Dendritic spikes induce ripples in parvalbumin interneurons during hippocampal sharp waves.
Sharp-wave ripples are transient oscillatory events in the hippocampus that are associated with the reactivation of neuronal ensembles within specific circuits during memory formation. Fast-spiking, parvalbumin-expressing interneurons (FS-PV INs) are thought to provide fast integration in these oscillatory circuits by suppressing regenerative activity in their dendrites. Here, using fast 3D two-photon imaging and a caged glutamate, we challenge this classical view by demonstrating that FS-PV IN dendrites can generate propagating Ca(2+) spikes during sharp-wave ripples. The spikes originate from dendritic hot spots and are mediated dominantly by L-type Ca(2+) channels. Notably, Ca(2+) spikes were associated with intrinsically generated membrane potential oscillations. These oscillations required the activation of voltage-gated Na(+) channels, had the same frequency as the field potential oscillations associated with sharp-wave ripples, and controlled the phase of action potentials. Furthermore, our results demonstrate that the smallest functional unit that can generate ripple-frequency oscillations is a segment of a dendrite.
Two-Photon Imaging Center, Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest 1083, Hungary; Faculty of Information Technology and Bionics, Pázmány Péter Catholic University, Budapest 1083, Hungary.
Balázs
B
Chiovini
Two-Photon Imaging Center, Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest 1083, Hungary; Department of Neuroscience, Columbia University, New York, NY 10032, USA.
Gergely F
GF
Turi
Two-Photon Imaging Center, Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest 1083, Hungary.
Gergely
G
Katona
Two-Photon Imaging Center, Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest 1083, Hungary; Faculty of Information Technology and Bionics, Pázmány Péter Catholic University, Budapest 1083, Hungary.
Attila
A
Kaszás
Two-Photon Imaging Center, Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest 1083, Hungary; Faculty of Information Technology and Bionics, Pázmány Péter Catholic University, Budapest 1083, Hungary.
Dénes
D
Pálfi
Department of Atomic Physics, Budapest University of Technology and Economics, Budapest 1111, Hungary.
Pál
P
Maák
Two-Photon Imaging Center, Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest 1083, Hungary.
Gergely
G
Szalay
Faculty of Information Technology and Bionics, Pázmány Péter Catholic University, Budapest 1083, Hungary; Laboratory of Cerebral Cortex Research, Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest 1083, Hungary.
Mátyás Forián
MF
Szabó
Transgenic Facility, Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest 1083, Hungary.
Gábor
G
Szabó
Two-Photon Imaging Center, Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest 1083, Hungary.
Zoltán
Z
Szadai
Faculty of Information Technology and Bionics, Pázmány Péter Catholic University, Budapest 1083, Hungary; Laboratory of Cerebral Cortex Research, Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest 1083, Hungary.
Szabolcs
S
Káli
Two-Photon Imaging Center, Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest 1083, Hungary; Faculty of Information Technology and Bionics, Pázmány Péter Catholic University, Budapest 1083, Hungary. Electronic address: rozsabal@koki.hu.
Balázs
B
Rózsa
D000200:Action Potentials / Q000187:drug effects / Q000502:physiology*; D000818:Animals; D058256:Brain Waves / Q000187:drug effects / Q000502:physiology*; D002118:Calcium / Q000378:metabolism; D003712:Dendrites / Q000187:drug effects / Q000502:physiology*; D018698:Glutamic Acid / Q000494:pharmacology; D049452:Green Fluorescent Proteins / Q000235:genetics; D006624:Hippocampus / Q000166:cytology* / Q000502:physiology*; D021621:Imaging, Three-Dimensional; D066298:In Vitro Techniques; D007395:Interneurons / Q000166:cytology* / Q000187:drug effects / Q000378:metabolism; D008810:Mice, Inbred C57BL; D010320:Parvalbumins / Q000378:metabolism*; D010775:Photic Stimulation
D010320:Parvalbumins; C485184:enhanced green fluorescent protein; D049452:Green Fluorescent Proteins; D018698:Glutamic Acid; D002118:Calcium