Olfactory perceptual stability and discrimination

Abstract

No two roses smell exactly alike, but our brain accurately bundles these variations into a single percept 'rose'. We found that ensembles of rat olfactory bulb neurons decorrelate complex mixtures that vary by as little as a single missing component, whereas olfactory (piriform) cortical neural ensembles perform pattern completion in response to an absent component, essentially filling in the missing information and allowing perceptual stability. This piriform cortical ensemble activity predicts olfactory perception.

Figure 1

Odor discrimination and stability. (a) Representative responses of two different aPCX single units and a mitral/tufted (M/T) cell to morphed complex odor mixtures. Raster plots show responses to 2-5 repeats of each 2-s stimulus. Waveforms are overlays of at least 100 consecutive spikes. Letter series to the right of each raster plot indicates the mixture of components that was present. Starred letters indicate component replacement (removal of a component from the mixture and replacement with a different component). Note that as stimulus mixtures morphed gradually, unit responses did not, and were not predictable from the change in stimulus. (b) Cross-correlation analyses of mitral/tufted and aPCX pyramidal cell ensemble responses to the 10c mix versus the various morphs. (c) Behavioral performance in a two-alternative forced-choice odor-discrimination task matched predictions from the aPCX ensembles, with discrimination of a single missing component being significantly more difficult than discrimination of a replaced component. The marked improvement that we observed in behavioral discrimination of 10c-2 relative to the gradual change in ensemble decorrelation could reflect a threshold phenomenon in cortical to behavioral translation. Error bars represent s.e.m.

Figure 2

Piriform cortical ensembles predict behavioral discrimination. (a) Rats could not detect removal of isoamyl acetate from a 10c mixture; however, rats could discriminate mixtures in which isoamyl acetate was replaced with any of three different molecules. (b) Over all mixture morphs, mixes with single replaced components were significantly easier for rats to discriminate from the 10c standard than mixes with a single removed component. (c) Similarly, cortical ensembles decorrelated mixes with single replaced components from the standard 10c mix significantly greater than mixes with a single removed component. Error bars represent s.e.m. Asterisks indicate a significant difference (P < 0.05) between Replace and Remove manipulations.