Global Features of Neural Activity in the Olfactory System Form a Parallel Code That Predicts Olfactory Behavior and Perception

Abstract

Odor identity is coded in spatiotemporal patterns of neural activity in the olfactory bulb. Here we asked whether meaningful olfactory information could also be read from the global olfactory neural population response. We applied standard statistical methods of dimensionality-reduction to neural activity from 12 previously published studies using seven different species. Four studies reported olfactory receptor activity, seven reported glomerulus activity, and one reported the activity of projection-neurons. We found two linear axes of neural population activity that accounted for more than half of the variance in neural response across species. The first axis was correlated with the total sum of odor-induced neural activity, and reflected the behavior of approach or withdrawal in animals, and odorant pleasantness in humans. The second and orthogonal axis reflected odorant toxicity across species. We conclude that in parallel with spatiotemporal pattern coding, the olfactory system can use simple global computations to read vital olfactory information from the neural population response.

The muted sense: neurocognitive limitations of olfactory language

“…An alternative theory holds that odor naming is instead constrained by an initial, valence-based encoding format that resists verbal translation [24]. According to this theory, hedonic valence might be critical because it typically emerges as a primary dimension of olfactory perception [25,26], and because variations in odor valences correlate with activation patterns in the olfactory neuroepithelium and the brain [27,28]. Whether configural objects or valences constitute the initial perceptual odor encoding stage should be reflected by the speed for ‘object-based’ versus ‘valence-based’ decisions.…”

Behavior Reveals Selective Summation and Max Pooling among Olfactory Processing Channels

“…These studies found positive and negative weights associated with specific ORN types (Knaden et al, 2012; Kreher et al, 2008). However, a limitation of these approaches is that the odor responses of different ORN types are statistically correlated (Haddad et al, 2010): an odor stimulus that strongly activates a given receptor tends to strongly activate other receptors as well. Because multiple ORN types are often co-activated by attractive odors, linear regression cannot tell us which ORN type causes the attraction.…”

Separation of different pollen types by chemotactile sensing in Bombus terrestris.

“…Whereas pure almond pollen and almond pollen extract evoked a negative EAG signal, pure apple pollen and apple pollen extract evoked a positive EAG response. Positive EAG signals have been reported many times in olfactory EAGs (Contreras et al, 1989;Haddad et al, 2010;Leskey et al, 2010;Light et al, 1988;Ramachandran et al, 1990;Schneider, 1957) and were hypothesized to be evoked by repellent compounds (Contreras et al, 1989). However, Leskey et al (2010) reported that the odor of preferred fruits evoked a positive signal in plum curculios (Conotrachelus nenuphar, Coleoptera), and Knaden et al (2012) postulated for Drosophila melanogaster that no reliable information about attractiveness or repellence was encoded in the neural signal before it reached the output neurons of the antennal lobe.…”