TY - JOUR
T1 - Excitation and inhibition compete to control spiking during hippocampal ripples
T2 - Intracellular study in behaving mice
AU - English, Daniel F.
AU - Peyrache, Adrien
AU - Stark, Eran
AU - Roux, Lisa
AU - Vallentin, Daniela
AU - Long, Michael A.
AU - Buzsáki, György
N1 - Publisher Copyright:
©2014 the authors.
PY - 2014/12/3
Y1 - 2014/12/3
N2 - High-frequency ripple oscillations, observed most prominently in the hippocampal CA1 pyramidal layer, are associated with memory consolidation. The cellular and network mechanisms underlying the generation of the rhythm and the recruitment of spikes from pyramidal neurons are still poorly understood. Using intracellular, sharp electrode recordings in freely moving, drug-free mice, we observed consistent large depolarizations in CA1 pyramidal cells during sharp wave ripples, which are associated with ripple frequency fluctuation of the membrane potential (“intracellular ripple”). Despite consistent depolarization, often exceeding pre-ripple spike threshold values, current pulse-induced spikes were strongly suppressed, indicating that spiking was under the control of concurrent shunting inhibition. Ripple events were followed by a prominent afterhyperpolarization and spike suppression. Action potentials during and outside ripples were orthodromic, arguing against ectopic spike generation, which has been postulated by computational models of ripple generation. These findings indicate that dendritic excitation of pyramidal neurons during ripples is countered by shunting of the membrane and postripple silence is mediated by hyperpolarizing inhibition.
AB - High-frequency ripple oscillations, observed most prominently in the hippocampal CA1 pyramidal layer, are associated with memory consolidation. The cellular and network mechanisms underlying the generation of the rhythm and the recruitment of spikes from pyramidal neurons are still poorly understood. Using intracellular, sharp electrode recordings in freely moving, drug-free mice, we observed consistent large depolarizations in CA1 pyramidal cells during sharp wave ripples, which are associated with ripple frequency fluctuation of the membrane potential (“intracellular ripple”). Despite consistent depolarization, often exceeding pre-ripple spike threshold values, current pulse-induced spikes were strongly suppressed, indicating that spiking was under the control of concurrent shunting inhibition. Ripple events were followed by a prominent afterhyperpolarization and spike suppression. Action potentials during and outside ripples were orthodromic, arguing against ectopic spike generation, which has been postulated by computational models of ripple generation. These findings indicate that dendritic excitation of pyramidal neurons during ripples is countered by shunting of the membrane and postripple silence is mediated by hyperpolarizing inhibition.
KW - Action potential threshold
KW - Hippocampus
KW - Inhibition
KW - Intracellular in vivo recording
KW - Oscillations
KW - Sharp wave ripples
UR - http://www.scopus.com/inward/record.url?scp=84914689470&partnerID=8YFLogxK
U2 - 10.1523/JNEUROSCI.2600-14.2014
DO - 10.1523/JNEUROSCI.2600-14.2014
M3 - ???researchoutput.researchoutputtypes.contributiontojournal.article???
C2 - 25471587
AN - SCOPUS:84914689470
SN - 0270-6474
VL - 34
SP - 16509
EP - 16517
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 49
ER -