TY - JOUR
T1 - Coherent olfactory bulb gamma oscillations arise from coupling independent columnar oscillators
AU - Peace, Shane T.
AU - Johnson, Benjamin C.
AU - Werth, Jesse C.
AU - Li, Guoshi
AU - Kaiser, Martin E.
AU - Fukunaga, Izumi
AU - Schaefer, Andreas T.
AU - Molnar, Alyosha C.
AU - Cleland, Thomas A.
N1 - Publisher Copyright:
Copyright © 2024 The Authors. Licensed under Creative Commons Attribution CC-BY 4.0.
PY - 2024/3
Y1 - 2024/3
N2 - Spike timing-based representations of sensory information depend on embedded dynamical frameworks within neuronal networks that establish the rules of local computation and interareal communication. Here, we investigated the dynamical properties of olfactory bulb circuitry in mice of both sexes using microelectrode array recordings from slice and in vivo preparations. Neurochemical activation or optogenetic stimulation of sensory afferents evoked persistent gamma oscillations in the local field potential. These oscillations arose from slower, GABA(A) receptor-independent intracolumnar oscillators coupled by GABA(A)ergic synapses into a faster, broadly coherent network oscillation. Consistent with the theoretical properties of coupled-oscillator networks, the spatial extent of zero-phase coherence was bounded in slices by the reduced density of lateral interactions. The intact in vivo network, however, exhibited long-range lateral interactions that suffice in simulation to enable zero-phase gamma coherence across the olfactory bulb. The timing of action potentials in a subset of principal neurons was phase-constrained with respect to evoked gamma oscillations. Coupled-oscillator dynamics in olfactory bulb thereby enable a common clock, robust to biological heterogeneities, that is capable of supporting gamma-band spike synchronization and phase coding across the ensemble of activated principal neurons.
AB - Spike timing-based representations of sensory information depend on embedded dynamical frameworks within neuronal networks that establish the rules of local computation and interareal communication. Here, we investigated the dynamical properties of olfactory bulb circuitry in mice of both sexes using microelectrode array recordings from slice and in vivo preparations. Neurochemical activation or optogenetic stimulation of sensory afferents evoked persistent gamma oscillations in the local field potential. These oscillations arose from slower, GABA(A) receptor-independent intracolumnar oscillators coupled by GABA(A)ergic synapses into a faster, broadly coherent network oscillation. Consistent with the theoretical properties of coupled-oscillator networks, the spatial extent of zero-phase coherence was bounded in slices by the reduced density of lateral interactions. The intact in vivo network, however, exhibited long-range lateral interactions that suffice in simulation to enable zero-phase gamma coherence across the olfactory bulb. The timing of action potentials in a subset of principal neurons was phase-constrained with respect to evoked gamma oscillations. Coupled-oscillator dynamics in olfactory bulb thereby enable a common clock, robust to biological heterogeneities, that is capable of supporting gamma-band spike synchronization and phase coding across the ensemble of activated principal neurons.
KW - multielectrode arrays
KW - neural circuit
KW - optogenetics
KW - slice electrophysiology
KW - synchronization
UR - http://www.scopus.com/inward/record.url?scp=85186270211&partnerID=8YFLogxK
U2 - 10.1152/jn.00361.2023
DO - 10.1152/jn.00361.2023
M3 - Article
C2 - 38264784
AN - SCOPUS:85186270211
SN - 0022-3077
VL - 131
SP - 492
EP - 508
JO - Journal of Neurophysiology
JF - Journal of Neurophysiology
IS - 3
ER -