Space Takes Time: Concentration Dependent Output Codes from Primary Olfactory Networks Rapidly Provide Additional Information at Defined Discrimination Thresholds

Abstract

As odor concentration increases, primary olfactory network representations expand in spatial distribution, temporal complexity and duration. However, the direct relationship between concentration dependent odor representations and the psychophysical thresholds of detection and discrimination is poorly understood. This relationship is absolutely critical as thresholds signify transition points whereby representations become meaningful to the organism. Here, we matched stimulus protocols for psychophysical assays and intracellular recordings of antennal lobe (AL) projection neurons (PNs) in the moth Manduca sexta to directly compare psychophysical thresholds and the output representations they elicit. We first behaviorally identified odor detection and discrimination thresholds across an odor dilution series for a panel of structurally similar odors. We then characterized spatiotemporal spiking patterns across a population of individually filled and identified AL PNs in response to those odors at concentrations below, at, and above identified thresholds. Using spatial and spatiotemporal based analyses we observed that each stimulus produced unique representations, even at sub-threshold concentrations. Mean response latency did not decrease and the percent glomerular activation did not increase with concentration until undiluted odor. Furthermore, correlations between spatial patterns for odor decreased, but only significantly with undiluted odor. Using time-integrated Euclidean distance (ED) measures, we determined that added spatiotemporal information was present at the discrimination but not detection threshold. This added information was evidenced by an increase in integrated distance between the sub-detection and discrimination threshold concentrations (of the same odor) that was not present in comparison of the sub-detection and detection threshold. After consideration of delays for information to reach the AL we find that it takes ~120–140 ms for the AL to output identity information. Overall, these results demonstrate that as odor concentration increases, added information about odor identity is embedded in the spatiotemporal representation at the discrimination threshold.

Characterizing neural coding performance for populations of sensory neurons: comparing a weighted spike distance metrics to other analytical methods

“…In vivo neural recordings were obtained from previous research and the details of the experiments are given in the corresponding publications (Daly et al, 2016a;Allen and Marsat, 2018). One second long PN recordings from the AL of moth where performed during and after the presentations of 6 different concentrated odors puffs (100 ms long) and one blank stimulus.…”

“…In this brief report, we compare these different methods by using three dataset representative of the lower levels of sensory systems. We use recordings from olfactory responses of projection neurons (PNs) in the antennal lobe (AL) of moth (Daly et al, 2016b), pyramidal cell (PC) responses to communication stimuli in the electrosensory lateral line lobe (ELL) of weakly electric fish (Allen and Marsat, 2018) and responses of leaky integrate and fire (LIF) model neurons to frozen white noise in a linear regime. Each system encode the relevant information in different aspect of the population response's spatiotemporal pattern.…”

Behavioral and Neural Aspects of the Spatial Processing of Conspecifics in the Electrosensory System

“…Even for olfactory signals, the message is represented by the quality (i.e. odor identity) and quantity of the odor (Aragón, 2009;Daly et al, 2016;de Bruyne & Baker, 2008). In most cases, the receiver also tries to determine the location of the signal's source.…”

Behavioral and Neural Aspects of the Spatial Processing of Conspecifics in the Electrosensory System

“…Even for olfactory signals, the message is represented by the quality (i.e. odor identity) and quantity of the odor (Aragón, 2009;Daly et al, 2016;de Bruyne & Baker, 2008). In most -if not all-cases, the receiver also tries to determine the location of the signal's source.…”