Many species use bilateral sampling for odor-guided navigation. Bilateral localization strategies typically involve balanced and lateralized sensory input and early neuronal processing. For example, if gradient direction is estimated by differential sampling, then any asymmetry could bias the perceived direction. Subsequent neuronal processing can compensate for this asymmetry but requires the presence of mechanisms to track changes in asymmetry. A high degree of laterality is also important for differential sampling because spillover of signals will dilute the perceived odor gradient. In apparent contradiction to this model, both symmetry and laterality of nasal air flow have been reported to be incomplete in rats. Here, we measured symmetry and laterality in early olfactory processing in the rat. We first established behavioral readouts of precisely controlled bilateral odorant stimuli. We found that rats could rapidly and accurately report the direction of a wide range of odor gradients, presented in random sequence. We then showed that nasal air flow was symmetric over an entire day in awake rats. Furthermore, odor sampling from the two nostrils in the behavioral task was highly lateralized. This lateralization extended to the receptor epithelium responses as measured by electro-olfactograms. We finally observed strong lateralization of intrinsic signal responses from the glomerular layer of the olfactory bulb. We confirmed that a differential comparison of glomerular responses was sufficient to localize odorants. Together, these results suggest that the rat olfactory system is symmetric, with highly lateralized odor flow and neuronal responses. In combination, these attributes support odor localization by differential comparison.
A first key step in studying a sensory modality is to define how the brain represents the features of the sensory stimulus. This has proven to be a challenge in olfaction, where even the stimulus features have been a matter of considerable debate. In this review, we focus on olfactory representations in the first stage of the olfactory pathway, the olfactory bulb (OB). We examine the diverging viewpoints on spatially organized versus distributed representations. We then consider how odor sampling through respiration is a key part of the odorant code. Finally, we ask how the bulb handles the challenging task of representing mixtures. We suggest that current evidence points toward a representation that is spatially organized at the inputs but later distributed, with the spatial organization not being used for much computation. Nevertheless, this is a simple representation that effectively represents multiple individual odorants, as well as odor mixtures.
While tracking odor plumes, male hawkmoths use optic flow cues to stabilize their flight movements with respect to their environment. We studied the responses of freely flying moths tracking odor plumes in a laboratory wind tunnel and tethered moths in an optomotor flight simulator to determine the locations on the compound eye on which critical optic flow cues are detected. In these behavioral experiments, we occluded specific regions of the compound eye and systematically examined the moths' behavior for specific deficits in optic flow processing. Freely flying moths with the dorsal half of the compound eye painted were unable to maintain stable flight and track the wind-borne odor plume. However, the plume tracking performance of moths with the ventral half of their compound eyes painted was the same as unpainted controls. In a matched set of experiments, we presented tethered moths with moving vertically oriented sinusoidal gratings and found that individuals with their eyes unpainted, ventrally painted and medially painted all responded by attempting optomotor-driven turns in the same proportion. In contrast, individuals with their compound eyes dorsally painted, laterally painted and completely painted showed no optomotor turning response. We decreased the contrast of the visual stimulus and found that this relationship was consistent down to a contrast level of 2.5%. We conclude that visual input from the dorso-lateral region of the moth's visual world is critical for successful maintenance of flight stability and that this species' visual environment must meet or exceed a contrast ratio of 2.5% to support visual flight control.
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