Enhanced activation of NMDA receptor responses at the immature retinogeniculate synapse

Ramoa, Ary S.; McCormick, David A.

doi:10.1523/jneurosci.14-04-02098.1994

Cited by 102 publications

(72 citation statements)

References 49 publications

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“…As a result, the ratio of NR2A:2B increases in most brain regions. This shift may underlie the functional differences between early and late NMDA receptors, with the latter displaying, inter alia, a reduced duration of excitatory postsynaptic responses (Tsumoto et a!., 1987;Carmignoto and Vicini, 1992;Hestrin, 1992;Ramoa and McCormick, 1994;Khazipov et al, 1995). The integration of the NR2A subunit into NMDA receptors appears to be necessary to meet the functional requirements of the mature circuitry.…”

Section: Rearrangement Of Nr Expression During Postnatal Developmentmentioning

confidence: 99%

NMDA Receptor Heterogeneity During Postnatal Development of the Rat Brain: Differential Expression of the NR2A, NR2B, and NR2C Subunit Proteins

Wenzel

Fritschy

Möhler

et al. 1997

Journal of Neurochemistry

406

254

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Abstract:Changes in the expression of the NMDA receptor subunits (NRs) NR2A, 2B, and 2C were investigated in histo blots of the developing rat brain with subunitspecific antisera. At birth, the NR2B subunit was detected almost ubiquitously, the NR2A subunit staining was faint and restricted to the hippocampus, cerebral cortex, and striatum, and no NR2C subunit immunoreactivity was detected. During the first 3 postnatal weeks, the NR2B subunit became confined to forebrain structures, whereas the NR2A immunoreactivity became abundantly expressed throughout the brain. The NR2C immunoreactivity emerged 5 days after birth in the olfactory bulb, thalamus, and vestibular nuclei and became very intense after 10 days in cerebellar granule cells, its primary site of expression in adulthood. After 3 weeks, NR2A and NR2B immunoreactivity decreased to adult levels, whereas NR2C immunoreactivity remained unchanged. The patterns of distribution of the subunit proteins were in agreement with those of their corresponding mRNAs, as monitored by in situ hybridization histochemistry, although the mRNA translation appeared to be delayed by several days in certain areas. Our results reveal a progressive increase in the heterogeneity of NMDA receptors due to the comparably late onset of NR2A and NR2C subunit expression and by the area-specific rearrangement of NR2B subunit expression following birth. Key Words: NMDA receptor -Subunit -specific antisera -DevelopjiientHisto blots-Rat. J. Neurochem. 68, 469-478 (1997).N-Methyl-D-aspartate (NMDA) receptors are glutamate-activated cation channels, characterized by a high Ca 2~INa~permeability ratio, a voltage-dependent Mg 2+ block, a requirement for glycine as coagonist, and slow activation and deactivation kinetics (Nowak et al

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Section: Rearrangement Of Nr Expression During Postnatal Developmentmentioning

confidence: 99%

NMDA Receptor Heterogeneity During Postnatal Development of the Rat Brain: Differential Expression of the NR2A, NR2B, and NR2C Subunit Proteins

Wenzel

Fritschy

Möhler

et al. 1997

Journal of Neurochemistry

406

254

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“…The presence of IPSPs at such an early postnatal age is in agreement with previous electrophysiological and anatomical investigations. In fact: (1) optic tract-evoked inhibitory interactions between cat dLGN neurons in vitro have been detected 6 d before birth (Shatz and Kirkwood, 1984); (2) medial thalamus-evoked I PSPs have been recorded from P1-P3 cat thalamic neurons in vivo (Thatcher and Purpura, 1973); (3) optic tract-evoked I PSPs have been observed as early as P7-P9 (White and Sur, 1992) in ferret dLGN neurons in vitro (but see Ramoa and McCormick, 1994b); and (4) GABA A receptor-mediated currents have been recorded at P5 in rat somatosensory thalamic neurons (Oh et al, 1995). Furthermore, glutamic acid decarboxylase (Shotwell et al, 1986) and GABA (Kalil et al, 1985) immunoreactivity has been observed in the cat dLGN at embryonic day 49 and by the first postnatal week, respectively.…”

Section: Spontaneous Synaptic Activitymentioning

confidence: 99%

Postnatal Development of Membrane Properties and δ Oscillations in Thalamocortical Neurons of the Cat Dorsal Lateral Geniculate Nucleus

et al. 1997

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The development of membrane properties, firing patterns, and ␦ oscillations in neurons of the cat dorsal lateral geniculate nucleus (dLGN) was investigated in vitro during the first 7 postnatal weeks. Compared with adult neurons, the resting membrane potential was more depolarized at postnatal days 1-9 (P1-P9), the input resistance was higher at P1-P7, and action potentials had a higher threshold and a smaller amplitude at P1-P3 and a longer duration at P1-P9. At P1-P3 trains longer than 200 msec were rarely observed, and trains with more than three action potentials were only present in 41% of the neurons, whereas at P1-P7 the normalized slope of the instantaneous frequencies at the first five interspike intervals was smaller than in the adult. A long-lasting (up to 6 sec) afterhyperpolarization followed a short train of action potentials in 88 and 30% of neurons at P1-P3 and P30-P32, respectively, but it was rarely observed in the adult. The low-threshold Ca 2ϩ potential could evoke a burst of action potentials since P1.However, at P1-P7 the number of action potentials per burst was smaller (range, one to five), and at P1-P9 their maximum instantaneous frequency was lower (Ͻ190 Hz) than in the adult (range, six to eight, and 344 Hz, respectively). No ␦ oscillations were observed until P17, and their frequency (0.36 Hz) was lower than that in the adult (1.8 Hz). The percentage of neurons displaying ␦ oscillations and their frequency reached adult values by the end of the seventh postnatal week, i.e., well after the maturation of the membrane properties and firing patterns (second postnatal week). In conclusion, the maturation of the electrophysiological properties of thalamocortical neurons in the cat dLGN is completed later than the retinogeniculate axon segregation (Shatz CJ, 1983), and the immaturity of the oscillatory, and not of the burst-firing, activity is a limiting factor in the development of ␦ waves (Jouvet-Mounier et al., 1970).

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“…In addition, NMDA has been found to be a much more potent excitant for postnatal 5D rat Purkinje cells, and the response became less responsive with age; this was most dramatically seen between 14 and 21D rat neurones (Garthwaite et al 1987). The participation of NMDA receptors in retinogeniculate transmission at an immature ferret synapse activity was also enhanced during the first two postnatal weeks (Ramoa & McCormick, 1994). The NMDA responses in the visual cortex of kittens and immature rats were greater than those in adults (Carmignoto & Vicini, 1992).…”

Section: Nmda Responsesmentioning

confidence: 99%

Age‐related functional changes of the glutamate receptor channels in rat Meynert neurones

Akaike

Rhee

1997

The Journal of Physiology

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The developmental changes of glutamate receptors (GluRs) in acutely dissociated rat Meynert neurones were investigated using the conventional whole‐cell and nystatin perforated patch recording modes under voltage‐clamp conditions. The neurones became less responsive to N‐methyl‐d‐aspartic acid (NMDA) with age, most dramatically between 1 day and 2 weeks, while the responses to kainic acid (KA) and l‐α‐amino‐3‐hydroxy‐5‐methyl‐4‐isoxazolepropionic acid (AMPA) gradually increased. The metabotropic GluR response appeared a few days after birth, but thereafter no further change was observed. The decrease in the NMDA response during postnatal development was due to an abrupt reduction in the number of receptors without affecting the affinity, voltage‐dependent Mg2+ blockade or high Ca2+ permeability (Pca/PCs≈ 7.0). P ca/PCs in the presence of KA decreased from 2.8 in the 1‐day‐old (1D) rat neurones to 1.1 and 0.44 in the 2‐week‐old (2W) and 6‐month‐old (6M) rat neurones, respectively. The concentration–response relationship for KA shifted to the left with age. The KA response was not affected by NS‐102, a KA‐selective antagonist, thus indicating that the increased affinity of the receptor for the ligand resulted from the change in the AMPA receptor channel subunits. The AMPA response in the presence of 10−4 M cyclothiazide showed a change in the inward rectifying current–voltage relationship with age. The KA response was strongly cross‐desensitized by the addition of AMPA and was also blocked by 6‐cyano‐7‐nitroquinoxaline‐2,3‐dione (CNQX), whereas a rapid desensitization of the AMPA response was removed in a concentration‐dependent manner by cyclothiazide. These results indicate that the non‐NMDA receptor channels are assembled from the subunits of the AMPA receptor family without the GluR‐2 subunit, thus resulting in a high Ca2+ permeability. The l‐glutamate (Glu)‐induced responses were more sensitive to dl‐2‐amino‐5‐phosphonopentanoic acid (APV) in the 1D rat neurones than in the adult rat neurones. Both NMDA and KA raised the intracellular Ca2+ concentration ([Ca2+]i) in all neurones of 1D, 2W and 6M rats, though the charybdotoxin‐sensitive Ca2+‐activated K+ current (IK(ca)) did not appear in the 1D rat neurones. An age‐related prolongation of both IK(Ca) decay and [Ca2+]i clearance was also seen after the removal of KA. It was thus concluded that the age‐related changes of ionotropic receptors appear to play a key role in the activities of immature and mature rat Meynert cholinergic neurones. The KA‐induced IK(Ca), which developed with ageing, may thus function as one of the negative feedback systems, and thereby prevent excess cell excitation and neural damage, especially in adult rats.

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Enhanced activation of NMDA receptor responses at the immature retinogeniculate synapse

Cited by 102 publications

References 49 publications

NMDA Receptor Heterogeneity During Postnatal Development of the Rat Brain: Differential Expression of the NR2A, NR2B, and NR2C Subunit Proteins

NMDA Receptor Heterogeneity During Postnatal Development of the Rat Brain: Differential Expression of the NR2A, NR2B, and NR2C Subunit Proteins

Postnatal Development of Membrane Properties and δ Oscillations in Thalamocortical Neurons of the Cat Dorsal Lateral Geniculate Nucleus

Age‐related functional changes of the glutamate receptor channels in rat Meynert neurones

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