Innate versus learned odour processing in the mouse olfactory bulb

Abstract

The mammalian olfactory system mediates various responses, including aversive behaviours to spoiled foods and fear responses to predator odours. In the olfactory bulb, each glomerulus represents a single species of odorant receptor. Because a single odorant can interact with several different receptor species, the odour information received in the olfactory epithelium is converted to a topographical map of multiple glomeruli activated in distinct areas in the olfactory bulb. To study how the odour map is interpreted in the brain, we generated mutant mice in which olfactory sensory neurons in a specific area of the olfactory epithelium are ablated by targeted expression of the diphtheria toxin gene. Here we show that, in dorsal-zone-depleted mice, the dorsal domain of the olfactory bulb was devoid of glomerular structures, although second-order neurons were present in the vacant areas. The mutant mice lacked innate responses to aversive odorants, even though they were capable of detecting them and could be conditioned for aversion with the remaining glomeruli. These results indicate that, in mice, aversive information is received in the olfactory bulb by separate sets of glomeruli, those dedicated for innate and those for learned responses. The mouse pictured knows no fear. More precisely, it cannot display the innate behavioural responses to aversive odours that normally protect mice from spoiled food or a predator. In this mouse the olfactory sensory neurons in an area of the olfactory epithelium, the odour-sensitive epithelial tissue inside the nasal cavity, have been ablated by targeted expression of the diphtheria toxin gene. Though lacking innate aversive behaviour, the mouse can still detect the aversive odours, and can be conditioned for aversion. These results suggest that like the immune system, the mouse olfactory system possesses 'hard-wired' genetically programmed neural circuits in parallel with adaptive circuits acquired later and hooked up to the innate system.