Encoding Innately Recognized Odors via a Generalized Population Code

Abstract

Odors carrying intrinsic values often trigger instinctive aversive or attractive responses.Innate valence is thought to be conveyed through hardwired circuits along the olfactory pathway, insulated from influences of other odors. Here we show that in mice, mixing of innately aversive or attractive odors with a neutral odor abolishes the behavioral responses. Surprisingly, mixing of two odors with the same valence also abolishes the expected responses. Recordings from the olfactory bulb indicate that odors are not masked at the level of peripheral activation and glomeruli independently encode components in the mixture. However, crosstalk among the mitral/tufted cells changes their patterns of activity such that those elicited by the congruent mixtures can no longer be decoded as separate components. The changes in behavioral and mitral/tufted cell responses are associated with reduced activation of brain areas linked to odor preferences. Thus, interactions of odor channels at the earliest processing stage in the olfactory pathway lead to re-coding of odor identity. These results are inconsistent with insulated labeled lines and support a model of a common mechanism of odor recognition for both innate and learned valence associations.

Acquisition of Innate Odor Preference Depends on Spontaneous and Experiential Activities During Critical Period

“…Figure 8C). This model is consistent with emerging evidence that suggests innate preference is context dependent, and has strong interactions among olfactory pathways (Qiu et al, 2020;Saraiva et al, 2016). It is also consistent with evidence that ethologically relevant odors are encoded similarly as ordinary odors in cortical structures thought to encode innate preference (Iurilli and Datta, 2017).…”

“…It was likely that at first odor presentation, investigative behavior was driven by two conflicting drives: risk assessment (approach) and avoidance. To have a consistent measure of odor preference, we thus combined the changes at the first and second odor epochs as an index to measure innate behavior preference (see Methods) (Qiu et al, 2020).…”

Acquisition of innate odor preference depends on spontaneous and experiential activities during critical period

“…We measured the duration of odor source investigation and compared it to the no odor period. The level of investigation indicated odor preference (Qiu et al, 2014). Control mice exhibited increased frequency and duration in sniffing the odor port during the presentation of peanut butter odor or mouse urine (Figure 1D).…”

“…We, therefore, used neutral odors to test odor detection and discrimination in the Kir2.1-off mice. We evaluated detection of low concentration of amyl acetate (AA) and 2heptanone (HPO) using a dishabituation assay that provided a sensitive readout of odor detection threshold in naïve animals (Qiu et al, 2014). Control and Kir2.1-off mice exhibited similar increases in investigation of the odor port with increasing concentration of odors (Figures 4A-i and Figure 4-figure supplement 1A).…”

“…We performed additional evaluation of detection thresholds using the Go/No Go task (Qiu et al, 2014). Water-restricted animals were trained to associate an odor with water reward then tested with lowered concentrations of the trained odor.…”