Profound Context-Dependent Plasticity of Mitral Cell Responses in Olfactory Bulb

Abstract

On the basis of its primary circuit it has been postulated that the olfactory bulb (OB) is analogous to the retina in mammals. In retina, repeated exposure to the same visual stimulus results in a neural representation that remains relatively stable over time, even as the meaning of that stimulus to the animal changes. Stability of stimulus representation at early stages of processing allows for unbiased interpretation of incoming stimuli by higher order cortical centers. The alternative is that early stimulus representation is shaped by previously derived meaning, which could allow more efficient sampling of odor space providing a simplified yet biased interpretation of incoming stimuli. This study helps place the olfactory system on this continuum of subjective versus objective early sensory representation. Here we show that odor responses of the output cells of the OB, mitral cells, change transiently during a go–no-go odor discrimination task. The response changes occur in a manner that increases the ability of the circuit to convey information necessary to discriminate among closely related odors. Remarkably, a switch between which of the two odors is rewarded causes mitral cells to switch the polarity of their divergent responses. Taken together these results redefine the function of the OB as a transiently modifiable (active) filter, shaping early odor representations in behaviorally meaningful ways.

Author Summary

The way in which the brain represents and processes sensory information remains a fundamental question. One model posits that stable neural representation of a stimulus during early stages of stimulus processing allows for unbiased interpretation of incoming stimuli by higher order cortical centers. Alternately, early stimulus representation could be shaped by previous experience, thus providing a biased yet relevant interpretation of incoming stimuli. This study examines the activity of output cells, mitral cells, from the first stage of odor information processing in the olfactory bulb during an odor discrimination task. We found that odor responses changed during the task in a manner that increased the ability of the circuit to convey information necessary to discriminate among closely related odors. A switch between which of the two odors were rewarded caused mitral cells to switch the polarity of their divergent responses in behaviorally relevant ways. These results show that early neural representations of odor can be shaped by previously derived meaning, providing a simplified yet biased interpretation of the odor environment to higher cortical structures.

Abstract

Early neural representation of odor can be shaped by previously derived meaning, providing a simplified yet biased interpretation of the odor environment to higher cortical structures.