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.
Highlights
A fundamental cornerstone of sensory neuroscience is to understand internal representations of external stimuli
Within group statistical comparisons of responses to the blank and responses to subsequent concentrations of CS indicated that 0.01 μg/2 μl of odor produced a significant increase in conditioned response (CR) probability for all odors
More diluted odors had lower latencies the discrimination threshold, suggesting that if information is present at the discrimination threshold, it likely takes a few milliseconds more to emerge. These analysis indicates that when the virtual ensemble data is collapsed by space and time, there is little if any measurable information remaining that could be used by the moth to determine odor identity at psychophysical threshold concentrations as all of the statistical effects were either by comparison with the blank or neat odorant
Summary
A fundamental cornerstone of sensory neuroscience is to understand internal representations of external stimuli. There has been considerable controversy about what ‘‘represents’’ an olfactory cue, almost no emphasis has been placed on establishing measures of olfactory representations at identified psychophysical limits of olfactory acuity. This absence of critically important relationship between psychophysical thresholds and physiological measures is unprecedented in sensory neuroscience. Olfactory sensory neurons (OSNs), which express the same receptor proteins (Buck and Axel, 1991; Clyne et al, 1999; Gao and Chess, 1999), project to the same glomerulus (or a pair of glomeruli in mammals) within the antennal lobe and olfactory bulb (AL/OB; Mombaerts et al, 1996; Wang et al, 1998; Vosshall et al, 2000) This input organization supports the proposition that odor identity is initially encoded as a spatial input pattern across glomeruli based on OSN tuning. With increased odor concentration, odor-dependent maps often expand and show increased excitation (Rubin and Katz, 1999; Fuss and Korsching, 2001; Sachse and Galizia, 2003; Strauch et al, 2012) and increasing concentration is often associated with better performance in behavioral discrimination tasks (Wright and Smith, 2004; Daly et al, 2008)
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