High-Fidelity Transmission Acquired via a Developmental Decrease in NMDA Receptor Expression at an Auditory Synapse

Futai, Kensuke; Okada, Masayoshi; Matsuyama, Kiminori; Takahashi, Tomoyuki

doi:10.1523/jneurosci.21-10-03342.2001

Cited by 116 publications

(182 citation statements)

References 31 publications

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“…NMDAR contribute to auditory nerve responses during development (Zhou and Parks, 1992; Zhang and Trussell, 1994a,b;Futai et al, 2001;Joshi and Wang, 2002;Hoffpauir et al, 2006). In the chick vestibulocochlear nuclei, NMDAR emerge at E6, with functional synapses apparently generated at E7 (Sato and Momose-Sato, 2003).…”

Section: Nih-pa Author Manuscriptmentioning

confidence: 99%

“…Zhou and Parks (1992) provided pharmacological evidence of age-dependent decreases in NMDAR responses in the auditory neurons in chicks. Replacement of NMDAR by AMPA receptors in the auditory brainstem is correlated with the maturation of functional synapses in both mouse and chick (Kubke and Carr, 1998;Parks, 2000;Futai et al, 2001). …”

Section: Nih-pa Author Manuscriptmentioning

confidence: 99%

“…In rodent cortex, NR2B is highly expressed before birth and remains roughly constant into adulthood, whereas NR2A is expressed after birth and increases with age (Watanabe et al, 1992;Sheng et al, 1994;Wenzel et al, 1997). During postnatal development, NR2C is expressed at low levels in cortex but at high levels in cerebellum, whereas NR2D is expressed at high levels in brainstem of mice (Watanabe et al, 1992), rats (Wenzel et al, 1997), and zebra finches (Wada et al, 2004).NMDAR contribute to auditory nerve responses during development (Zhou and Parks, 1992; Zhang and Trussell, 1994a,b;Futai et al, 2001;Joshi and Wang, 2002;Hoffpauir et al, 2006). In the chick vestibulocochlear nuclei, NMDAR emerge at E6, with functional synapses apparently generated at E7 (Sato and Momose-Sato, 2003).…”

mentioning

confidence: 99%

“…Similarly, in the mouse, where the early postnatal developmental period corresponds to a late embryonic stage in chick (Kubke and Carr, 2000), synaptogenesis in the calyx of Held is marked by both AMPAand NMDAR-mediated currents (Hoffpauier et al, 2006). The mean amplitude of NMDA EPSCs in calicine terminals in the mouse medial nucleus of the trapezoid body (MNTB) decreases in a stepwise fashion between P5 and P13, whereas the mean amplitude of AMPA EPSCs increases steadily from P5 to P15 (Futai et al, 2001;Joshi and Wang, 2002;Youssoufian et al, 2005). 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).…”

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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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Section: Nih-pa Author Manuscriptmentioning

confidence: 99%

Section: Nih-pa Author Manuscriptmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Development of NMDA R1 expression in chicken auditory brainstem

Tang

Carr

2004

Hearing Research

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“…Similar properties of the small excitatory inputs were noted by Hamann et al Another criterion used to distinguish likely calyceal from noncalyceal inputs was those excitatory postsynaptic currents (EPSCs) Ͼ391 pA versus those Ͻ196 pA (after correcting for the difference in holding potential to Ϫ80 mV) (Barnes-Davies and Forsythe 1995;Forsythe and Barnes-Davies 1993a). Another group has used a higher cutoff value (Ͼ1 nA) (Futai et al 2001;Ishikawa et al 2003). However, when the excitatory inputs are stimulated by afferent fiber stimulation, the experimenter has no information about the morphology of the large input.…”

Section: Introductionmentioning

confidence: 99%

Multiple Large Inputs to Principal Cells in the Mouse Medial Nucleus of the Trapezoid Body

Bergsman¹,

Camilli²,

McCormick³

2004

Journal of Neurophysiology

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The calyx of Held is a giant nerve terminal that forms a synapse directly onto the principal cells of the medial nucleus of the trapezoid body (MNTB) in the mammalian auditory brain stem. This central synapse, which is involved in sound localization, has become widely used for studying synaptic transmission. Anatomical studies of this nucleus have indicated that each principal cell is innervated by only one calyx. Here we use previously established electrophysiological criteria of excitatory postsynaptic current amplitude, kinetics, and transmitter type, as well as other characteristics commonly reported for this synapse, to examine the input properties of principal neurons. Our findings indicate that some principal cells receive more than one strong excitatory input. These inputs meet previously established electrophysiological criteria for identification as calyceal nerve terminals. Implications for the execution and analysis of experiments to avoid errors due to such multiple inputs are discussed.

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Developmental increase in postsynaptic alpha-amino-3-hydroxy-5-methyl-4 isoxazolepropionic acid receptor compartmentalization at the calyx of held synapse

et al. 2006

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The pattern of expression of ionotropic glutamate receptor (GluR) subunits 1-4 in the medial nucleus of the trapezoid body (MNTB) has been reported to change during development. The aim of this study was to compare the distribution of the GluR1-4 subunits in the MNTB at postnatal day (P) 9, before high-frequency signal transmission in the auditory system has developed, with that observed in mature adult rats. GluR1-4 subunits were studied by preembedding and postembedding immunocytochemical methods. Increased levels of GluR1, 2/3, and 4 associated with development were evident only at postsynaptic sites of MNTB principal cell bodies receiving calyces of Held synapses, whereas receptor density at nonsynaptic sites was found to remain unaltered. Taken together, the expression pattern of GluR subunits and the density of immunoparticles in postsynaptic specializations are indicative of a compartmentalization of alpha-amino-3-hydroxy-5-methyl-4 isoxazolepropionic acid (AMPA) subunits upon development. These developmental changes provide a morphological basis for establishment of the postsynaptic properties needed for high-frequency synaptic transmission of auditory signals to MNTB principal neurons.

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High-Fidelity Transmission Acquired via a Developmental Decrease in NMDA Receptor Expression at an Auditory Synapse

Cited by 116 publications

References 31 publications

Development of NMDA R1 expression in chicken auditory brainstem

Development of NMDA R1 expression in chicken auditory brainstem

Multiple Large Inputs to Principal Cells in the Mouse Medial Nucleus of the Trapezoid Body

Developmental increase in postsynaptic alpha-amino-3-hydroxy-5-methyl-4 isoxazolepropionic acid receptor compartmentalization at the calyx of held synapse

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