Developmental changes in synaptic properties in hippocampus of neonatal rats

Michelet, Dominique; Oliver, Michael W.; Lynch, Gary

doi:10.1016/0165-3806(89)90063-1

Cited by 116 publications

(62 citation statements)

References 29 publications

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“…The EGABA in the PN2-5 neurones showed a strong dependence on the Cl-gradient and matched closely the EGABA predicted by the GHK equation at the given ionic conditions, indicating a GABA-mediated Clconductance. Thus, the previous findings of a lack of IPSPs (Mueller et al 1984;Janigro & Schwartzkroin, 1988;Chesnut & Swann, 1989) or GABAA-mediated inhibition (Dunwiddie, 1981;Harris & Teyler, 1983;Michelson & Lothman, 1989;Muller et at. 1989) in CAL neurones of the first postnatal week were probably due to a lower Cl-gradient, such that the EIPSP was so near the resting potential that the GABAA-mediated synaptic potentials were not apparent.…”

Section: Discussionmentioning

confidence: 80%

Development of GABA‐mediated, chloride‐dependent inhibition in CA1 pyramidal neurones of immature rat hippocampal slices.

Zhang

Spigelman

Carlen

1991

The Journal of Physiology

176

102

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SUMMARY1. y-Aminobutyric acid (GABA)-mediated, Cl--dependent inhibitory postsynaptic potentials (IPSPs) and GABA currents in immature rat hippocampal CAI neurones were studied using the whole-cell recording technique in brain slices.2. IPSPs evoked by electrical stimulation were observed in postnatal 2-to 5-(PN2-5), 8-to 13-(PN8-13) and 15-to 20-(PN15-20)day-old CAI neurones. In the presence of glutamate receptor blockers 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) and D-2-amino-5-phosphonovaleric acid (APV), the reversal potential for the IPSP (ElPSP) was near the resting membrane potential (RMP) in the PN2-5 neurones, but 13 and 25 mV more negative than the RMP in PN8-13 and PN15-20 neurones respectively. IPSPs and GABA currents were blocked by the GABAAreceptor antagonists bicuculline or picrotoxin.3. The reversal potential for somatic GABA currents (EGABA) was examined in the presence of tetrodotoxin (TTX). There was a strong dependence of the EGABA upon the patch pipette [Cl-] ([CI-]p), indicating that the GABA currents were mediated by a Cl-conductance. In PN2-5 neurones, EGABA agreed with the value predicted by the Goldman-Hodgkin-Katz equation at given concentrations of internal and external anions permeable through GABA-activated Cl-channels, whereas EGABA in older neurones was 8-18 mV more negative.4. Examination of the relations between EGABA, holding potential, [Cl-]p and resting conductance indicated that the membrane of the PN2-5 neurones was readily permeable to Cl-which followed a passive Donnan equilibrium. Passive distribution of Cl-played a decreasing role in PN8-13 neurones and in PN1S-20 neurones.5. To assess the contribution of outward Cl-co-transport, bath applications of high K+ or furosemide were performed. High K+ and furosemide caused a reversible positive shift of EGABA in PN15-20 neurones. Raising the temperature moved EGABA to a more negative potential, with a Qlo of 5 mV. A similar change of EGABA in response to high K+, but not to furosemide, was found in PN8-13 neurones.6. The present data indicate the existence of GABAA-mediated inhibitory synaptic connections in CAI neurones at the earliest stages of postnatal life. During the first postnatal week, Cl-ions are passively distributed and the EIPSP and EGABA NS 9102 L. ZHANG, I. SPIGELMAN AND P. L. CARLEN are near the RMP. After the first postnatal week, EIPSP and EGABA move to potentials more negative than the RMP, partly due to the gradual development of Cl-extrusion system(s), thereby maintaining a driving force for hyperpolarizing IPSPs at the resting potential in the more mature neurones.

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Section: Discussionmentioning

confidence: 80%

Development of GABA‐mediated, chloride‐dependent inhibition in CA1 pyramidal neurones of immature rat hippocampal slices.

Zhang

Spigelman

Carlen

1991

The Journal of Physiology

176

102

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“…In both experiments, spontaneous alternation was observed only in P30 animals; at younger ages, the subjects explored randomly. Second, the mechanisms for synaptic plasticity are present in the hippocampus, as in the visual cortex, during this postnatal period of behavioral impairment; potentiation in the hippocampus reaches or exceeds adult levels by P15 (Harris and Teyler, 1984;Muller et al, 1989;Bekenstein and Lothman, 1991). In the current study, adult-like LTP was observed in control animals at the youngest age (P16; Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Spontaneous alternation, like other behaviors that seem to require hippocampal f unction in adult rats, emerges after ϳ3 weeks of age (Douglas, 1975;Moye and Rudy, 1985;Castro et al, 1987;Rudy et al, 1987;Green and Stanton, 1989;Randall, 1992, 1995;Rudy, 1993;Rudy and Morledge, 1994). Much of hippocampal synaptogenesis occurs postnatally (Crain et al, 1973;Stirling and Bliss, 1978;Bayer, 1980;Amaral and Dent, 1981;Baudry et al, 1981;Amaral and Kurz, 1985), and hippocampal synapses exhibit plasticity before the emergence of mature behavioral function (Harris and Teyler, 1984;Muller et al, 1989;Bekenstein and Lothman, 1991). It is the maturation of these anatomical and physiological properties that is thought to underlie the emergence of adult-like behavior (Dumas and Foster, 1995).…”

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confidence: 99%

Insensitivity of the Hippocampus to Environmental Stimulation during Postnatal Development

1997

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Development of cortical sensory systems is influenced by environmental experience during "sensitive periods," before onset of behavioral function. During these periods, synaptic plasticity is observed, and neuronal function shows increased responsiveness to environmental stimulation. Because the hippocampus is late to develop, and because it demonstrates synaptic plasticity before the onset of behavioral function, this experiment was designed to determine whether, like the sensory cortices, the hippocampus undergoes a period of enhanced responsiveness to the environment. Rats at three ages [postnatal day 16 (P16), P23, and P30] were tested on a hippocampally dependent task, spontaneous alternation, and exposed to a novel environment. They were then killed and processed for immunocytochemistry to Fos or for in vitro electrophysiology in hippocampal area CA1. Age-matched control subjects were killed immediately after removal from the home cage. Spontaneous alternation was only observed in the oldest (P30) animals. In these same animals, the environmental manipulation resulted in an increase in Fos-like immunoreactivity (FL-IR), relative to controls, and a decrease in the ability to induce long-term potentiation (LTP). In P16 and P23 animals, the environmental manipulation resulted in no differences in hippocampal FL-IR or LTP. These results suggest that, rather than showing increased responsiveness to the environment at these ages, the hippocampus is environmentally insensitive and that it is isolated from the effects of environmental stimuli. The hippocampus, a neural region important for higher cognitive function, may develop via a mechanism different from those observed in the primary sensory cortices.

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“…LTP in the hippocampus, however, may behave differently. Previous reports have indicated that hippocampal LTP is either difficult to generate (Harris and Teyler 1984;Muller et al 1989) or not possible (Dudek and Bear 1993;Bolshakov and Siegelbaum 1995) in rats <8 days old.…”

Section: Introductionmentioning

confidence: 99%

Deficiency in induction but not expression of LTP in hippocampal slices from young rats.

Liao¹,

Malinow²

1996

Learning & Memory

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In this study we examine developmental changes between postnatal day (PND) 4 and 14 in synaptic transmission and plasticity in the CA1 region of hippocampal slices. We confirm previous results that tetanus-induced long-term potentiation (LTP) in field recordings is diminished in slices from younger animals. LTP in whole-cell current-clamp recordings is also diminished in younger animals. However, robust LTP can be induced in young animals if sufficient postsynaptic depolarization is provided during LTP induction. Furthermore, we find differences in synaptic transmission between PND 4 and 14, suggesting that the depolarization during tetanic stimulation in young tissue is ineffective to produce LTP. These results indicate that the smaller potentiation in field recordings in slices from younger animals is attributable to insufficient postsynaptic depolarization during LTP induction rather than a defect in expression mechanisms.

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Developmental changes in synaptic properties in hippocampus of neonatal rats

Cited by 116 publications

References 29 publications

Development of GABA‐mediated, chloride‐dependent inhibition in CA1 pyramidal neurones of immature rat hippocampal slices.

Development of GABA‐mediated, chloride‐dependent inhibition in CA1 pyramidal neurones of immature rat hippocampal slices.

Insensitivity of the Hippocampus to Environmental Stimulation during Postnatal Development

Deficiency in induction but not expression of LTP in hippocampal slices from young rats.

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