during neuronal morphogenesis. Because of its elevated expression in neocortical regions and hippocampus, tau might play a role in sculpting collective neural responses underlying slow and fast brain oscillations and/or long-range synchronization patterns between hippocampus and neocortex. To test this hypothesis, local field potentials were recorded in tau-deficient (tau 2/2 ) and wild-type mice from different neocortical regions and from the hippocampus during spontaneous motor exploratory behavior. We found that tau 2/2 mice showed hippocampal theta slowing and reduced levels of gamma long-range synchronization involving the frontal cortex. We hypothesize that the lack of normal phosphorylated tau during early stages of development might influence the maturation of parvalbumin interneurons affecting the spatiotemporal structure of long-range gamma synchronization. Also, the proper functioning of gap-junction channels might be compromised by the absence of tau in hippocampal networks. Altogether, these results provide novel insights into the functional role of tau protein in the formation of collective neural responses and emergence of neocortical-hippocampal interactions in the mammalian brain. V V C 2010 Wiley-Liss, Inc.

show abstract

Gap junctions on GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus (CA1 region)

Cited by 67 publications

References 18 publications

EPSPs of dentate gyrus granule cells during epileptiform bursts of dentate hilar "mossy" cells and area CA3 pyramidal cells in disinhibited rat hippocampal slices

EPSPs of dentate gyrus granule cells during epileptiform bursts of dentate hilar "mossy" cells and area CA3 pyramidal cells in disinhibited rat hippocampal slices

Highly Energized Inhibitory Interneurons are a Central Element for Information Processing in Cortical Networks

Role of tau protein on neocortical and hippocampal oscillatory patterns

Contact Info

Product

Resources

About