Topological Reorganization of Odor Representations in the Olfactory Bulb

Abstract

Odors are initially represented in the olfactory bulb (OB) by patterns of sensory input across the array of glomeruli. Although activated glomeruli are often widely distributed, glomeruli responding to stimuli sharing molecular features tend to be loosely clustered and thus establish a fractured chemotopic map. Neuronal circuits in the OB transform glomerular patterns of sensory input into spatiotemporal patterns of output activity and thereby extract information about a stimulus. It is, however, unknown whether the chemotopic spatial organization of glomerular inputs is maintained during these computations. To explore this issue, we measured spatiotemporal patterns of odor-evoked activity across thousands of individual neurons in the zebrafish OB by temporally deconvolved two-photon Ca ²⁺ imaging. Mitral cells and interneurons were distinguished by transgenic markers and exhibited different response selectivities. Shortly after response onset, activity patterns exhibited foci of activity associated with certain chemical features throughout all layers. During the subsequent few hundred milliseconds, however, MC activity was locally sparsened within the initial foci in an odor-specific manner. As a consequence, chemotopic maps disappeared and activity patterns became more informative about precise odor identity. Hence, chemotopic maps of glomerular input activity are initially transmitted to OB outputs, but not maintained during pattern processing. Nevertheless, transient chemotopic maps may support neuronal computations by establishing important synaptic interactions within the circuit. These results provide insights into the functional topology of neural activity patterns and its potential role in circuit function.

Author Summary

Many sensory brain areas contain topographic maps where the physical location of neuronal activity contains information about a stimulus feature. In the first central processing center of the olfactory pathway, the olfactory bulb, chemically distinct odors often elicit spatially segregated input activity so that general chemical features are initially represented in a topographic fashion. It is, however, unclear whether this “chemotopic” organization of odor representations is maintained at subsequent stages of odor processing. To address this question, we visualized activity patterns across thousands of individual neurons in the intact olfactory bulb of zebrafish over time using two-photon calcium imaging. Our results demonstrate that odor-evoked activity across the output neurons of the olfactory bulb is chemotopically organized shortly after stimulus onset but becomes more widely distributed during the subsequent few hundred milliseconds of the response. This reorganization of olfactory bulb output activity is most likely mediated by inhibitory feedback and reduces the redundancy in activity patterns evoked by related stimuli. These results indicate that topographically organized activity maps in the olfactory bulb are not maintained during information processing, but contribute to the function of local circuits.

Abstract

Two-photon calcium imaging in the zebrafish olfactory bulb reveals that mitral cells show more selective responses to odors than interneurons, and odor-evoked firing patterns of populations of mitral cells evolve over hundreds of milliseconds to become more distinct for different odors, thus providing more information about odor identity.