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Frontiers in Neuroanatomy (1)
The European journal of neuroscience (1)
Gutiérrez, Rafael (2)
Traub, Roger D. (2)
Davidson, Kimberly G. V. (1)
Hamzei-Sichani, Farid (1)
Hof, Patrick R. (1)
Janssen, William G. M. (1)
Ottersen, Ole P. (1)
Rash, John E. (1)
Vivar, Carmen (1)
Wearne, Susan L. (1)
Yasumura, Thomas (1)
Year of Publication
Mixed Electrical-Chemical Transmission between Hippocampal Mossy Fibers and Pyramidal Cells
Traub, Roger D.
The European journal of neuroscience
Morphological and electrophysiological studies have shown that granule cell axons, the mossy fibers (MFs), establish gap junctions and, therefore, electrical communication among them. That granule cells express gap junctional proteins in their axons suggests the possibility that their terminals express them as well. If this were to be the case, mixed electrical-chemical communication could be supported, as MF terminals normally use glutamate for fast communication with their target cells. Here we present electrophysiological and modeling studies consistent with this hypothesis. We show that MF activation produced fast spikelets followed by excitatory postsynaptic potentials in pyramidal cells (PCs), which, unlike the spikelets, underwent frequency potentiation and were strongly depressed by activation of metabotropic glutamate receptors, as expected from transmission of MF origin. The spikelets, which persisted during blockade of chemical transmission, wee potentiated by dopamine and suppressed by the gap junction blocker carbenoxolone. The various waveforms evoked by MF stimulation were replicated in a multi-compartment model of a PC by brief current pulse injections into the proximal apical dendritic compartment, where MFs are known to contact PCs. Mixed electrical and glutamatergic communication between granule cells and some PCs in CA3 may ensure the activation of sets of PCs, bypassing the strong action of concurrent feed-forward inhibition that granule cells activate. Importantly, MF-to-PC electrical coupling may allow bidirectional, possibly graded communication that can be faster than chemical synapses and subject to different forms of modulation.
CA3; mossy fibers; spikelets; mixed transmission; electrical communication
Mixed Electrical–Chemical Synapses in Adult Rat Hippocampus are Primarily Glutamatergic and Coupled by Connexin-36
Davidson, Kimberly G. V.
Janssen, William G. M.
Wearne, Susan L.
Hof, Patrick R.
Traub, Roger D.
Ottersen, Ole P.
Rash, John E.
Frontiers in Neuroanatomy
Dendrodendritic electrical signaling via gap junctions is now an accepted feature of neuronal communication in mammalian brain, whereas axodendritic and axosomatic gap junctions have rarely been described. We present ultrastructural, immunocytochemical, and dye-coupling evidence for “mixed” (electrical/chemical) synapses on both principal cells and interneurons in adult rat hippocampus. Thin-section electron microscopic images of small gap junction-like appositions were found at mossy fiber (MF) terminals on thorny excrescences of CA3 pyramidal neurons (CA3pyr), apparently forming glutamatergic mixed synapses. Lucifer Yellow injected into weakly fixed CA3pyr was detected in MF axons that contacted four injected CA3pyr, supporting gap junction-mediated coupling between those two types of principal cells. Freeze-fracture replica immunogold labeling revealed diverse sizes and morphologies of connexin-36-containing gap junctions throughout hippocampus. Of 20 immunogold-labeled gap junctions, seven were large (328–1140 connexons), three of which were consistent with electrical synapses between interneurons; but nine were at axon terminal synapses, three of which were immediately adjacent to distinctive glutamate receptor-containing postsynaptic densities, forming mixed glutamatergic synapses. Four others were adjacent to small clusters of immunogold-labeled 10-nm E-face intramembrane particles, apparently representing extrasynaptic glutamate receptor particles. Gap junctions also were on spines in stratum lucidum, stratum oriens, dentate gyrus, and hilus, on both interneurons and unidentified neurons. In addition, one putative GABAergic mixed synapse was found in thin-section images of a CA3pyr, but none were found by immunogold labeling, suggesting the rarity of GABAergic mixed synapses. Cx36-containing gap junctions throughout hippocampus suggest the possibility of reciprocal modulation of electrical and chemical signals in diverse hippocampal neurons.
CA3; dentate gyrus; interneuron; pyramidal neuron; principal cell; mossy fiber; gap junction
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