Olfactory cortical adaptation facilitates detection of odors against background

Abstract

Detection and discrimination of odors generally, if not always, occurs against an odorous background. On any given inhalation, olfactory receptor neurons will be activated by features of both the target odorant and features of background stimuli. To identify a target odorant against a background therefore, the olfactory system must be capable of grouping a subset of features into an odor object distinct from the background. Our previous work has suggested that rapid homosynaptic depression of afferents to the anterior piriform cortex (aPCX) contributes to both cortical odor adaptation to prolonged stimulation and habituation of simple odor-evoked behaviors. We hypothesize here that this process may also contribute to figure-ground separation of a target odorant from background stimulation. Single-unit recordings were made from both mitral/tufted cells and aPCX neurons in urethan-anesthetized rats and mice. Single-unit responses to odorant stimuli and their binary mixtures were determined. One of the odorants was randomly selected as the background and presented for 50 s. Forty seconds after the onset of the background stimulus, the second target odorant was presented, producing a binary mixture. The results suggest that mitral/tufted cells continue to respond to the background odorant and, when the target odorant is presented, had response magnitudes similar to that evoked by the binary mixture. In contrast, aPCX neurons filter out the background stimulus while maintaining responses to the target stimulus. Thus the aPCX acts as a filter driven most strongly by changing stimuli, providing a potential mechanism for olfactory figure-ground separation and selective reading of olfactory bulb output.

FIG. 1

Top: experimental design for analysis of figure-ground separation by anterior piriform cortex (aPCX) and mitral/tufted neurons. Each component and the binary mixture were given twice for 2 s with at least a 60-s interval to determine initial response magnitude. Then 1 component of the binary mixture (background odorant) was presented for 50 s. Forty seconds after the onset of background, the other (target) odorant was added for 2 s, essentially creating a 2nd binary mixture. Binary mixtures and target against background stimuli were created by dividing the airstream toward both odors, thus total flow rate of odorized air did not differ between component and mixture stimuli. Bottom: representative examples of mitral/tufted and aPCX neuron responses during single stimulus and background stimulation. While both the mitral/tufted and aPCX neuron increased firing rate when the target odorant was presented against background, because the aPCX neuron had stopped responding to the background, its response was more similar to the target alone. The mitral/tufted cell response magnitude was more similar to the binary mixture under this same condition. Mean waveforms for both cells are shown to the right.

FIG. 2

A: histograms of main olfactory bulb (MOB) mitral/tufted cell and aPCX neuron response magnitudes to a binary mixture as a ratio of the response magnitude to the most effective component of that mixture. Although the distribution was relatively continuous, cells were divided into mixture suppression and mixture addition groups based on previous work. B: example peristimulus time histograms (PSTHs) of single units showing mixture addition and mixture suppression. The number of evoked spikes/2-s stimulus are shown above each histogram. Mean waveforms for both cells are shown to the right. C: percentage of units demonstrating mixture addition and mixture suppression of mitral/tufted and aPCX neurons. Approximately 30% of units obtained in both MOB and aPCX showed mixture addition, and 70% mixture suppression. Right: standardized response magnitude of mitral/tufted and aPCX neurons to the target odorants and binary mixtures. The average response magnitude of mixture-addition neurons to the binary mixtures (A + B) was more than twice than that to the individual odorants (A or B), whereas that of mixture-suppression neurons to the binary mixture was less than that to the target odorants in both mitral/tufted and aPCX neurons.

FIG. 3

Left: mean activity of mixture-addition mitral/tufted (top) and aPCX (bottom) neurons before (1st 2 s) and after 40-s exposure (last 2 s) to the background odorant. Mitral/tufted neurons did not significantly adapt to the background odorant, whereas aPCX neurons did. In both sites, presentation of the target odorant against the background evoked an increase in activity. Right: mean response magnitudes of mitral/tufted (top) and aPCX (bottom) neurons to the target (nonbackground) odorant alone, the binary mixture and the target odorant against the background (same stimulus as the binary mixture). Response magnitudes are calculated as odor-evoked spikes during the 2-s stimulus minus spike rate during 2 s of spontaneous activity. Mitral/tufted cell response magnitude to the target odorant against background was similar to binary mixture and significantly different from the response to the nonadapted component alone. In contrast, aPCX neuron response magnitude to the target odorant against background was similar to the nonadapted component alone and significantly different from the binary mixture. The results are consistent with a role for aPCX neurons in filtering out background odorants and responding to new target odorants presented against the background as distinct.

FIG. 4

Left: mean activity of mixture-suppression mitral/tufted (top) and aPCX (bottom) neurons before (1st 2 s) and after (last 2 s) 40-s exposure to the background odorant. Mitral/tufted neurons did not significantly adapt to the background odorant, whereas aPCX neurons did. In both sites, presentation of the target odorant against the background evoked an increase in activity. Right: mean response magnitudes of mitral/tufted (top) and aPCX (bottom) neurons to the target (nonbackground) odorant alone, the binary mixture before, the target odorant against the background odorants. Mitral/tufted cells responded to the target odorant against background with a level of activity no different from their response to the binary mixture or a single odor component alone. In contrast, aPCX neurons responded to the odorant against background with a level of activity significantly different from either the binary mixture or the single component alone.

FIG. 5

Response correlations for units tested with isoamyl acetate (IAA) as the target odorant and pentane (C5) as the background odorant (n = 21 units). Response magnitudes to IAA presented against C5 background were significantly correlated with the response of the same units to IAA alone. There was no significant correlation between IAA against C5 background and the binary mixture of IAA and C5 despite the fact that these two stimuli are identical at the nose.

FIG. 6

Reconstructed positions of aPCX neurons recorded in this study. Distances noted are anterior to Bregma. These neurons were located in aPCX layer II/III. There was no significant difference in distributions among neurons with mixture addition, mixture suppression, and mixture addition/suppression. All cells were located in the dorsal region of the aPCX. AI, agranular insular cortex; CC, corpus callosum; Cl, claustrum; CPu, caudate putamen; DEn, dorsal endopiriform nucleus; DI, dysgranular insular cortex; GI, granular insular cortex; LOT, lateral olfactory track; Pir, piriform cortex; Tu, olfactory tubercle; VP, ventral pallidum

FIG. 7

A: example of an aPCX single-unit odor response in urethan-anesthetized mouse. B, top: mean evoked activity of mixture-addition mouse aPCX neurons before (1st 2 s) and after (last 2 s) 40-s exposure to the background odorant and in response to presentation of the target odorant against the background. Mouse data mirrors data obtained in rat (cf. Fig. 3). Bottom: mouse aPCX neurons responded to the target odorant against background similarly to the nonadapted component alone, and significantly different from the binary mixture. Again, this data are similar to rat data shown in Fig. 3. C: similar presentation of data from mouse aPCX mixture suppression cells. Note similarity with rat data in Fig. 4.