Coding of odors in the anterior olfactory nucleus

Abstract

Odorant molecules stimulate olfactory receptor neurons, and axons of these neurons project into the main olfactory bulb where they synapse onto mitral and tufted cells. These project to the primary olfactory cortex including the anterior olfactory nucleus (AON), the piriform cortex, amygdala, and the entorhinal cortex. The properties of mitral cells have been investigated extensively, but how odor information is processed in subsequent brain regions is less well known. In the present study, we recorded the electrical activity of AON neurons in anesthetized rats. Most AON cells fired in bursts of 2–10 spikes separated by very short intervals (<20 ms), in a period linked to the respiratory rhythm. Simultaneous recordings from adjacent neurons revealed that the rhythms of adjacent cells, while locked to the same underlying rhythm, showed marked differences in phase. We studied the responses of AON cells to brief high‐frequency stimulation of the lateral olfactory tract, mimicking brief activation of mitral cells by odor. In different cells, such stimuli evoked transient or sustained bursts during stimulation or, more commonly, post‐stimulation bursts after inhibition during stimulation. This suggests that, in AON cells, phase shifts occur as a result of post‐inhibitory rebound firing, following inhibition by mitral cell input, and we discuss how this supports processing of odor information in the olfactory pathway. Cells were tested for their responsiveness to a social odor (the bedding of a strange male) among other simple and complex odors tested. In total, 11 cells responded strongly and repeatedly to bedding odor, and these responses were diverse, including excitation (transient or sustained), inhibition, and activation after odor presentation, indicating that AON neurons respond not only to the type of complex odor but also to temporal features of odor application.

Characterization of odor-evoked neural activity in the olfactory peduncle

“…Despite a higher median spontaneous rate compared to that observed in the present sample, a similar proportion of cells were responsive to odor presentation. Consistent with these findings, the majority of cells assessed fired in phased with ongoing respiration with a preference for peak firing during the expiration phase, which may relate in part to GABAergic inhibition resulting from activation of the lateral olfactory tract ( Tsuji et al, 2019 ).…”

“… Lei et al (2006) demonstrated that histologically identified pyramidal neurons intracellularly recorded from the AON were broadly tuned to multiple components of odor mixtures, a pattern that may emerge through convergence of synaptic input from narrowly-tuned OB mitral cells ( Apicella et al, 2010 ; Miyamichi et al, 2011 ) and through integration of OB input through associational fiber networks ( Luskin & Price, 1983 ). Tsuji et al (2019) recently reported evidence for several classes of rhythmic cells in the ventrolateral AON in urethane anesthetized rats. Despite a higher median spontaneous rate compared to that observed in the present sample, a similar proportion of cells were responsive to odor presentation.…”

“…Sensory physiological studies characterizing principles of sensory representation are necessary to provide insight to fully develop theories addressing functional diversity within the olfactory system. Although piriform cortex (PC), the most prominent OB target, has been the main focus for physiological investigation among primary olfactory areas ( Isaacson, 2010 ; Stettler & Axel, 2009 ; Wilson & Sullivan, 2011 ), a growing body of research is examining features of sensory coding and functional organization in closely associated olfactory regions, including the olfactory tubercle (OT) ( Gadziola et al, 2015 ; Payton et al, 2012 ; Rampin et al, 2012 ; Wesson & Wilson, 2010 ), entorhinal cortex (EC) ( Xu & Wilson, 2012 ), cortical amygdala (CoA) ( Iurilli & Datta, 2017 ), and the anterior olfactory nucleus (AON) ( Kikuta et al, 2008 , 2010 ; Lei et al, 2006 ; ; Tsuji et al, 2019 ). Limited data available to date from single-unit electrophysiological studies suggest that, despite cytoarchitectural and organizational differences across olfactory areas, populations of neurons often exhibit response characteristics that resemble those observed in PC ( Iurilli & Datta, 2017 ; Payton et al, 2012 ).…”

A stable, distributed code for cue value in mouse cortex during reward learning

“…Our findings in AON, DP, and TTd differ from reports that piriform cortex lacks odor value representations (Blazing and Franks, 2020;Wang et al, 2020a;Winkelmeier et al, 2022) and suggest that these olfactory peduncular areas, as well as olfactory tubercle (Gadziola et al, 2015;Millman and Murthy, 2020;Winkelmeier et al, 2022), may provide more value-related processing of odor cues than better-studied odor processing routes through piriform cortex (Blazing and Franks, 2020;Mori and Sakano, 2021;Winkelmeier et al, 2022). Previous recordings in AON, DP, and TTd were in anesthetized rodents (Cousens, 2020;Kikuta et al, 2008;Lei et al, 2006;Tsuji et al, 2019); as the first recordings in awake behaving animals, our results bring these regions into focus for future work on the transformation of odor information into task-relevant coding.…”

Neural circuits of social behaviors: Innate yet flexible

“…Very little is known regarding the function of the AON. Two studies involving electrophysiological recordings of AON cells in anesthetized mice and rats showed that AON cells integrate inputs from diverse chemical classes and that some cells are tuned specifically to socially relevant olfactory cues (e.g., soiled bedding) (Lei et al, 2006;Tsuji et al, 2019). The CoApl also sends weak projections to the NAc and is activated preferentially by innately attractive odors.…”