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Amazon Drive Cloud storage from Amazon. Alexa Actionable Analytics for the Web. AmazonGlobal Ship Orders Internationally. Amazon Inspire Digital Educational Resources. Amazon Rapids Fun stories for kids on the go. Amazon Restaurants Food delivery from local restaurants. Changes in synaptic efficacy were estimated by using the EPSP amplitudes expressed as a percentage of the mean EPSP amplitude from either the total baseline or the 3 min baseline period immediately before each pairing episode.
Statistical significance was assessed using the Student's two-tailed t test and linear regression analysis. To compare the effectiveness of a single-spike pairing protocol at inducing LTP in hippocampal slices from juvenile and young adult mice, perforated patch-clamp recordings were made from visualized CA1 pyramidal neurons Fig. EPSP peak amplitudes were monitored in two pathways stimulated alternately every 5 sec.
The stimulation frequency was unaltered during the pairing. In hippocampal slices from juvenile mice P9-P14 , this single-spike pairing protocol was sufficient to induce input-specific LTP in the test pathway [EPSP amplitude measured 15 min after pairing: To investigate whether this apparent age-dependent difference in induction of LTP is robust against changes in recording mode or species, identical pairing protocols were performed with conventional whole-cell patch-clamp recordings in slices from juvenile PP15 and young adult rats PP Thus, the period of maturation of synaptic plasticity might last longer in rats than in mice, but we conclude that a developmental shift in induction requirement for associative LTP holds for both rats and mice and under conventional whole-cell as well as perforated patch-clamp recording conditions.
Developmental change in LTP induction in juvenile and young adult rats. The plot shows the EPSP amplitude monitored over time 6 responses averaged per minute expressed as a percentage of the mean amplitude before single-spike pairing, using whole-cell patch-clamp recordings. Single arrow heads indicate an episode of single-spike pairing; double arrow heads indicate an episode of burst pairing.
Peak EPSP amplitude was expressed as a percentage of a 3 min baseline period immediately before each pairing episode. Double exponential functions were fitted to the data robust fitting minimizing absolute deviations and are shown as dotted lines in the graphs.
EPSP amplitudes 6 responses averaged per minute expressed as a percentage of prepairing baseline period were monitored over time using whole-cell patch-clamp recordings. To analyze whether the change in induction rules is a gradual process or occurs abruptly during development, the amount of synaptic potentiation induced by these pairing protocols was compared over a range of different developmental ages in rats PP43 Fig.
The amount of potentiation induced by the single-spike pairing protocol varied considerably between experiments and within the same age group. Therefore, during maturation of the hippocampal network, there appears to be a gradual shift in the effectiveness of postsynaptic single spikes to induce input-specific synaptic potentiation such that by young adulthood, postsynaptic bursts become necessary.
We asked whether changes in membrane potential or width of the action potential during pairing episodes could explain the changes in synaptic plasticity that we observed. Although these data failed to show any correlation between the somatically recorded spike parameters during pairing and the observed shift in induction rules, developmental changes in the extent of dendritic back-propagation of action potentials cannot be excluded. In contrast to our findings during control conditions Fig.
We demonstrated here that there is a developmental shift in the effectiveness of a single-spike pairing protocol at inducing LTP in the CA1 subfield of hippocampus. The amount of synaptic potentiation induced by single-spike pairing correlates negatively with developmental age. Thus, in hippocampal slices from young rodents P9-P15 , repeated pairings of presynaptic stimuli with single postsynaptic action potentials are sufficient for LTP induction, whereas in older rodents PP43 , postsynaptic burst activity appears to be necessary to induce similar increases in synaptic efficacy.
Furthermore, in rat hippocampi from a range of developmental ages PP43 , the total synaptic potentiation after both single-spike and burst pairing was similar in the younger and older groups, and single-spike pairing was negatively correlated with any additional potentiation after burst-spike pairing. We also investigated whether an alteration in GABAergic inhibition could underlie this developmental change in induction rules, and report that under conditions of blocked GABA A receptor-mediated inhibition, a single-spike pairing protocol alone can induce LTP in the adult hippocampus.
This potentiation is comparable in magnitude to that observed in the young hippocampus, as well as to the total potentiation after burst pairing in the adult hippocampus under control conditions. STDP, whereby single presynaptic and postsynaptic action potentials are paired in a relative order within a narrow time window, has been observed in a variety of different preparations Paulsen and Sejnowski, ; Bi and Poo, Our findings in rodents up to 2 weeks of age are in agreement with these studies. However, our results show that as the hippocampus matures, single postsynaptic action potentials within this pairing protocol become progressively less effective at inducing LTP.
One study has reported the induction of LTP using presynaptic stimuli paired with single postsynaptic action potentials at 5 Hz in CA1 hippocampus of PP33 rats Nishiyama et al. Postsynaptic burst activity has been observed previously to be necessary for induction of LTP using a theta-frequency stimulation paradigm with both extracellular and microelectrode recordings in adult mouse and rat hippocampus in vitro , respectively Thomas et al. Our findings confirm and extend those data with whole-cell and perforated patch recordings by showing that for an STDP paradigm in the young adult hippocampus, postsynaptic burst activity is sufficient for synaptic plasticity when paired with single afferent stimuli; we also show that no change from the baseline frequency of presynaptic stimulation is required.
What is the cellular mechanism underlying the shift in induction requirement with developmental age? A developmental transition from a depolarizing to a hyperpolarizing effect of synaptic GABA A receptor activation has been reported in hippocampal circuitry during the first postnatal week Cherubini et al. In the ensuing postnatal weeks, fast GABA A receptor-mediated miniature IPSCs increase in frequency and decrease in both amplitude and decay time, with adult-level maturation of such kinetic IPSC properties reached by the third postnatal week, although more subtle changes in GABA A receptor-mediated responses to benzodiazepines still develop between adolescent and adult hippocampus Cohen et al.
Thus, the transition from a postsynaptic single-spike to burst-pairing protocol may be explained by a gradual maturation in GABA A receptor-mediated inhibition in the hippocampus, whereby greater postsynaptic depolarization is necessary for LTP induction in mature synapses. Although we did not detect any correlation with spike parameters as measured at the soma, there may still be differences in dendritic back-propagation of action potentials between juvenile and adult animals.
Because back-propagation of action potentials is under GABAergic inhibitory control Tsubokawa and Ross, , and back-propagating action potentials again can control dendritic GABAergic input Morishita and Alger, , there appears to be an intimate relationship between back-propagating action potentials, GABAergic inhibition, and synaptic plasticity. Maturational changes in any of these three factors might thus influence the computational properties of the network. What could be the function of such a developmental shift in induction rules for plasticity?
In the developing brain, correlated activity appears to be important in refining the synaptic connections in a neuronal network. However, in the adult brain, a more refined mechanism of induction of plasticity might be necessary to, for example, prevent random presynaptic and postsynaptic coincident activity from altering patterns of synaptic weights. One proposal is that burst activity plays a role that is different from that of single spiking during memory processing in hippocampal circuitry Paulsen and Moser, ; Pike et al.
In the adult hippocampus, complex spike burst activity is observed during certain behavioral states, including spatial exploration of an environment, when an animal is presumably learning about that environment O'Keefe, ; Buzsaki et al. Of interest, in vivo electrophysiological studies have reported a reduction in interneuron activity during experience of a novel location in spatial behavioral tasks, with the suggestion that such decreases in inhibition might relate to encoding of new information Wilson and McNaughton, ; Fyhn et al.
One could speculate that the switch in induction rules for LTP that we observe in the adult hippocampus during reduced GABA A receptor-mediated inhibition could reflect different encoding rules dependent on the state of the local hippocampal GABAergic network in which those synapses are being modified. In conclusion, in addition to the extensive changes in synaptic plasticity that occur in very early postnatal development Yasuda et al.
Thus, in the mature hippocampal network, it is not only the temporal order of synaptic activation but also the nature of the postsynaptic signal within the local network state that become of crucial importance for synaptic plasticity. Correspondence should be addressed to Dr. We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.
Skip to main content. Meredith , Anna M. Floyer-Lea and Ole Paulsen. Abstract The induction rules of synaptic plasticity are important for the functional operation of a neural network. Introduction The rules of synaptic plasticity are fundamental to the functional properties of a neural network.