Precision of Classification of Odorant Value by the Power of Olfactory Bulb Oscillations Is Altered by Optogenetic Silencing of Local Adrenergic Innervation

Abstract

Neuromodulators such as noradrenaline appear to play a crucial role in learning and memory. The goal of this study was to determine the role of norepinephrine in representation of odorant identity and value by olfactory bulb oscillations in an olfactory learning task. We wanted to determine whether the different bandwidths of olfactory bulb oscillations encode information involved in associating the odor with the value, and whether norepinephrine is involved in modulating this association. To this end mice expressing halorhodopsin under the dopamine-beta-hydrolase (DBH) promoter received an optetrode implant targeted to the olfactory bulb. Mice learned to differentiate odorants in a go-no-go task. A receiver operating characteristic (ROC) analysis showed that there was development of a broadband differential rewarded vs. unrewarded odorant-induced change in the power of local field potential oscillations as the mice became proficient in discriminating between two odorants. In addition, the change in power reflected the value of the odorant rather than the identity. Furthermore, optogenetic silencing of local noradrenergic axons in the olfactory bulb altered the differential oscillatory power response to the odorants for the theta, beta, and gamma bandwidths.

Improved Separation of Odor Responses in Granule Cells of the Olfactory Bulb During Odor Discrimination Learning

“…These studies combined with our findings suggest that GCs in the OB likely mediate the pattern separation in M/T cells. This hypothesis is further supported by a recent study showing that odor-induced changes in the power of local field potential oscillations in the OB also display learning-related separation (Ramirez-Gordillo et al, 2018). A previous study has shown that GC-specific silencing does not alter the firing rate of mitral cell (Fukunaga et al, 2014).…”

“…Previous studies have shown that both odor-induced oscillations in the OB and odor responses in M/T cells differ between FA and CR trials (Ramirez-Gordillo et al, 2018;Wang et al, 2019), which are incorrect and correct responses to the same odorant (S-), respectively. Using the methods described above, we analyzed GC activity during the Hit, FA, and CR trials in the last session of the go/no go task.…”

Complex neural representation of odour information in the olfactory bulb

“…Both the number of units responding to odours and the number of units showing divergent response to S+ (rewarded odour) and S− (unrewarded odour) increases, after the animals learned to discriminate odours (Figure ), suggesting strong plasticity of M/Ts responding to odours during learning . Similar plasticity has been also found for oscillations of local field potentials in behaving rodents . Furthermore, whether this type of plasticity exists in the olfactory sensory neurons is controversial .…”

“…Although specific manipulation of noradrenergic neurons by optogenetics is feasible, surprisingly only 1 study has used this technique to date. This study finds that Optogenetic inhibition of adrenergic fibres alters odorant‐induced changes in power of oscillations in the OB in mice learning to discriminate odorants . Information is still lacking about the effects of optogenetic activation of noradrenergic inputs on odour‐related spiking in the OB in awake animals.…”

“…It will be interesting to discover how sniffing modulates the activity of other types of interneurons in the glomerular and external plexiform layers in future studies. Interestingly, oscillations of the local field potential in the OB are locked to lick patterns in animals undergoing fast sniffing in the go/no go task raising the question whether there is a motor relationship between the theta LFP, sniff and licking in this behavioural state …”