Learning improves decoding of odor identity with phase-referenced oscillations in the olfactory bulb

Abstract

Local field potential oscillations reflect temporally coordinated neuronal ensembles— coupling distant brain regions, gating processing windows, and providing a reference for spike timing-based codes. In phase amplitude coupling (PAC), the amplitude of the envelope of a faster oscillation is larger within a phase window of a slower carrier wave. Here, we characterized PAC, and the related theta phase-referenced high gamma and beta power (PRP), in the olfactory bulb of mice learning to discriminate odorants. PAC changes throughout learning, and odorant-elicited changes in PRP increase for rewarded and decrease for unrewarded odorants. Contextual odorant identity (is the odorant rewarded?) can be decoded from peak PRP in animals proficient in odorant discrimination, but not in naïve mice. As the animal learns to discriminate the odorants the dimensionality of PRP decreases. Therefore, modulation of phase-referenced chunking of information in the course of learning plays a role in early sensory processing in olfaction.SignificanceEarly processing of olfactory information takes place in circuits undergoing slow frequency theta oscillations generated by the interplay of olfactory input modulated by sniffing and centrifugal feedback from downstream brain areas. Studies in the hippocampus and cortex suggest that different information “chunks” are conveyed at different phases of the theta oscillation. Here we show that in the olfactory bulb, the first processing station in the olfactory system, the amplitude of high frequency gamma oscillations encodes for information on whether an odorant is rewarded when it is observed at the peak phase of the theta oscillation. Furthermore, encoding of information by the theta phase-referenced gamma oscillations becomes more accurate as the animal learns to differentiate two odorants.

Olfactory impairment in men and mice related to aging and amyloid-induced pathology

“…This process is accompanied by gamma oscillations [ 121 ], including low (40–70 Hz) and high (70–100 Hz) gamma [ 88 ]. Besides gamma oscillations, phase-amplitude coupling was also reported to be involved in the processing of odor information [ 95 ]. Deficits in both OB gamma network oscillations and phase-amplitude coupling were found in aging and AD mice [ 2 – 4 , 12 ].…”

Oxytocin modulates neural processing of mitral/tufted cells in the olfactory bulb

“…33 Oscillations recorded from the OB contain crucial information on chemical properties of the odour and as well as odour identity encoding during olfactory learning. 34,35 Thus, we next compared the LFP signals in awake mice before and after direct application of oxytocin into the OB. The raw LFP signals were divided into theta (2-12 Hz), beta , low gamma (36-65 Hz) and high gamma (66-95 Hz) bands (Figure 4A).…”

The human olfactory bulb process odor valence representation and initiate motor avoidance behavior

“…Different functional roles have been attributed to PAC, including sensory signal detection (Händel and Haarmeier 2009), executive functions (Tort et al 2009), and attentional selection (Schroeder and Lakatos 2009). Specifically for olfaction, it has recently been demonstrated that PAC in the OB shapes early sensory processing in mice (Losacco et al 2020). Given this, we examined PAC between beta and gamma oscillation within the OB and its relation to the processing of the individual's odor valence using RSA.…”