TY - JOUR
T1 - Mechanosensory-Based Phase Coding of Odor Identity in the Olfactory Bulb
AU - Iwata, Ryo
AU - Kiyonari, Hiroshi
AU - Imai, Takeshi
N1 - Funding Information:
We thank Momo Fujii, Naho Atsumi, and Miwako Nomura for technical assistance; Kazushige Touhara for instruction on artificial sniffing; Takashi R. Sato and Tatsuo K. Sato for instruction on imaging in awake mice; Mineto Yokoi, Hongkui Zeng, and Karel Svoboda for mouse strains; and Marcus N. Leiwe, Takashi R. Sato, Keiji Miura, and Charles Yokoyama for critical reading of the manuscript. This work was supported by grants from the PRESTO program of the Japan Science and Technology Corporation (JST) (T.I.), the Sumitomo Foundation (T.I.), the Nakajima Foundation (T.I.), the Brain Science Foundation (T.I.), and the Japan Society for the Promotion of Science (JSPS) (KAKENHI 23680038 , 15H05572 , 15K14336 , 16K14568 , 16H06456 , and 17H06261 to T.I.; 15K18353 to R.I.), and an intramural grant from RIKEN Center for Developmental Biology (T.I.). R.I. was supported by the Special Postdoctoral Researchers program of RIKEN and the JSPS postdoctoral fellowship. The imaging experiments were supported by the RIKEN Kobe Light Microscopy Facility. Animal experiments were supported by the Animal Resource Development Unit at the RIKEN Center for Life Science Technologies.
Publisher Copyright:
© 2017 Elsevier Inc.
PY - 2017/12/6
Y1 - 2017/12/6
N2 - Mitral and tufted (M/T) cells in the olfactory bulb produce rich temporal patterns of activity in response to different odors. However, it remains unknown how these temporal patterns are generated and how they are utilized in olfaction. Here we show that temporal patterning effectively discriminates between the two sensory modalities detected by olfactory sensory neurons (OSNs): odor and airflow-driven mechanical signals. Sniff-induced mechanosensation generates glomerulus-specific oscillatory activity in M/T cells, whose phase was invariant across airflow speed. In contrast, odor stimulation caused phase shifts (phase coding). We also found that odor-evoked phase shifts are concentration invariant and stable across multiple sniff cycles, contrary to the labile nature of rate coding. The loss of oscillatory mechanosensation impaired the precision and stability of phase coding, demonstrating its role in olfaction. We propose that phase, not rate, coding is a robust encoding strategy of odor identity and is ensured by airflow-induced mechanosensation in OSNs. Iwata et al. demonstrate that phase coding, but not rate coding, in mitral cells is useful for concentration-invariant odor identity coding. They also found that mechanosensation in olfactory sensory neurons facilitates, rather than masks, the robust phase coding of odors.
AB - Mitral and tufted (M/T) cells in the olfactory bulb produce rich temporal patterns of activity in response to different odors. However, it remains unknown how these temporal patterns are generated and how they are utilized in olfaction. Here we show that temporal patterning effectively discriminates between the two sensory modalities detected by olfactory sensory neurons (OSNs): odor and airflow-driven mechanical signals. Sniff-induced mechanosensation generates glomerulus-specific oscillatory activity in M/T cells, whose phase was invariant across airflow speed. In contrast, odor stimulation caused phase shifts (phase coding). We also found that odor-evoked phase shifts are concentration invariant and stable across multiple sniff cycles, contrary to the labile nature of rate coding. The loss of oscillatory mechanosensation impaired the precision and stability of phase coding, demonstrating its role in olfaction. We propose that phase, not rate, coding is a robust encoding strategy of odor identity and is ensured by airflow-induced mechanosensation in OSNs. Iwata et al. demonstrate that phase coding, but not rate coding, in mitral cells is useful for concentration-invariant odor identity coding. They also found that mechanosensation in olfactory sensory neurons facilitates, rather than masks, the robust phase coding of odors.
UR - http://www.scopus.com/inward/record.url?scp=85037364278&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85037364278&partnerID=8YFLogxK
U2 - 10.1016/j.neuron.2017.11.008
DO - 10.1016/j.neuron.2017.11.008
M3 - Article
C2 - 29216451
AN - SCOPUS:85037364278
VL - 96
SP - 1139-1152.e7
JO - Neuron
JF - Neuron
SN - 0896-6273
IS - 5
ER -