The fundamental role of memory in olfactory perception

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Abstract

Current emphasis on odorant physiochemical features as the basis for perception largely ignores the synthetic and experience-dependent nature of olfaction. Olfaction is synthetic, as mammals have only limited ability to identify elements within even simple odor mixtures. Furthermore, olfaction is experience-bound, as exposure alone can significantly affect the extent to which stimuli can be discriminated. We propose that early analytical processing of odors is inaccessible at the behavioral level and that all odors are initially encoded as ‘objects’ in the piriform cortex. Moreover, we suggest that odor perception is wholly dependent on the integrity of this memory system and that its loss severely impairs normal perception.

Section snippets

Synthetic olfactory perception

Synthetic odor processing is suggested by two types of finding. The first derives from experiments in which human participants are asked to identify the component parts of odor mixtures. Having first learned the labels for each of the odorants to be mixed, participants are presented with mixtures consisting of two or more constituents. Using a variety of different methods, participants can rarely identify an individual odor as being present when the mixture consists of three or more components

Memory and olfactory perception

Several lines of evidence show that olfactory perception is also heavily dependent on learning and memory. First, participants are initially poor at discriminating unfamiliar odors from each other, but they improve rapidly with exposure 16, 17. Second, the qualities that are described by participants when smelling an odor can be acquired. In a series of studies we have shown that unfamiliar odors paired with sweet tastes are thought to smell sweeter, and those paired with sour tastes, sourer

Olfactory sensory physiology

The relative behavioral inaccessibility of odorant features or odor-mixture component information, compared with the analytical abilities of other sensory systems, might reflect the unique shortened receptor-to-cortex pathway of the olfactory system (there is no thalamic relay between second-order neurons and the primary sensory cortex). In addition, or alternatively, it might reflect coding strategies required for processing of complex, dynamic olfactory stimuli that do not contain within

Cortical mechanisms of olfactory perceptual learning

Based on new data that extend the theoretical work of previous investigators 39, 40, 41, 42, we propose that the olfactory bulb circuitry creates odor-specific spatial–temporal patterns that are synthesized and stored in the piriform cortex through Hebbian synaptic plasticity (Fig. 3). The anatomical basis for such synthesis exists both in the projection of mitral cells conveying receptor-specific input that converges in overlapping terminal patches on the anterior piriform cortex [43] and,

Concluding remarks

Together, these new behavioral and neurophysiological results show a strong synthetic component to odor discrimination that is inconsistent with a highly analytical, feature-detecting system. Cortical synthetic processing has the adaptive advantage of allowing identification of, and discrimination between, a broad range of complex odorants containing novel combinations of features, in addition to allowing recognition of partially degraded familiar inputs. Thus, rapid perceptual learning, based

Acknowledgements

Our work was supported by grants from the National Institute on Deafness and Communication Disorders and the National Science Foundation (D.A.W.) and from the Australian Research Council and Macquarie University (R.J.S.).

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