Coherent olfactory bulb gamma oscillations arise from coupling independent columnar oscillators

Abstract

Spike timing-based representations of sensory information depend on embedded dynamical frameworks within neural structures that establish the rules of local computation and interareal communication. Here, we investigated the dynamical properties of mouse olfactory bulb circuitry. Neurochemical activation or optogenetic stimulation of sensory afferents evoked persistent (minutes) 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, exhibits long-range lateral interactions theoretically sufficient to enable zero-phase coherence across the complete network. These coupled-oscillator dynamics thereby establish a common clock, robust to biological heterogeneities, that is capable of supporting gamma-band phase coding across the spiking output of olfactory bulb principal neurons.

A coupled-oscillator model of olfactory bulb gamma oscillations

“…The present model is based on our earlier two-layer model of cholinergic neuromodulation in the OB [ 25 ], but embeds these glomerular layer and intercolumnar EPL computations within an explicit spatial framework. The results from this model favor the PRING mechanism described above [ 35 ], and demonstrate that this inhibition-coupled cellular oscillator architecture supports the diverse phenomena observed in OB neurophysiological recordings. These phenomena include (1) patterned spiking activity in MCs and GCs that both is broadly heterogeneous and occurs at lower frequencies than the population rhythm, (2) tolerance to a wide range of afferent MC excitation levels, which is important for mediating the representation of different odor qualities, (3) tolerance for substantial changes in MC-GC synaptic weights, which underlie intrinsic odor learning within the OB [ 47 – 49 ], (4) the broad coherence of gamma-band oscillations across a physically extensive network despite the incoherent activity of some neurons within that network, (5) the phase-constraining of spikes within each cycle of the gamma oscillation [ 10 , 13 ], and (6) the persistence of LFP gamma oscillations at consistent frequencies despite sparse network connectivity (connection probability p = 0.3 between MCs and GCs) and sharply heterogeneous afferent activation levels.…”

“…However, this model required substantially higher-frequency MC STOs than have been experimentally described, and also was not clearly compatible with the sparse spiking behavior of GCs [ 34 ]. Fourth, a hybrid network based on inhibition-coupled intrinsic cellular oscillators has been proposed [ 35 ], in which the intrinsic STOs of MCs are transiently coupled during afferent activation into a coherent oscillatory network [ 36 ] paced by GC-mediated inhibitory synaptic inputs that periodically reset the slower MC STOs. (Pulsed inhibitory inputs, including shunting inhibition, have been demonstrated to effectively reset MC STOs [ 28 , 37 – 39 ]).…”

Rapid online learning and robust recall in a neuromorphic olfactory circuit

“…That is, individual odor presentations ("sniffs") comprised steady-state feature vectors in which the pattern of amplitudes across vector elements reflected odor quality as well as sampling error arising from plume turbulence. 6 The EPL network is intrinsically oscillogenic in the gamma band (30-80 Hz) 17,35 , and MC action potentials are statistically phase-constrained with respect to these local oscillations 16,18 .…”

Presynaptic NMDA receptors cooperate with local action potentials to implement activity-dependent GABA release from the reciprocal olfactory bulb granule cell spine

“…This mechanism will allow GC-mediated lateral inhibition to participate in synthesizing the olfactory percept at the level of the bulb from the individual olfactory receptor channels, most likely via synchronization in the gamma band (e.g. Laurent et al 1996, Kashiwadani et al 1999, Schoppa 2006, Brea et al 2009, Li et al 2015, Peace et al 2017, while at the same time preventing unnecessary energy expenditure and unwanted inhibition of other glomerular columns (i.e. if GABA release would happen from all spines of an activated GC).…”