Broad activation of the olfactory bulb produces long-lasting changes in odor perception

Abstract

A number of electrophysiological experiments have shown that odor exposure alone, unaccompanied by behavioral training, changes the response patterns of neurons in the olfactory bulb. As a consequence of these changes, across mitral cells in the olfactory bulb, individual odors should be better discriminated because of previous exposure. We have previously shown that a daily 2-h exposure to odorants during 2 weeks enhances rats' ability to discriminate between chemically similar odorants. Here, we first show that the perception of test odorants is only modulated by enrichment with odorants that activate at least partially overlapping regions of the olfactory bulb. Second, we show that a broad activation of olfactory bulb neurons by daily local infusion of NMDA into both olfactory bulbs enhances the discrimination between chemically related odorants in a manner similar to the effect of daily exposure to odorants. Computational modeling of the olfactory bulb suggests that activity-dependent plasticity in the olfactory bulb can support the observed modulation in olfactory discrimination capability by enhancing contrast and synchronization in the olfactory bulb. Last, we show that blockade of NMDA receptors in the olfactory bulb impairs the effects of daily enrichment, suggesting that NMDA-dependent plasticity is involved in the changes in olfactory processing observed here. discrimination ͉ enrichment ͉ plasticity B ehavioral enrichment is thought to be a major modulator of animals' ability to learn behavioral tasks. It has been shown many times that an enriched environment during development dramatically increases animals' learning and memory abilities during adult life (1, 2). Enrichment during adult life can counteract learning disabilities due to absence of NMDA receptors in genetically modified mice (3), as well as the decrease in learning capabilities seen in older rodents (4,5). Most studies investigating the beneficial effects of enriched housing environments focus on complex learning tasks such as the Morris water maze (5-7) or the Hebb-Williams maze (8) that have been linked to hippocampal function (9-11). In contrast to previous studies, we here focus on sensory perception, a predeterminant of all learning tasks in animals. Using olfactory perception in rats, we have recently shown for the first time that sensory enrichment during a relatively short period improves animals' sensory discrimination capabilities in an odor-unspecific manner (12). Here, we show that the modulation of olfactory discrimination abilities due to daily enrichment with odorants arises in the first olfactory sensory structure, the olfactory bulb (OB). First, we show that enrichment only affects the perception of those odorants that activate at least partially overlapping regions of the OB, suggesting that nonspecific activation of OB neurons suffices to produce lasting changes in perception and that spatial specificity of odor responses is of importance in this process. Second, we show that unspecific activation of OB neurons via l...

Olfactory perceptual learning requires adult neurogenesis

“…We have shown that odor enrichment enhances rats' ability to discriminate between chemically similar odorants in a relatively odor-unspecific manner (5,6). Indeed, the discrimination of a pair of similar odorants is improved by enrichment with the same odorants or with other odorants that activate regions of the OB partially overlapping with the regions activated by the discriminated pair.…”

“…For instance, animals trained on a tactile discrimination task improve their behavioral performances and in parallel, the neural representation of the stimuli is sharpened (2,3). In the olfactory modality, perceptual learning has been shown to occur in humans (4), and an experimental model of olfactory perceptual learning has recently been proposed in rats (5). Olfactory perceptual learning is crucial for basic olfactory functions because it sets the degree of discrimination between stimuli, and thus contributes to the perceptual representation of the environment, which guides the animal's behavior.…”

“…Indeed, the discrimination of a pair of similar odorants is improved by enrichment with the same odorants or with other odorants that activate regions of the OB partially overlapping with the regions activated by the discriminated pair. Even if the mechanisms underlying this learning remain unclear, it has been shown that infusions of NMDA into the OB improves odor discrimination in a manner similar to odor enrichment indicating that changes in OB processing contribute at least partially to the perceptual plasticity (5). A computational model proposed that activation of OB neurons produces widespread changes in inhibitory processing, which can underlie the observed improvement of odor discrimination (5).…”

“…Even if the mechanisms underlying this learning remain unclear, it has been shown that infusions of NMDA into the OB improves odor discrimination in a manner similar to odor enrichment indicating that changes in OB processing contribute at least partially to the perceptual plasticity (5). A computational model proposed that activation of OB neurons produces widespread changes in inhibitory processing, which can underlie the observed improvement of odor discrimination (5). In support to this model, odor exposure has been shown to increase inhibition of mitral cells (7) and to increase the responsiveness of the inhibitory granule cells to odorants, as measured by expression of an immediate early gene (8).…”

Functional units in the olfactory system

“…Although early bulb ablation studies, most of which were not guided by knowledge of actual odorant responses, questioned the relevance of domain organization in the olfactory bulb, more recent interventive experiments have confirmed the critical involvement of spatially restricted regions in the perception of particular odorants. Pharmacological blockade of dorsal bulbar activity interferes with experiencedependent modification of responses to odorants whose activity involves those dorsal regions, but it does not affect responses to odorants activating only the ventral part of the bulb (9). Chemical ablation of particular domains in the epithelium diminishes responses to odorants expected to be represented in those regions but does not diminish responses to odorants expected to activate intact regions (10).…”