Task-Demand-Dependent Neural Representation of Odor Information in the Olfactory Bulb and Posterior Piriform Cortex

Abstract

In awake rodents, the neural representation of olfactory information in the olfactory bulb is largely dependent on brain state and behavioral context. Learning-modified neural plasticity has been observed in mitral/tufted cells, the main output neurons of the olfactory bulb. Here, we propose that the odor information encoded by mitral/tufted cell responses in awake mice is highly dependent on the behavioral task demands. We used fiber photometry to record calcium signals from the mitral/tufted cell population in awake, head-fixed male mice under different task demands. We found that the mitral/tufted cell population showed similar responses to two distinct odors when the odors were presented in the context of a go/go task, in which the mice received a water reward regardless of the identity of the odor presented. However, when the same odors were presented in a go/no-go task, in which one odor was rewarded and the other was not, then the mitral cell population responded very differently to the two odors, characterized by a robust reduction in the response to the nonrewarded odor. Thus, the representation of odors in the mitral/tufted cell population depends on whether the task requires discrimination of the odors. Strikingly, downstream of the olfactory bulb, pyramidal neurons in the posterior piriform cortex also displayed a task-demand-dependent neural representation of odors, but the anterior piriform cortex did not, indicating that these two important higher olfactory centers use different strategies for neural representation.

Excitability of Neural Activity is Enhanced, but Neural Discrimination of Odors is Slightly Decreased, in the Olfactory Bulb of Fasted Mice

“…The microelectrodes (16-channel, Jiangsu Brain Medical Technology Co. Ltd, Nanjing, China) were implanted into a specific region of the brain as previously described [18,19]. Briefly, mice were anesthetized with pentobarbital sodium (90 mg/kg body weight, i.p.)…”

“…The recordings were initiated after the mice had recovered from surgery, as in previous studies [18][19][20][21]. Briefly, awake mice were head-fixed with two horizontal bars and were able to maneuver on an air-supported free-floating Styrofoam ball (Thinkerbiotech, Nanjing, China).…”

“…Offline spike sorting and statistics of single-cell spiking data: When we did spike sorting, all the files were put together to make sure signals recorded at different stages were from same units. Similar to previous studies, single units were sorted and identified with principal components analysis in Offline Sorter V4 software [18,19]. In addition, we performed further analysis on all recorded unit to double check that the spikes were from the same units (repeated measures ANOVA on the spike amplitude and half-width).…”

“…An auROC curve is defined from 0.5 to 1.0. A value of 0.5 indicates completely overlapping distributions, whereas a value of 1 predicts perfect discriminability [19].…”

The olfactory bulb contributes to the adaptation of odor responses: the input-output transformation

“…The number of identified interneuron types of likely to increase when newer methods for determining the number are used (Parrish-Aungst et al, 2007;Shekhar et al, 2016;Zeng and Sanes, 2017). Despite its position as the first stage of olfactory information processing, the olfactory bulb has been implicated in diverse sensory functions including concentration invariance (Cleland et al, 2007;Banerjee et al, 2015;Sirotin et al, 2015;Storace and Cohen, 2017), metabolism (Fadool et al, 2011;Thiebaud et al, 2014;Riera et al, 2017), learning (Kass et al, 2013), and context-dependent processing (Doucette et al, 2011;Nunez-Parra et al, 2014;Li et al, 2017;Koldaeva et al, 2019;Wang et al, 2019).…”