Laterality and Symmetry in Rat Olfactory Behavior and in Physiology of Olfactory Input

Abstract

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.

Dynamic cortical lateralization during olfactory discrimination learning

“…Although there can be asymmetry in nasal airflow in mammals, and this asymmetry affects central olfactory system activity (Bojsen‐Moller & Fahrenkrug, ; Werntz et al . ; Parthasarathy & Bhalla, ), we consider that this nasal asymmetry does not account for the lateralized effects observed in the present study. Nasal patency can change over the course of hours and days but, to account for the effects observed in the present study, such changes would need to be linked to performance on the discrimination task.…”

“…Bilateral comparisons can be used for odour localization (Rajan et al . ; Parthasarathy & Bhalla, ). Single‐units in the anterior olfactory nucleus (Kikuta et al .…”

“…Unilateral activation of the olfactory bulb in rodents suppresses activity in the contralateral olfactory bulb (von Baumgarten et al 1962;Wilson, 1997), perhaps contributing to binaral stimulus comparisons (Wilson & Sullivan, 1999;Rajan et al 2006;Porter et al 2007). Bilateral comparisons can be used for odour localization (Rajan et al 2006;Parthasarathy & Bhalla, 2013). Single-units in the anterior olfactory nucleus (Kikuta et al 2010) and PCX (Wilson, 1997) express bilateral spatial tuning characteristics.…”

An Objective and Reproducible Test of Olfactory Learning and Discrimination in Mice

“…Rats, for example, have been instrumental in revealing neuronal function within the OB 11,12 . Due to their intelligence, rats also have faster learning times than mice 13,14 Despite these limitations, we chose mice for this protocol because of their genetic tractability for performing cell type specific manipulations and recordings 15 .…”

Sniff-invariant intensity perception using olfactory bulb coding of inhalation dynamics

“…Thus, even on short timescales, a 150 more rapid inhalation mimics concentration increases at the level of the olfactory bulb output. 151 152 Rodents have previously demonstrated the ability to discriminate odor concentrations (Abraham et 153 al., 2004;Parthasarathy and Bhalla, 2013;Slotnick and Ptak, 1977;Wojcik and Sirotin, 2014). Given 154 the physiology ( Fig.…”