Developmental increase in CA3-CA1 presynaptic function in the hippocampal slice

Abstract

1. We recorded extracellular and intracellular CA3-CA1 synaptic responses in hippocampal slices from neonatal rats [postnatal day (P) 15-21 and P29-35]. Presynaptic function was examined by measuring input-output relationships and paired-pulse facilitation and by quantal analysis of minimally evoked responses. 2. Extracellular recording revealed no difference in excitatory postsynaptic potential (EPSP) threshold or the fiber potential response for a given stimulus intensity between the two age groups. However, the slope of the field EPSP was consistently larger in older animals. The increase in EPSP slope was associated with a decrease in paired-pulse facilitation, suggesting an increase in presynaptic function with postnatal development. 3. Extracellular results were confirmed by intracellular recordings that revealed no difference in the minimal stimulation intensity needed to evoke a response, an increase in mean EPSP amplitude with development, and a decrease in paired-pulse facilitation. Quantal parameters were extracted by three separate methods including method of failures, coefficient of variance, and parameter optimization through noise deconvolution. All methods supported presynaptic mediation of facilitation. Comparison of quantal parameters during development indicated an increase in mean quantal content. 4. The results demonstrate that synaptic strength is altered over the course of development because of, at least in part, changes in presynaptic release mechanisms. Developmental differences in presynaptic function provide an explanation of differences in mechanisms for expression of long-term potentiation. The lower initial probability of transmitter release in neonates may permit increased presynaptic change.

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

“…A recent study described developmental decreases in P r at hippocampal synapses, as measured by PPF and the rate of MK801 blockade, but these changes occurred during an earlier developmental window (from P6 to P12) than our developmental switch . Other studies of P r later in hippocampal development (P15-P35) report an increase in P r or no change (Dumas and Foster, 1995;Hsia et al, 1998). We think that the greater DHPGinduced changes in PPF and rate of MK801 blockade at neonatal synapses represent a greater presynaptic contribution to the LTD compared with more mature synapses.…”

“…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.…”

Insensitivity of the Hippocampus to Environmental Stimulation during Postnatal Development

“…The behavioral manipulation, testing in the Y-maze and exposure to a novel environment, was sufficient to induce Fos expression in area CA1 and the subiculum of P30 animals, after the emergence of alternation behavior. Although the significance of these locations is unclear, it may be related to developmental changes at the CA3-CA1 synapse (Dumas and Foster, 1995). However, rather than an increase of Fos expression in the immature animals, a lack of staining was observed.…”

“…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). Therefore, the postnatal development of the hippocampus seems similar to that of the primary sensory cortices; it undergoes a period of synaptic plasticity before the emergence of mature behavioral function.…”

Gain and fidelity of transmission patterns at cortical excitatory unitary synapses improve spike encoding

“…However, a facilitation or depression without fluctuation was observed by activating population synapses (Manabe et al, 1993;Dumas and Foster, 1995) or using minimal stimuli (Stevens and Wang, 1995;Dobrunz and Stevens, 1997). The reasons for these differences need to be explored, because a complete understanding of such issues will tell us which configuration to record synaptic signals is more suitable for assessing synapse dynamics and plasticity.…”