Narrowly confined and glomerulus-specific onset latencies of odor-evoked calcium transients in the juxtaglomerular cells of the mouse main olfactory bulb

Abstract

Odor information is transmitted from olfactory sensory neurons to principal neurons at the glomeruli of the olfactory bulb. The intraglomerular neuronal circuit also includes hundreds of interneurons referred to as juxtaglomerular (JG) cells. Stimulus selectivity is well correlated among many JG cells that are associated with the same glomerulus, consistent with their highly homogeneous sensory inputs. However, much less is known about the temporal aspects of their activity, including the temporal coordination of their odor-evoked responses. As many JG cells within a glomerular module respond to the same stimulus, the extent to which their activity is temporally aligned will affect the temporal profile of their population inhibitory inputs. Using random-access high-speed two-photon microscopy, we recorded the odor-evoked calcium transients of mouse JG cells and compared the onset latency and rise time among neurons putatively associated with the same and different glomeruli. Whereas the overall onset latencies of odor-evoked transients were distributed across a ∼150 ms time window, those from cells putatively associated with the same glomerulus were confined to a much narrower window of several tens of milliseconds. This result suggests that onset latency primarily depends on the associated glomerulus. We also observed glomerular specificity in the rise time. The glomerulus-specific temporal pattern of odor-evoked activity implies that the temporal patterns of inputs from the intraglomerular circuit are unique to individual glomerulus–odor pairs, which may contribute to efficient shaping of the temporal pattern of activity in the principal neurons.

Significance Statement The sense of smell is essential for assessing chemicals in one’s atmospheric environment. In understanding the biological mechanisms by which humans and animals recognize various odorous chemicals, a key question is how the signals sent from the nose are transformed in the brain. In this work, we studied the temporal pattern of activity in interneurons that tune the sensory inputs to the principal (signal-carrying) neurons in the olfactory bulb via structures known as glomeruli. We found that the odor responses of these interneurons are precisely coordinated in time, suggesting that the glomerulus is a temporally well-organized unit. Our finding suggests that the temporal coordination of glomerular activity is important in signal transformation in the olfactory system.