Separate encoding of identity and similarity of complex familiar odors in piriform cortex

Abstract

Piriform cortical circuits are hypothesized to form perceptions from responses to specific odorant features, but the anterior piriform cortex (aPCX) and posterior piriform cortex (pPCX) differ markedly in their anatomical organization, differences that could lead to distinct roles in odor encoding. Here, we tested whether experience with a complex odorant mixture would modify encoding of the mixture and its components in aPCX and pPCX. Rats were exposed to an odorant mixture and its components in a go/no-go rewarded odor discrimination task. After reaching behavioral performance criterion, single-unit recordings were made from the aPCX and pPCX in these rats and in odor-naïve, control, urethane-anesthetized rats. After odor experience, aPCX neurons were more narrowly tuned to the test odorants, and there was a decorrelation in aPCX population responses to the mixture and its components, suggesting a more distinct encoding of the familiar mixture from its components. In contrast, pPCX neurons were more broadly tuned to the familiar odorants, and pPCX population responses to the mixture and its components became more highly correlated, suggesting a pPCX encoding of similarity between familiar stimuli. The results suggest aPCX and pPCX play different roles in the processing of familiar odors and are consistent with an experience-dependent encoding (perceptual learning) of synthetic odorant identity in aPCX and an experience-dependent encoding of odor similarity or odor quality in pPCX.

Fig. 1.

Behavioral discrimination (error ratio) of each component and air from the mixture for the last 14 sessions. Performance improved across the sessions. There was no significant difference in improvement between air and the three components.

Fig. 2.

Reconstructed positions of aPCX (Left) and pPCX (Right) recording sites and representative single-unit responses in each region in this study. Layer II is shown in gray. Cells were located in layer II/III between 0.96 and −0.60 mm anterior to bregma in aPCX and between 2.8 and 4.24 mm posterior to bregma in pPCX. The neuron (100105#1-6668) was obtained at 0.0 mm anterior to bregma. This neuron responded to acetic acid (AA), eugenol (Eug), limonene (Lim), and Mix. The average spike waveform of this neuron is shown at the top of the column. Another neuron (012606#2-6355) was located at 3.3 mm posterior to bregma. This cell also responded to AA, Eug, Lim, and Mix. The average spike waveform of this neuron is shown at the top of the column.

Fig. 3.

Breadth of tuning (entropy) of aPCX (Upper) and pPCX (Lower) neurons in control and trained animals. In aPCX, the breadth of tuning in odor-experienced animals was significantly reduced (more selective) compared with that in control animals. In contrast, pPCX neurons showed significantly broader tuning (less selective) after odor experience compared with controls.

Fig. 4.

Correlation matrices of unit responses (evoked response magnitude) to individual odorants and the mixture. (A) PCX population responses to individual odorants were significantly less well correlated with other individual odorants than they were to responses to mixtures containing those odorants in naïve control animals. (B Left) The enhanced correlation between aPCX population responses to mixtures and their components was eliminated in experienced rats. Thus, the mixture was encoded as distinctly as the individual components in experienced rats. (B Right) In pPCX, both intercomponent and component-mixture correlations were significantly increased by experience.