Neural representation of intraoral olfactory and gustatory signals by the mediodorsal thalamus in alert rats.

The mediodorsal thalamus is a multimodal region involved in a variety of cognitive behaviors, including olfactory attention, odor discrimination, and the hedonic perception of flavors. Although the mediodorsal thalamus forms connections with principal regions of the olfactory and gustatory networks, its role in processing olfactory and gustatory signals originating from the mouth remains unclear. Here, we recorded single-unit activity in the mediodorsal thalamus of behaving female rats during the intraoral delivery of individual odors, individual tastes, and odor-taste mixtures. Our results are the first to demonstrate that neurons in the mediodorsal thalamus dynamically encode chemosensory signals originating from the mouth. This chemoselective population is broadly tuned, exhibits excited and suppressed responses, and responds to odor-taste mixtures differently than an odor or taste alone. Furthermore, a subset of chemoselective neurons encodes the palatability-related features of tastes and may represent associations between previously experienced odor-taste pairs. Our results further demonstrate the multidimensionality of the mediodorsal thalamus and provide additional evidence of its involvement in processing chemosensory information important for ingestive behaviors.SIGNIFICANCE STATEMENTThe perception of food relies upon the concurrent processing of olfactory and gustatory signals originating from the mouth. The mediodorsal thalamus is a higher-order thalamic nucleus involved in a variety of chemosensory-dependent behaviors and connects the olfactory and gustatory cortices with the prefrontal cortex. However, it is unknown how neurons in the mediodorsal thalamus process intraoral chemosensory signals. Using tetrode recordings in alert rats, our results are the first to show that neurons in the mediodorsal thalamus dynamically represent olfactory and gustatory signals from the mouth. Our findings are consistent with the mediodorsal thalamus being a key node between sensory and prefrontal cortical areas for processing chemosensory information underlying ingestive behavior.

Experience Informs Consummatory Choices for Congruent and Incongruent Odor-Taste Mixtures in Rats.

Experience is an essential factor informing food choice. Eating food generates enduring odor-taste associations that link an odor with a taste's quality and hedonic value (pleasantness/unpleasantness) and creates the perception of a congruent odor-taste combination. Previous human psychophysical experiments demonstrate that experience with odor-taste mixtures shapes perceptual judgments related to the intensity, familiarity, and pleasantness of chemosensory stimuli. However, how these perceptual judgments inform consummatory choice is less clear. Using rats as a model system and a 2-bottle brief-access task, we investigated how experience with palatable and unpalatable odor-taste mixtures influences consummatory choice related to odor-taste congruence and stimulus familiarity. We found that the association between an odor and a taste, not the odor's identity or its congruence with a taste, informs consummatory choice for odor-taste mixtures. Furthermore, we showed that the association between an odor and a taste, not odor neophobia, informs consummatory choice for odors dissolved in water. Our results provide further evidence that the association between an odor and a taste, after odor-taste mixture experience, is a fundamental feature guiding consummatory choice.

Experience-Dependent c-Fos Expression in the Mediodorsal Thalamus Varies With Chemosensory Modality.

The mediodorsal thalamus is a higher order thalamic nucleus critical for many cognitive behaviors. Defined by its reciprocal connections with the prefrontal cortex, the mediodorsal thalamus receives strong projections from chemosensory cortical areas for taste and smell, gustatory cortex and piriform cortex. Recent studies indicate the mediodorsal thalamus is involved in experience-dependent chemosensory processes, including olfactory attention and discrimination and the hedonic perception of odor-taste mixtures. How novel and familiar chemosensory stimuli are represented within this structure remains unclear. Here, we compared the expression of c-Fos in the mediodorsal thalami of rats familiar with an odor, a taste, or an odor-taste mixture with those that sampled the stimuli for the first time. We found that familiar tastes or odor-taste mixtures induced significantly greater c-Fos expression in the mediodorsal thalamus than novel tastes or odor-taste mixtures, whereas novel odors induced greater c-Fos expression than familiar odors. These experience-dependent and modality-specific differences in c-Fos expression may relate to the behavioral relevance of the chemosensory stimulus, including odor neophobia. In a two-bottle brief-access preference task, rats preferred water to isoamyl acetate-odorized water over multiple days. However, after experience with isoamyl acetate mixed with sucrose (odor-taste mixture), the preference for water was eliminated. These findings demonstrate that experience with chemosensory stimuli modulates responses in the mediodorsal thalamus, suggesting this structure plays an integral role in communicating behaviorally relevant chemosensory information to higher order areas to guide food-related behaviors.