Application of optogenetic technology in the research on olfactory bulb neural projection from advanced brain regions to regulate olfactory signal processing_Journal of Biomedical Engineering

Authors：

ZHOU Tong , WU Yifan , HU Meng , TANG Xin , ZHU Ping , DU Liping ,  WU Chunsheng

Institute of Medical Engineering, Department of Biophysics, School of Basic Medicine, Xi'an Jiaotong University, Xi'an 710061, P. R. China;

Corresponding author：

Keywords：

Photogenetics; Olfactory bulb; Neural projection; Neural circuit; Olfactory signal

DOI：

10.7507/1001-5515.202404009

Video：

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Olfactory bulb is a critical component in encoding and processing olfactory signals, characterized by its intricate neural projections and networks dedicated to this function. It has been found that descending neural projections from the olfactory cortex and other advanced brain regions can modulate the excitability of olfactory bulb output neurons in the olfactory bulb, either directly or indirectly, which can further influence olfactory discrimination, learning, and other abilities. In recent years, advancements in optogenetic technology have facilitated extensive application of neuron manipulation for studying neural circuits, thereby greatly accelerating research into olfactory mechanisms. This review summarizes the latest research progress on the regulatory effects of neural projections from the olfactory cortex, basal forebrain, raphe nucleus, and locus coeruleus on olfactory bulb function. Furthermore, the important role that photogenetic technology plays in olfactory mechanism research is evaluated. Finally, the existing problems and future development trends in current research are preliminarily proposed and explained. This review aims to provide new insights into the mechanisms underlying olfactory neural regulation as well as applications of optogenetic technology, which are crucial for advancing the research on olfactory mechanism and the application of optogenetic technology.

Citation： ZHOU Tong, WU Yifan, HU Meng, TANG Xin, ZHU Ping, DU Liping, WU Chunsheng. Application of optogenetic technology in the research on olfactory bulb neural projection from advanced brain regions to regulate olfactory signal processing. Journal of Biomedical Engineering, 2024, 41(6): 1265-1270. doi: 10.7507/1001-5515.202404009 Copy

1.	Kurian S M, Naressi R G, Manoel D, et al. Odor coding in the mammalian olfactory epithelium. Cell Tissue Res, 2021, 383(1): 445-456.
2.	Cinelli A R, Ferreyra-Moyano H, Barragan E. Reciprocal functional connections of the olfactory bulbs and other olfactory related areas with the prefrontal cortex. Brain Res. Bull., 1987, 19(6): 651-661.
3.	Qi M, Fadool D A, Storace D A. An anatomically distinct subpopulation of orexin neurons project from the lateral hypothalamus to the olfactory bulb. J Comp Neurol, 2023, 531(15): 1510-1524.
4.	Gonzalez J, Torterolo P, Tort A B L. Mechanisms and functions of respiration-driven gamma oscillations in the primary olfactory cortex. Elife, 2023, 12: e83044.
5.	Wang D, Wu J, Liu P, et al. VIP interneurons regulate olfactory bulb output and contribute to odor detection and discrimination. Cell Rep, 2022, 38(7): 110383.
6.	Schreck M R, Zhuang L, Janke E, et al. State-dependent olfactory processing in freely behaving mice. Cell Rep, 2022, 38(9): 110450.
7.	Dalal T, Haddad R. Upstream γ-synchronization enhances odor processing in downstream neurons. Cell Rep, 2022, 39(3): 110693.
8.	Bagur S, Lefort J M, Lacroix M M, et al. Breathing-driven prefrontal oscillations regulate maintenance of conditioned-fear evoked freezing independently of initiation. Nat Commun, 2021, 12(1): 2605.
9.	Wang L, Li X, Chen F, et al. Organizational principles of the centrifugal projections to the olfactory bulb. Int J Mol Sci, 2023, 24(5): 4579.
10.	Kharlamova A S, Godovalova O S, Otlyga E G, et al. Primary and secondary olfactory centres in human ontogeny. Neurosci Res, 2023, 190: 1-16.
11.	Brunert D, Medinaceli Quintela R, Rothermel M. The anterior olfactory nucleus revisited - An emerging role for neuropathological conditions?. Prog Neurobiol, 2023, 228: 102486.
12.	Kostka J K, Hanganu-Opatz I L. Olfactory-driven beta band entrainment of limbic circuitry during neonatal development. J Physiol, 2023, 601(16): 3605-3630.
13.	Diaz C, Franks K M, Blazing R M. Neuroscience: Seq-ing maps in the olfactory cortex. Curr Biol, 2023, 33(7): R266-R269.
14.	Poo C, Agarwal G, Bonacchi N, et al. Spatial maps in piriform cortex during olfactory navigation. Nature, 2022, 601(7894): 595-599.
15.	Chen Y, Chen X, Baserdem B, et al. High-throughput sequencing of single neuron projections reveals spatial organization in the olfactory cortex. Cell, 2022, 185(22): 4117-4134.
16.	Li Q, Takeuchi Y, Wang J, et al. Reinstating olfactory bulb-derived limbic gamma oscillations alleviates depression-like behavioral deficits in rodents. Neuron, 2023, 111(13): 2065-2075.
17.	Wang C Y, Liu Z, Ng Y H, et al. A synaptic circuit required for acquisition but not recall of social transmission of food preference. Neuron, 2020, 107(1): 144-157.
18.	Mazo C, Lepousez G, Nissant A, et al. GABAB receptors tune cortical feedback to the olfactory bulb. J Neurosci. 2016, 36(32): 8289-8304.
19.	Mazo C, Nissant A, Saha S, et al. Long-range GABAergic projections contribute to cortical feedback control of sensory processing. Nat Commun, 2022, 13(1): 6879.
20.	Terral G, Harrell E, Lepousez G, et al. Endogenous cannabinoids in the piriform cortex tune olfactory perception. Nat Commun, 2024, 15(1): 1230.
21.	Soria-Gómez E, Bellocchio L, Reguero L, et al. The endocannabinoid system controls food intake via olfactory processes. Nat. Neurosci., 2014, 17(3): 407-415.
22.	Hook C, Puche A C. Bulbar projecting subcortical GABAergic neurons send collateral branches extensively and selectively to primary olfactory cortical regions. J Comp Neurol, 2023, 531(3): 451-460.
23.	Lepousez G, Nissant A, Bryant A K, et al. Olfactory learning promotes input-specific synaptic plasticity in adult-born neurons. Proc Natl Acad Sci U S A, 2014, 111(38): 13984-13989.
24.	Oboti L, Sokolowski K. Gradual wiring of olfactory input to amygdala feedback circuits. Sci Rep, 2020, 10(1): 5871.
25.	Venegas J P, Navarrete M, Orellana-Garcia L, et al. Basal forebrain modulation of olfactory coding in vivo. Int J Psychol Res (Medellin), 2023, 16(2): 62-86.
26.	Ma M, Luo M. Optogenetic activation of basal forebrain cholinergic neurons modulates neuronal excitability and sensory responses in the main olfactory bulb. J Neurosci., 2012, 32(30): 10105-10116.
27.	Rothermel M, Carey R M, Puche A, et al. Cholinergic inputs from Basal forebrain add an excitatory bias to odor coding in the olfactory bulb. J Neurosci, 2014, 34(13): 4654-4664.
28.	Hanson E, Brandel-Ankrapp K L, Arenkiel B R. Dynamic cholinergic tone in the basal forebrain reflects reward-seeking and reinforcement during olfactory behavior. Front Cell Neurosci. 2021, 15: 635837.
29.	Yun Y, Wang X, Xu J, et al. Optogenetic stimulation of basal forebrain cholinergic neurons prevents neuroinflammation and neuropsychiatric manifestations in pristane induced lupus mice. Behav Brain Funct, 2023, 19(1): 11.
30.	Villar P S, Hu R, Araneda R C. Long-range GABAergic inhibition modulates spatiotemporal dynamics of the output neurons in the olfactory bulb. J Neurosci, 2021, 41(16): 3610-3621.
31.	Case D T, Burton S D, Gedeon J Y, et al. Layer- and cell type-selective co-transmission by a basal forebrain cholinergic projection to the olfactory bulb. Nat Commun, 2017, 8(1): 652.
32.	De Saint Jan D. Target-specific control of olfactory bulb periglomerular cells by GABAergic and cholinergic basal forebrain inputs. Elife, 2022, 11: e71965.
33.	Kapoor V, Provost A C, Agarwal P, et al. Activation of raphe nuclei triggers rapid and distinct effects on parallel olfactory bulb output channels. Nat Neurosci, 2016, 19(2): 271-282.
34.	Piszár I, Lőrincz M L. Differential serotonergic modulation of synaptic inputs to the olfactory cortex. Int J Mol Sci, 2023, 24(3): 1950.
35.	魏梦霞, 纪树钦, 李子杰, 等. 脑干蓝斑到前庭神经核的神经环路投射及在压力应激下的激活研究. 集成技术, 2021, 10(5): 12-22.
36.	高晴, 张颖颍, 王肖莹, 等. 蓝斑损伤介导帕金森病疼痛病理机制的研究进展. 神经疾病与精神卫生, 2022, 22(7): 517-521.
37.	Ramirez-Gordillo D, Ma M, Restrepo D. Precision of classification of odorant value by the power of olfactory bulb oscillations is altered by optogenetic silencing of local adrenergic innervation. Front Cell Neurosci, 2018, 12: 48.
38.	Linster C, Midroit M, Forest J, et al. Noradrenergic activity in the olfactory bulb is a key element for the stability of olfactory memory. J Neurosci, 2020, 40(48): 9260-9271.
39.	Yeon C, Im J M, Kim M, et al. Cranial and spinal window preparation for in vivo optical neuroimaging in rodents and related experimental t echniques. Exp Neurobiol, 2022, 31(3): 131-146.

1. Kurian S M, Naressi R G, Manoel D, et al. Odor coding in the mammalian olfactory epithelium. Cell Tissue Res, 2021, 383(1): 445-456.
2. Cinelli A R, Ferreyra-Moyano H, Barragan E. Reciprocal functional connections of the olfactory bulbs and other olfactory related areas with the prefrontal cortex. Brain Res. Bull., 1987, 19(6): 651-661.
3. Qi M, Fadool D A, Storace D A. An anatomically distinct subpopulation of orexin neurons project from the lateral hypothalamus to the olfactory bulb. J Comp Neurol, 2023, 531(15): 1510-1524.
4. Gonzalez J, Torterolo P, Tort A B L. Mechanisms and functions of respiration-driven gamma oscillations in the primary olfactory cortex. Elife, 2023, 12: e83044.
5. Wang D, Wu J, Liu P, et al. VIP interneurons regulate olfactory bulb output and contribute to odor detection and discrimination. Cell Rep, 2022, 38(7): 110383.
6. Schreck M R, Zhuang L, Janke E, et al. State-dependent olfactory processing in freely behaving mice. Cell Rep, 2022, 38(9): 110450.
7. Dalal T, Haddad R. Upstream γ-synchronization enhances odor processing in downstream neurons. Cell Rep, 2022, 39(3): 110693.
8. Bagur S, Lefort J M, Lacroix M M, et al. Breathing-driven prefrontal oscillations regulate maintenance of conditioned-fear evoked freezing independently of initiation. Nat Commun, 2021, 12(1): 2605.
9. Wang L, Li X, Chen F, et al. Organizational principles of the centrifugal projections to the olfactory bulb. Int J Mol Sci, 2023, 24(5): 4579.
10. Kharlamova A S, Godovalova O S, Otlyga E G, et al. Primary and secondary olfactory centres in human ontogeny. Neurosci Res, 2023, 190: 1-16.
11. Brunert D, Medinaceli Quintela R, Rothermel M. The anterior olfactory nucleus revisited - An emerging role for neuropathological conditions?. Prog Neurobiol, 2023, 228: 102486.
12. Kostka J K, Hanganu-Opatz I L. Olfactory-driven beta band entrainment of limbic circuitry during neonatal development. J Physiol, 2023, 601(16): 3605-3630.
13. Diaz C, Franks K M, Blazing R M. Neuroscience: Seq-ing maps in the olfactory cortex. Curr Biol, 2023, 33(7): R266-R269.
14. Poo C, Agarwal G, Bonacchi N, et al. Spatial maps in piriform cortex during olfactory navigation. Nature, 2022, 601(7894): 595-599.
15. Chen Y, Chen X, Baserdem B, et al. High-throughput sequencing of single neuron projections reveals spatial organization in the olfactory cortex. Cell, 2022, 185(22): 4117-4134.
16. Li Q, Takeuchi Y, Wang J, et al. Reinstating olfactory bulb-derived limbic gamma oscillations alleviates depression-like behavioral deficits in rodents. Neuron, 2023, 111(13): 2065-2075.
17. Wang C Y, Liu Z, Ng Y H, et al. A synaptic circuit required for acquisition but not recall of social transmission of food preference. Neuron, 2020, 107(1): 144-157.
18. Mazo C, Lepousez G, Nissant A, et al. GABAB receptors tune cortical feedback to the olfactory bulb. J Neurosci. 2016, 36(32): 8289-8304.
19. Mazo C, Nissant A, Saha S, et al. Long-range GABAergic projections contribute to cortical feedback control of sensory processing. Nat Commun, 2022, 13(1): 6879.
20. Terral G, Harrell E, Lepousez G, et al. Endogenous cannabinoids in the piriform cortex tune olfactory perception. Nat Commun, 2024, 15(1): 1230.
21. Soria-Gómez E, Bellocchio L, Reguero L, et al. The endocannabinoid system controls food intake via olfactory processes. Nat. Neurosci., 2014, 17(3): 407-415.
22. Hook C, Puche A C. Bulbar projecting subcortical GABAergic neurons send collateral branches extensively and selectively to primary olfactory cortical regions. J Comp Neurol, 2023, 531(3): 451-460.
23. Lepousez G, Nissant A, Bryant A K, et al. Olfactory learning promotes input-specific synaptic plasticity in adult-born neurons. Proc Natl Acad Sci U S A, 2014, 111(38): 13984-13989.
24. Oboti L, Sokolowski K. Gradual wiring of olfactory input to amygdala feedback circuits. Sci Rep, 2020, 10(1): 5871.
25. Venegas J P, Navarrete M, Orellana-Garcia L, et al. Basal forebrain modulation of olfactory coding in vivo. Int J Psychol Res (Medellin), 2023, 16(2): 62-86.
26. Ma M, Luo M. Optogenetic activation of basal forebrain cholinergic neurons modulates neuronal excitability and sensory responses in the main olfactory bulb. J Neurosci., 2012, 32(30): 10105-10116.
27. Rothermel M, Carey R M, Puche A, et al. Cholinergic inputs from Basal forebrain add an excitatory bias to odor coding in the olfactory bulb. J Neurosci, 2014, 34(13): 4654-4664.
28. Hanson E, Brandel-Ankrapp K L, Arenkiel B R. Dynamic cholinergic tone in the basal forebrain reflects reward-seeking and reinforcement during olfactory behavior. Front Cell Neurosci. 2021, 15: 635837.
29. Yun Y, Wang X, Xu J, et al. Optogenetic stimulation of basal forebrain cholinergic neurons prevents neuroinflammation and neuropsychiatric manifestations in pristane induced lupus mice. Behav Brain Funct, 2023, 19(1): 11.
30. Villar P S, Hu R, Araneda R C. Long-range GABAergic inhibition modulates spatiotemporal dynamics of the output neurons in the olfactory bulb. J Neurosci, 2021, 41(16): 3610-3621.
31. Case D T, Burton S D, Gedeon J Y, et al. Layer- and cell type-selective co-transmission by a basal forebrain cholinergic projection to the olfactory bulb. Nat Commun, 2017, 8(1): 652.
32. De Saint Jan D. Target-specific control of olfactory bulb periglomerular cells by GABAergic and cholinergic basal forebrain inputs. Elife, 2022, 11: e71965.
33. Kapoor V, Provost A C, Agarwal P, et al. Activation of raphe nuclei triggers rapid and distinct effects on parallel olfactory bulb output channels. Nat Neurosci, 2016, 19(2): 271-282.
34. Piszár I, Lőrincz M L. Differential serotonergic modulation of synaptic inputs to the olfactory cortex. Int J Mol Sci, 2023, 24(3): 1950.
35. 魏梦霞, 纪树钦, 李子杰, 等. 脑干蓝斑到前庭神经核的神经环路投射及在压力应激下的激活研究. 集成技术, 2021, 10(5): 12-22.
36. 高晴, 张颖颍, 王肖莹, 等. 蓝斑损伤介导帕金森病疼痛病理机制的研究进展. 神经疾病与精神卫生, 2022, 22(7): 517-521.
37. Ramirez-Gordillo D, Ma M, Restrepo D. Precision of classification of odorant value by the power of olfactory bulb oscillations is altered by optogenetic silencing of local adrenergic innervation. Front Cell Neurosci, 2018, 12: 48.
38. Linster C, Midroit M, Forest J, et al. Noradrenergic activity in the olfactory bulb is a key element for the stability of olfactory memory. J Neurosci, 2020, 40(48): 9260-9271.
39. Yeon C, Im J M, Kim M, et al. Cranial and spinal window preparation for in vivo optical neuroimaging in rodents and related experimental t echniques. Exp Neurobiol, 2022, 31(3): 131-146.

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