Developmental Changes in Release Properties of the CA3-CA1 Glutamate Synapse in Rat Hippocampus

Abstract

Wasling, P., E. Hanse, and B. Gustafsson. Developmental changes in release properties of the CA3-CA1 glutamate synapse in rat hippocampus. J Neurophysiol 92: 2714 -2724, 2004; 10.1152/jn.00464. 2004. Developmental changes in release probability (P r ) and pairedpulse plasticity at CA3-CA1 glutamate synapses in hippocampal slices of neonatal rats were examined using field excitatory postsynaptic potential (EPSP) recordings. Paired-pulse facilitation (PPF) at these synapses was, on average, absent in the first postnatal week but emerged and became successively larger during the second postnatal week. This developmental increase in PPF was associated with a reduction in P r , as indicated by the slower progressive block of the N-methyl-D-aspartate (NMDA) EPSP by the noncompetitive NMDA receptor antagonist MK-801. This developmental reduction in P r was not homogenous among the synapses. As shown by the MK-801 analysis, the P r heterogeneity observed among adult CA3-CA1 synapses is present already during the first postnatal week, and the developmental P r reduction was found to be largely selective for synapses with higher P r values, leaving P r of the vast majority of the synapses essentially unaffected. A reduction in P ves , the release probability of the individual vesicle, possibly caused by reduction in Ca 2ϩ influx, seems to explain the reduction in P r . In vivo injection of tetanus toxin at the end of the first postnatal week did not prevent the increase in PPF, indicating that this developmental change in release is not critically dependent on normal neural activity during the second postnatal week. I N T R O D U C T I O NFollowing their formation, synapses undergo various collective changes, commonly referred to as synaptic maturation. One salient example of such maturation is a developmental decrease in release probability to a single action potential (P r ). This decrease in P r has been documented among glutamate synapses in several regions, including the developing neocortex (Kumar and Huguenard 2001; Reyes and Sakmann 1999), calyx of Held (Iwasaki and Takahashi 2001; Taschenberger et al. 2002), striatum (Choi and Lovinger 1997), and hippocampus (Bolshakov and Siegelbaum 1995; but see Hsia et al. 1998;Muller et al. 1989), suggesting that it represents an essential step in the maturation of the glutamate synapse. In the striatum, patterned neural activity supports the induction of a long-term depression (LTD) that is expressed as a decrease in P r (Choi and Lovinger 1997), suggesting that neural activity may underlie this form of maturation. However, whether inhibition of neural activity or of LTD during a critical period interferes with the maturation of P r has never been directly tested.Studies of hippocampal CA3-CA1 glutamate synapses have shown a considerable P r heterogeneity among the mature synapses (Hessler et al. 1993;Huang and Stevens 1997). During the first postnatal week, however, the synapse population has been described both to have a uniformly high P r (Bolshakov and Siegelbaum 1995)...

Developmentally Regulated Actions of Alcohol on Hippocampal Glutamatergic Transmission

“…7 A, B). This finding indicates that the probability of glutamate release at CA3 pyramidal neurons is lower in juvenile rats, which is in general agreement with some studies of glutamatergic synaptic transmission at developing CA3-CA1 synapses (Bolshakov and Siegelbaum, 1995;Wasling et al, 2004) (but see Hsia et al, 1998). Figure 7A 1 shows the effect of 50 mM ethanol on paired-pulse plasticity in a P5 neuron.…”

Developmental Switch in Synaptic Mechanisms of Hippocampal Metabotropic Glutamate Receptor-Dependent Long-Term Depression

“…Nascent synapses are characterized by high presynaptic release probability and few postsynaptic AMPA receptors (AMPARs). Synapse maturation is accompanied by the acquisition of AMPARs and decreases in neurotransmitter release probability (Bolshakov and Siegelbaum, 1995;Pouzat and Hestrin, 1997;Liao et al, 1999;Petralia et al, 1999;Reyes and Sakmann, 1999;Pickard et al, 2000;Wasling et al, 2004) (but see Dumas and Foster, 1995;Hsia et al, 1998). For developing synapses to remain plastic over the course of synapse maturation, plasticity mechanisms must adapt with these changing synaptic properties.…”

Responses of excitatory hippocampal synapses to natural stimulus patterns reveal a decrease in short‐term facilitation and increase in short‐term depression during postnatal development

“…Previous studies have shown that the amount of paired-pulse facilitation in the hippocampus increases during postnatal weeks one and two (Muller et al, 1989;Bolshakov and Siegelbaum, 1995;Wasling et al, 2004), and then subsequently decreases during later neonatal development Foster, 1995, 1997;Dumas and Foster, 1998a,b; but see Hsia et al, 1998). It is not known whether developmental changes also occur in other forms of short-term plasticity, such as short-term high frequency depression.…”