Tuning and Topography in an Odor Map on the Rat Olfactory Bulb

Abstract

The sense of smell originates in a diverse array of receptor neurons, comprising up to 1000 different types. To understand how these parallel channels encode chemical stimuli, we recorded the responses of glomeruli in the olfactory bulbs of the anesthetized rat, by optical imaging of intrinsic signals. Odor stimulation produced two kinds of optical responses at the surface of the bulb: a broad diffuse component superposed by discrete small spots. Histology showed that the spots correspond to individual glomeruli, and that ∼400 of them can be monitored in this way. Based on its wavelength-dependence, this optical signal appears to derive from changes in light scattering during neural activity. Pure odorants generally activated several glomeruli in a bilaterally symmetric pattern, whose extent varied greatly with concentration. A simple formalism for ligand binding accounts quantitatively for this concentration dependence and yields the effective affinity with which a glomerulus responds to an odorant. When tested with aliphatic molecules of increasing carbon chain length, many glomeruli were sharply tuned for one or two adjacent chain lengths. Glomeruli with similar tuning properties were located near each other, producing a systematic map of molecular chain length on the surface of the olfactory bulb. Given local inhibitory circuits within the olfactory bulb, this can account for the observed functional inhibition between related odors. We explore several parallels to the function and architecture of the visual system that help interpret the neural representation of odors.