TY - JOUR
T1 - Inhibition-Induced theta resonance in cortical circuits
AU - Stark, Eran
AU - Eichler, Ronny
AU - Roux, Lisa
AU - Fujisawa, Shigeyoshi
AU - Rotstein, Horacio G.
AU - Buzsáki, György
N1 - Funding Information:
We thank Kenji Mizuseki and Anton Sirota for insightful comments and Karl Deisseroth for providing the rAAV5-CaMKII::ChR2 virus. This study was supported by NIH NS034994 (to G.B.), NIH MH54671 (to G.B.), NS074015 (to G.B.), the Rothschild Foundation (to E.S.), the Human Frontiers in Science Project LT-000346/2009-L (to E.S.), the Machiah Foundation (to E.S.), NSF DMS-0817241 (to H.G.R.), and DMS-1313861 (to H.G.R.).
PY - 2013/12/4
Y1 - 2013/12/4
N2 - Both circuit and single-cell properties contribute to network rhythms. Invitro, pyramidal cells exhibit theta-band membrane potential (subthreshold) resonance, but whether and how subthreshold resonance translates into spiking resonance in freely behaving animals is unknown. Here, we used optogenetic activation to trigger spiking in pyramidal cells or parvalbumin immunoreactive interneurons (PV) in the hippocampus and neocortex of freely behaving rodents. Individual directly activated pyramidal cells exhibited narrow-band spiking centered on a wide range of frequencies. In contrast, PV photoactivation indirectly induced theta-band-limited, excess postinhibitory spiking in pyramidal cells (resonance). PV-inhibited pyramidal cells and interneurons spiked at PV-inhibition troughs, similar to CA1 cells during spontaneous theta oscillations. Pharmacological blockade of hyperpolarization-activated (Ih) currents abolished theta resonance. Inhibition-induced theta-band spiking was replicated in a pyramidal cell-interneuronmodel that included Ih. Thus, PV interneurons mediate pyramidal cell spiking resonance in intact cortical networks, favoring transmission at theta frequency.
AB - Both circuit and single-cell properties contribute to network rhythms. Invitro, pyramidal cells exhibit theta-band membrane potential (subthreshold) resonance, but whether and how subthreshold resonance translates into spiking resonance in freely behaving animals is unknown. Here, we used optogenetic activation to trigger spiking in pyramidal cells or parvalbumin immunoreactive interneurons (PV) in the hippocampus and neocortex of freely behaving rodents. Individual directly activated pyramidal cells exhibited narrow-band spiking centered on a wide range of frequencies. In contrast, PV photoactivation indirectly induced theta-band-limited, excess postinhibitory spiking in pyramidal cells (resonance). PV-inhibited pyramidal cells and interneurons spiked at PV-inhibition troughs, similar to CA1 cells during spontaneous theta oscillations. Pharmacological blockade of hyperpolarization-activated (Ih) currents abolished theta resonance. Inhibition-induced theta-band spiking was replicated in a pyramidal cell-interneuronmodel that included Ih. Thus, PV interneurons mediate pyramidal cell spiking resonance in intact cortical networks, favoring transmission at theta frequency.
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U2 - 10.1016/j.neuron.2013.09.033
DO - 10.1016/j.neuron.2013.09.033
M3 - Article
C2 - 24314731
AN - SCOPUS:84888875140
SN - 0896-6273
VL - 80
SP - 1263
EP - 1276
JO - Neuron
JF - Neuron
IS - 5
ER -