Routing of spike series by dynamic circuits in the hippocampus

authors: Frédéric Pouille, Massimo Scanziani
doi: 10.1038/nature02615

CITATION

Pouille, F., & Scanziani, M. (2004). Routing of spike series by dynamic circuits in the hippocampus. Nature, 429(6993), 717–723. https://doi.org/10.1038/nature02615

ABSTRACT

fleeting notes


highlights


It is believed that action potentials convey information through their timing and frequencyPage

We therefore investigated whether distinct temporal features of a series of spikes in CA1 pyramidal cells—the principal hippocampal output—are selectively captured by local neuronal circuitsPage

Recurrent inhibition was evoked by stimulating the axons of CA1 pyramidal cells at various frequencies with an electrode placed in the alveusPage

Specifically, alveus stimuli repeated at 0.2 Hz elicited recurrent inhibitory postsynaptic potentials (IPSPs) that were 25.3 ^ 1.8% smaller at the dendritic recording site than at the somatic onePage

with series of two to four stimuli at 100 HzPage

inhibition became progressively larger in the dendrites than in the somaPage

These results indicate that recurrent IPSPs elicited at low stimulation frequencies are predominantly generated by perisomatic conductancesPage

Furthermore, the amplitude of IPSCs recorded in the V-clamped soma progressively decreased with increasing stimulus numbePage

after the onset of a series of stimuli delivered to the alveus, recurrent inhibitory conductances subside in the pyramidal cell layer and build up in more distal regions.Page 2

stratum oriens that are therefore likely to receive recurrent excitation from CA1 pyramidal cellsPage 2

the probability of spiking was highest at the onset of the series and rapidly fell with subsequent stimuli (‘onset-transient’ interneurons;Page 2

second group (16 out of 49 cells) the probability of spike generation was lowest after the first stimulus and increased to a plateau between the third and tenth stimuli (‘late-persistent’ interneurons;Page 2

Spikes recorded in onset-transient interneurons showed very little variability in delay (‘jitter’; standard deviation, ^470ms; Fig. 3b), suggesting that they may operate as coincidence detectorsPage 2

strongly suggest that the onset of recurrent inhibition in the pyramidal cell layer and its subsequent shift to more distal regions result from the recruitment of distinct interneuron typesPage 3

fast EPSC kinetics and membrane time constants may be essential in reducing temporal summation of consecutive EPSPs in onset-transient interneurons1Page 4

slower EPSCs and membrane time constant observed in late-transient interneurons may prolong the time for effective summation of consecutive EPSPsPage 4

The disynaptic IPSP decreased the window for temporal summation of consecutive EPSPs (Fig. 5a, b). This effect was more marked at the beginning than at the end of a series of stimuliPage 5

disynaptic IPSPs repolarize the membrane shortly after the first EPSP and are thus likely to contribute to the transience of the response in onset-transient interneurons.Page 5

The inhibition/excitation ratio was computed as the gabazine-sensitive charge divided by the gabazine-resistant charge and was found to be 2.1 times larger in onset-transient than in latepersistent interneuronsPage 5

inhibition contributes to temporally segregating the activation of early-transient versus late-persistent interneurons by CA1 pyramidal cellsPage 6

interplay between four properties, namely: EPSC kinetics, the membrane time constant, short-term plasticity and disynaptic inhibition of interneuronsPage 6

coincidence detection and integrationPage 6

The coincidence-detection mode reports the onset of a spike series by activating perisomatic inhibitory conductances on pyramidal cellsPage 6

We therefore expect the wide range of temporal activity patterns characteristic of CA1 pyramidal cells during exploratory behaviour in rats29 to be represented as a spatially distinct inhibitory pattern across hippocampal layers.Page 6

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