Developmental changes in EPSC quantal size and quantal content at a central glutamatergic synapse in rat

Bellingham, Mark C.; Lim, Rebecca; Walmsley, Bruce

doi:10.1111/j.1469-7793.1998.861bg.x

Cited by 104 publications

(108 citation statements)

References 37 publications

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“…Our results are partially consistent with previous reports studying developmental plasticity of the calyx-type synapse in rat (Bellingham et al 1998;Chuhma & Ohmori, 1998;Taschenberger & von Gersdorff, 2000;Iwasaki & Takahashi, 2001).…”

Section: Discussionsupporting

confidence: 83%

“…Similar to what we have described, it has been reported that AMPAR-EPSCs show an age-dependent increase in amplitude at both the rat calyx of Held (Chuhma & Ohmori, 1998) and the endbulb of the Held synapse (Bellingham et al 1998). The former study attributed this increase to an upregulation of presynaptic voltage-gated Ca 2+ channels and release probability, whereas the latter suggested a postsynaptic increase in synaptic conductance.…”

Section: Discussionsupporting

confidence: 67%

“…Unlike previous studies showing a gradual decrease in NMDAR-EPSC amplitude at calyx-type synapses (Bellingham et al 1998;Taschenberger & von Gersdorff, 2000), we have shown that there are relatively more NMDARs than AMPARs at P3/4 and that this ratio reverses after presynaptic terminals have made contact with their postsynaptic targets after P5/6 (Fig. 3).…”

Section: Discussioncontrasting

confidence: 51%

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Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem

Joshi

Wang

2002

J Physiology

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Using whole-cell recordings from presynaptic terminals and postsynaptic principal neurons in the mouse medial nucleus of the trapezoid body (MNTB), we have characterized properties of the calyx of Held synapse during the first three postnatal weeks. We observed that evoked excitatory postsynaptic currents (EPSCs) mediated by NMDA receptors (NMDAR) increased until postnatal day 11/12 (P11/12) after which they declined to very low or undetectable levels at P16. Meanwhile, EPSCs mediated by AMPA receptors (AMPAR) showed an approximate three-fold increase in amplitude. These changes were paralleled by NMDAR and AMPAR currents evoked by exogenous NMDA and kainate to MNTB neurons except that whole-cell kainate currents remained constant after P7/8 while AMPAR-EPSCs continued to increase. We found that the decay time constant t for NMDAR-EPSCs and AMPAR-EPSCs declined by about 30 % and 70 %, respectively. Analyses of NMDAR-EPSCs with subunit-specific pharmacological agents including ifenprodil, N,N,N‚,N‚-tetrakis(2-pyridylmethyl)-ethylenediamine (TPEN), zinc and Mg 2+ revealed subtle developmental changes in subunit composition. As maturation progressed, this synapse displayed a reduction in the number of presynaptic spike failures and the extent of synaptic depression in response to trains of stimuli (50-300 Hz) while the recovery rate from depression accelerated. These results demonstrate profound changes in the size and kinetics of postsynaptic glutamate receptors and in the spike-firing capability of presynaptic terminals at the calyx of Held-MNTB synapse during early development. We suggest that these concurrent presynaptic and postsynaptic adaptations represent important steps for synapse consolidation and refinement and ultimately for the development of fast high-fidelity transmission at this synapse. synaptic properties of the mouse calyx of Held-MNTB synapse within the first three postnatal weeks. We found that synaptic NMDARs were present only transiently within the first 2 weeks, and exhibited a unique developmental profile. Although synaptic AMPARs exhibited a nearly linear growth in density over the same period, the total population of functional AMPARs (i.e. whole-cell kainate currents) reached a maximum by the end of the first postnatal week. We suggest that these changes, along with concurrent alterations in kinetic properties of EPSCs and in synaptic depression and recovery, contribute significantly to the development of high-fidelity synaptic transmission at this synapse. Part of this study had been previously published in abstract form (Joshi & Wang, 2000). METHODS Slice preparationMice were housed in the facility certified by the Canadian Council of Animal Care and used for this study according to a protocol approved by the Hospital for Sick Children Animal Care Committee. Brainstem slices were prepared from P3-P18 mice (CD1/C57 black) as previously described (Forsythe & BarnesDavis, 1993). Mice were decapitated with a small guillotine and brains were rapidly dissected and immersed in ice-cold artif...

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Section: Discussionsupporting

confidence: 83%

Section: Discussionsupporting

confidence: 67%

Section: Discussioncontrasting

confidence: 51%

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Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem

Joshi

Wang

2002

J Physiology

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“…From 2 to 3 weeks of age, a decrease in average EPSP halfwidth from 0.78 to 0.55 ms is temporally correlated with a nearly fourfold increase in I K(LVA) . One possible mechanism underlying this change in EPSP duration is an acceleration in AMPA receptor kinetics, which has been described in studies of other auditory brainstem synapses (Bellingham et al, 1998;Lawrence and Trussell, 2000;Taschenberger and von Gersdorff, 2000;Joshi et al, 2004;MacLeod and Carr, 2005). However, this issue has not yet been addressed in the MSO.…”

Section: Properties and Developmental Regulation Of I K(lva) In Mso Pmentioning

confidence: 90%

Posthearing Developmental Refinement of Temporal Processing in Principal Neurons of the Medial Superior Olive

Scott¹,

Mathews²,

Golding³

2005

J. Neurosci.

161

229

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In mammals, principal neurons of the medial superior olive (MSO) exhibit biophysical specializations that enable them to detect soundlocalization cues with microsecond precision. In the present study, we used whole-cell patch recordings to examine the development of the intrinsic electrical properties of these neurons in brainstem slices from postnatal day 14 (P14) to P38 gerbils. In the week after hearing onset (P14 -P21), we observed dramatic reductions in somatic EPSP duration, input resistance, and membrane time constant. Surprisingly, somatically recorded action potentials also dramatically declined in amplitude over a similar period (38 Ϯ 3 to 17 Ϯ 2 mV; ϭ 5.2 d). Simultaneous somatic and dendritic patch recordings revealed that these action potentials were initiated in the axon, which primarily emerged from the soma. In older gerbils, the rapid speed of membrane voltage changes and the attenuation of action potential amplitudes were mediated extensively by low voltage-activated potassium channels containing the Kv1.1 subunit. In addition, whole-cell voltage-clamp recordings revealed that these potassium channels increase nearly fourfold from P14 to P23 and are thus a major component of developmental changes in excitability. Finally, the electrophysiological features of principal neurons of the medial nucleus of the trapezoid body did not change after P14, indicating that posthearing regulation of intrinsic membrane properties is not a general feature of all time-coding auditory neurons. We suggest that the striking electrical segregation of the axon from the soma and dendrites of MSO principal neurons minimizes spike-induced distortion of synaptic potentials and thus preserves the accuracy of binaural comparisons.

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“…In rat MNTB, AMPA receptor-mediated EPSCs as well as quantal synaptic currents acquire progressively faster kinetics, whereas NMDAR-mediated EPSCs diminish with age, as indicated by a 50% reduction in mean amplitude and faster decay kinetics from P5 to P14 (Taschenberger and von Gersdorff, 2000). The mean conductance of both spontaneous and evoked NMDA-EPSCs in the endbulb-bushy cell synapse decreased by more than half between P4-11 and P12-22 (Isaacson and Walmsley, 1995;Bellingham et al, 1998). Thus in both MNTB and cochlear nucleus, AMPA-receptor-mediated evoked synaptic responses become larger and faster, and NMDAR-mediated EPSCs diminish with age.…”

Section: Glutamate Receptors In Mammalian and Avian Auditory Developmentmentioning

confidence: 99%

Development of NMDA R1 expression in chicken auditory brainstem

Tang

Carr

2004

Hearing Research

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N-methyl-D-aspartate (NMDA) receptor subunit-specific probes were used to characterize developmental changes in the distribution of excitatory amino acid receptors in the chicken's auditory brainstem nuclei. Although NR1 subunit expression does not change greatly during the development of the cochlear nuclei in the chicken Hear. , there are significant developmental changes in NR2 subunit expression. We used in situ hybridization against NR1, NR2A, NR2B, NR2C, and NR2D to compare NR1 and NR2 expression during development. All five NMDA subunits were expressed in the auditory brainstem before embryonic day (E) 10, when electrical activity and synaptic responses appear in the nucleus magnocellularis (NM) and the nucleus laminaris (NL). At this time, the dominant form of the receptor appeared to contain NR1 and NR2B. NR2A appeared to replace NR2B by E14, a time that coincides with synaptic refinement and evoked auditory responses. NR2C did not change greatly during auditory development, whereas NR2D increased from E10 and remained at fairly high levels into adulthood. Thus changes in NMDA NR2 receptor subunits may contribute to the development of auditory brainstem responses in the chick. Indexing termscochlear nucleus; magnocellularis; laminaris; angularis; tonotopic gradient Physiological studies have shown that the auditory system is characterized by fast, accurate encoding of auditory information (Warchol and Dallos, 1990; Zhang and Trussell, 1994a,b;Fukui and Ohmori, 2003). We have therefore investigated the distribution of subtypes of Nmethyl-D-aspartate (NMDA) receptors (NMDAR) in the brainstem auditory nuclei of the chicken to determine whether changes in receptors may reflect the development of specializations for temporal processing. NMDAR can contain two classes of subunits, NR1 and NR2 (A-D). The third class of subunits (NR3), containing NR3A and NR3B, is thought to act as modulators of the NMDAR (Ciabarra et al., 1995;Nishi et al., 2001; for review see Cull-Candy, 2001). A functional NMDAR appears to consist of two NR1 subunits and two or three NR2 subunits. NR1 is the fundamental subunit necessary for the NMDAR complex, and its expression is spatiotemporally ubiquitous compared with that of NR2 subunits in vertebrate brain (Watanabe et al., 1992;Wada et al., 2004).Changes in NMDAR composition characterize the development of forebrain circuits. NR2B has been shown to be necessary for synapse formation and plasticity (Tang et al., 1999;Slutsky et al., 2004), whereas NR2A expression is associated with synaptic maturation (Fu et al., 2005). NMDAR made up of NR2B and NR1 subunits are the dominant form during NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript the "critical period" window for plasticity in mouse visual cortex (Quinlan et al., 1999a) and barrel cortex ) and in vocal learning regions of songbirds (Basham et al., 1999;Singh et al., 2000;Ding and Perkel, 2004). Near the end of the critical period, there is a gradual increase in the contribution of NR2A subunits i...

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Developmental changes in EPSC quantal size and quantal content at a central glutamatergic synapse in rat

Cited by 104 publications

References 37 publications

Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem

Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem

Posthearing Developmental Refinement of Temporal Processing in Principal Neurons of the Medial Superior Olive

Development of NMDA R1 expression in chicken auditory brainstem

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