Critical animal behaviors, especially among rodents, are guided by odors in remarkably well-coordinated manners, yet many extramodal sensory cues compete for cognitive resources in these ecological contexts. That rodents can engage in such odor-guided behaviors suggests that they can selectively attend to odors. Indeed, higher-order cognitive processes-such as learning, memory, decision making, and action selection-rely on the proper filtering of sensory cues based on their relative salience. We developed a behavioral paradigm to reveal that rats are capable of selectively attending to odors in the presence of competing extramodal stimuli. We found that this selective attention facilitates accurate odor-guided decisions, which become further strengthened with experience. Further, we uncovered that selective attention to odors adaptively sharpens their representation among neurons in the olfactory tubercle, an olfactory cortex region of the ventral striatum that is considered integral for evaluating sensory information in the context of motivated behaviors. Odor-directed selective attention exerts influences during moments of heightened odor anticipation and enhances odorant representation by increasing stimulus contrast in a signal-to-noise-type coding scheme. Together, these results reveal that rats engage selective attention to optimize olfactory outcomes. Further, our finding of attention-dependent coding in the olfactory tubercle challenges the notion that a thalamic relay is integral for the attentional control of sensory coding.
The olfactory tubercle (OT), a trilaminar structure located in the basal forebrain of mammals, is thought to play an important role in olfaction. While evidence has accumulated regarding the contributions of the OT to odor information processing, studies exploring the role of the OT in olfaction in awake animals remain unavailable. In the present study, we begin to address this void through multiday recordings of local field potential (LFP) activity within the OT of awake, freely exploring Long-Evans rats. We observed spontaneous OT LFP activity consisting of theta- (2-12 Hz), beta- (15-35 Hz) and gamma- (40-80 Hz) band activity, characteristic of previous reports of LFPs in other principle olfactory structures. Beta- and gamma-band powers were enhanced upon odor presentation. Simultaneous recordings of OT and upstream olfactory bulb (OB) LFPs revealed odor-evoked LFP power at statistically similar levels in both structures. Strong spectral coherence was observed between the OT and OB during both spontaneous and odor-evoked states. Furthermore, the OB theta rhythm more strongly cohered with the respiratory rhythm, and respiratory-coupled theta cycles in the OT occurred following theta cycles in the OB. Finally, we found that the animal's internal state modulated LFP activity in the OT. Together, these data provide initial insights into the network activity of the OT in the awake rat, including spontaneous rhythmicity, odor-evoked modulation, connectivity with upstream sensory input, and state-dependent modulation.
Intranasal trigeminal sensory input, often perceived as a burning, tingling, or stinging sensation, is well known to affect odor perception. While both anatomical and functional imaging data suggest that the influence of trigeminal stimuli on odor information processing may occur within the olfactory cortex, direct electrophysiological evidence for the encoding of trigeminal information at this level of processing is unavailable. Here, in agreement with human functional imaging studies, we found that 26% of neurons in the mouse piriform cortex (PCX) display modulation in firing to carbon dioxide (CO 2 ), an odorless stimulant with known trigeminal capacity. Interestingly, CO 2 was represented within the PCX by distinct temporal dynamics, differing from those evoked by odor. Experiments with ascending concentrations of isopentyl acetate, an odorant known to elicit both olfactory and trigeminal sensations, resulted in morphing of the temporal dynamics of stimulus-evoked responses. Whereas low concentrations of odorant evoked responses upon stimulus onset, high concentrations of odorant and/or CO 2 often evoked responses structured to stimulus offset. These physiological experiments in mice suggest that PCX neurons possess the capacity to encode for stimulus modality (olfactory vs trigeminal) by differential patterns of firing. These data provide mechanistic insights into the influences of trigeminal information on odor processing and place constraints on models of olfactory-trigeminal sensory integration.
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