Selective attention controls olfaction in rodents

Abstract

Critical animal behaviors, especially among rodents, are guided by odors in remarkably well-coordinated manners. While many extramodal sensory cues compete for cognitive resources in these ecological contexts, that rodents can engage in such odor-guided behaviors suggests that they selectively attend to odors. We developed an operant task to reveal that rats are indeed capable of selectively attending to odors in the presence of competing extramodal stimuli and found that this selective attention facilitates accurate odor-guided behavior. Further, we uncovered that attention to odors adaptively sharpens their representation among individual neurons in a brain region considered integral for odor-driven behaviors. Thus, selective attention contributes to olfaction in rodents in a manner analogous to that observed for other sensory systems in more cognitively-advanced animals. Main Text:From neonatal attachment and suckling responses (1-3), to selecting mates, finding food sources, and avoiding predators (4-6), rodent behavior is guided by olfactory stimuli in remarkably well-coordinated manners. The fact that these behaviors can be successfully orchestrated lends reason to believe that rodents must selectively attend to odors in these contexts at the expense of competing extramodal cues. For instance, during foraging for food and sniffing out food odors, a rat must simultaneously 'filter' out competing auditory and visual stimuli arising from irrelevant sources. While we know that rodents readily display shifting of attentional sets, including those involving odors (7), and even that they can display attention towards information from other modalities (8,9), whether selective attention regulates olfactory perception and odor coding remains unresolved. This question is of great importance given the prevalence of rodents as models for olfactory function and due to the fact that we know odordirected attention shapes olfaction in humans (10, 11).Given the aforementioned importance of olfaction for survival, we reasoned that olfactory brain centers would adaptively encode odor information in manners dependent upon attentional demands. Further, while there are many locations within the olfactory system which are modulated by attention in humans (10, 12) as a starting place to uncover cellular modulation by attention, we predicted that selective attention would shape the representation of odors within the ventral striatum (VS). This is reasonable given that the VS is a collection of brain regions important for evaluating sensory information in the context of motivated behaviors (13), a function considered integral for attention (14). Offering precedence for this is evidence provided by human functional imaging for increased hemodynamic responses to odors in the VS during attention (10,12), particularly in the olfactory tubercle region of the VS, which is extensively innervated by olfactory input (15,16). Notably, the olfactory system does not have a classic thalamic relay, a component widely considered to be integral to a...