Olfactory Reciprocal Synapses: Dendritic Signaling in the CNS

Isaacson, Jeffry S.; Strowbridge, Ben W.

doi:10.1016/s0896-6273(00)81013-2

Cited by 468 publications

(615 citation statements)

References 48 publications

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“…It has been shown that dendrodendritic synapses possess unique functional properties, such as a dependence on NMDA receptors rather than AMPA receptors for their activation (Isaacson and Strowbridge, 1998;Schoppa et al, 1998). Here, we have shown that NMDA and AMPA receptors are colocalized at dendrodendritic synapses and that they are distributed along the entire postsynaptic specialization of granule cell spines.…”

Section: Glutamate Receptors In Granule Cellsmentioning

confidence: 59%

“…These studies have demonstrated that mitral cells release glutamate and excite granule cell dendrites (Trombley and Shepherd, 1992;Wellis and Kauer, 1994), which in turn mediate GABAergic inhibition back onto the mitral cells (Nicoll, 1971;Nowycky et al, 1981a;Jahr and Nicoll, 1982;Wellis and Kauer, 1993). Recent electrophysiological investigations have revealed unexpected properties of dendrodendritic synapses, including a dependence on NMDA, rather than AMPA, receptors for the activation of granule cells (Isaacson and Strowbridge, 1998;Schoppa et al, 1998) and a self-excitation of mitral cell dendrites, similarly dependent on NMDA receptors (Aroniadou-Anderjaska et al, 1999;Isaacson, 1999). Based on these observations, one would hypothesize that NMDA receptors are located presynaptically as well as postsynaptically at dendrodendritic synapses, but this remains to be shown by anatomical techniques.…”

Section: Abstract: Dendrodendritic Synapse; Olfactory Bulb; Nmda Recmentioning

confidence: 99%

“…Likewise, it is not known whether NMDA and AMPA receptors differ in their distance from the presynaptic active zones, which could explain why AMPA receptors are less effective than NMDA receptors at eliciting GABA release from granule cells. The specialized arrangement of reciprocal synapses also suggests that NMDA receptors could be located close to the GABA release sites on granule cell dendrites and that entry of calcium through these receptors could contribute to trigger the release of GABA (see Discussion in Isaacson and Strowbridge, 1998;Schoppa et al, 1998).…”

Section: Abstract: Dendrodendritic Synapse; Olfactory Bulb; Nmda Recmentioning

confidence: 99%

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Organization of Ionotropic Glutamate Receptors at Dendrodendritic Synapses in the Rat Olfactory Bulb

Sassoè‐Pognetto

Ottersen

2000

J. Neurosci.

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Dendrodendritic synapses between mitral (or tufted) and granule cells of the olfactory bulb play a major role in the processes of odor discrimination and olfactory learning. Release of glutamate at these synapses activates postsynaptic receptors on the dendritic spines of granule cells, as well as presynaptic NMDA receptors in the mitral cell membrane. However, immunocytochemical studies have failed to demonstrate the presence of ionotropic glutamate receptors in granule cell dendrites. By using a postembedding immunogold procedure, we describe here the precise organization of neurotransmitter receptors at dendrodendritic synapses. We show that there is a selective localization of glutamate and GABA receptors at asymmetric and symmetric synaptic junctions, respectively. In addition, we demonstrate that NMDA and AMPA receptors are clustered at postsynaptic specializations on granule cell spines and that they are extensively colocalized. Conversely, glutamate receptors do not appear to be concentrated in clusters on mitral cell dendrites, suggesting that the presynaptic effects of glutamate are mediated by a small complement of extrasynaptic receptors. By analyzing the subsynaptic distribution of the NR1 and GluR2/3 subunits, we show that they are distributed along the entire extent of the postsynaptic specialization, indicating that both NMDA and AMPA receptors are available for dendrodendritic signaling between mitral and granule cells. These results indicate that the principles recently found to underlie the organization of glutamate receptors at axospinous synapses also apply to dendrodendritic synapses.

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Section: Glutamate Receptors In Granule Cellsmentioning

confidence: 59%

Section: Abstract: Dendrodendritic Synapse; Olfactory Bulb; Nmda Recmentioning

confidence: 99%

Section: Abstract: Dendrodendritic Synapse; Olfactory Bulb; Nmda Recmentioning

confidence: 99%

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Organization of Ionotropic Glutamate Receptors at Dendrodendritic Synapses in the Rat Olfactory Bulb

Sassoè‐Pognetto

Ottersen

2000

J. Neurosci.

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“…A similar type of neural organization (combination of reciprocal, afferent, and``efferent'' terminals formed by the same``interneuron'' on different cellsÐreciprocal interaction) is very common at the level of second-order neurons in the olfactory bulb and retina. These interneurons have been suspected of forming``reciprocal inhibition circuits '' (Anton et al 1993;Chen et al 2000;Kirillova and Lin 1998;Nakanishi 1995;Woolf et al 1991;Isaacson and Strowbridge 1998).…”

Section: Reciprocal Innervationmentioning

confidence: 99%

“…This type of synaptic relationship has been described in both the central and peripheral nervous systems. Reciprocal synapses are common in the brain (Famiglietti 1970;Guan et al 1995;Marcos et al 1996), retina (Harveit 1999;Dowling 1968), olfactory bulb (Kirillova and Lin 1998;Isaacson and Strowbridge 1998), autonomic nervous system (Kawai 1996;Yagamuchi et al 1975), carotid bulb (McDonald and Mitchell 1975;Matsumoto et al 1980), and vestibular macula (Ross 1997;Dunn 1980;Lysakowski and Goldberg 1997). In the organ of Corti, reciprocal synapses are characterized by the presence of both afferent and efferent types of synaptic membrane specializations between a single nerve ®ber and a hair cell (Nadol 1981).…”

Section: Introductionmentioning

confidence: 99%

Reciprocal Innervation of Outer Hair Cells in a Human Infant

Thiers

Burgess

Nadol

2002

JARO

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Reciprocal synapses are characterized by the presence of both afferent and efferent types of synaptic specializations between two cells. They have been described at the neural poles of outer hair cells (OHCs) in humans with advanced age and two monkey species. Our objective was to study the innervation of the OHCs and determine if reciprocal synapses were present in a young (8-month-old infant) human subject. We studied the synaptic and cytoplasmic morphology of 162 nerve terminals innervating 29 OHCs using serial section transmission electron microscopy. Seventy-six percent of all OHCs were innervated by terminals with reciprocal synapses. This prevalence increased from the ®rst toward the third row (p < 0.001), and 100% of OHCs in the third row demonstrated at least one reciprocal synapse. The prevalence of terminals with reciprocal synapses was higher in the human infant than in older human subjects and was very similar to what has been reported for the chimpanzee. Reciprocal synapses occur in suf®cient numbers to be physiologically signi®cant in primates. The nerve terminals were found to segregate into two groups on the basis of their cytoplasmic morphological characteristics: (1) vesicle-rich/neuro®lament-poor (VR/NP) and (2) vesicle-poor/neuro®lament-rich (VP/NR). All afferent and reciprocal terminals were of the VP/NR variety. The majority of the efferent terminals originated from VR/NP nerve ®bers (classical olivocochlear morphology), but 23.5% of the efferent terminals were VP/NR. The hypothesis that peripheral processes of type II spiral ganglion cells form classical afferent, reciprocal, and a number of purely presynaptic terminals on OHCs is discussed. The presence of different types of synaptic specializations on OHCs formed by nerve ®bers of the same type (VP/NR) suggests the existence of reciprocal neuronal circuits between OHCs sharing the dendritic arborization of a type II spiral ganglion cell.

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Differential distribution of ionotropic glutamate receptor subunits in the rat olfactory bulb

Montague

Greer

1999

J. Comp. Neurol.

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The localization of ionotropic glutamate receptor (GluR) subunits was examined in the rat olfactory bulb in a series of three experiments using antibodies to alpha-amino-3hydroxy-5-methylisoxazole-4-propionic acid (AMPA) receptor subunits: GluRl, GluR2/3, and GluR4; and kainate (KA) receptor subunits: GluR5/6/7. In the first experiment, the subcellular localization of GluR 1-7 was examined with light and electron microscopy in the adult rat olfactory bulb. The data demonstrate a highly specific laminar, cellular and subcellular distribution of ionotropic GluR subunits within the primary afferent and local synaptic circuits of the adult olfactory bulb. These results are consistent with the notion that the different roles subserved by glutamate in the olfactory bulb are actuated, in part, by a differential distribution of GluR subunits. In the second experiment, the developmental appearance of GluR 1-7 was studied in embryonic day 18, postnatal day 1, and postnatal day 6 rat olfactory bulbs. The data demonstrate a highly specific laminar and cellular distribution of ionotropic GluRs in the developing olfactory bulb. In addition, the results show a differential expression of several GluRs over the course of development, which may indicate an inductive role for glutamate during olfactory bulb development In the third study, I wished to establish whether the expression of ionotropic glutamate receptor subunits in the olfactory bulb was strongly regulated by afferent input. To do so, I examined the distribution of GluR 1-7 in rat pup olfactory bulbs deafferented by either naris Reproduced with permission of the copyright owner. Further reproduction prohibited without permission.occlusion or nerve transection. Although deafferented olfactory bulbs exhibited a significant decrease in tyrosine hydroxylase iramunoreactivity, there were no observable changes in the GluR staining patterns. These results suggest that the distribution of the ionotropic GluRs is independent of afferent glutamatergic input The stability of GluR distribution may provide a mechanism to ensure that glutamate appropriately influences specific post-synaptic cell populations and local synaptic circuits within the context of the normal turnover of the olfactory nerve throughout life.Reproduced with permission of the copyright owner. Further reproduction prohibited without permission.

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Olfactory Reciprocal Synapses: Dendritic Signaling in the CNS

Cited by 468 publications

References 48 publications

Organization of Ionotropic Glutamate Receptors at Dendrodendritic Synapses in the Rat Olfactory Bulb

Organization of Ionotropic Glutamate Receptors at Dendrodendritic Synapses in the Rat Olfactory Bulb

Reciprocal Innervation of Outer Hair Cells in a Human Infant

Differential distribution of ionotropic glutamate receptor subunits in the rat olfactory bulb

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