Shaping the Olfactory Map: Cell Type-specific Activity Patterns Guide Circuit Formation

Overview

Journal Front Neural Circuits

Date 2024 Jun 11

PMID 38860141

Authors

Ai Nakashima

Haruki Takeuchi

Affiliations

Soon will be listed here.

Abstract

The brain constructs spatially organized sensory maps to represent sensory information. The formation of sensory maps has traditionally been thought to depend on synchronous neuronal activity. However, recent evidence from the olfactory system suggests that cell type-specific temporal patterns of spontaneous activity play an instructive role in shaping the olfactory glomerular map. These findings challenge traditional views and highlight the importance of investigating the spatiotemporal dynamics of neural activity to understand the development of complex neural circuits. This review discusses the implications of new findings in the olfactory system and outlines future research directions.

References

Martini F, Guillamon-Vivancos T, Moreno-Juan V, Valdeolmillos M, Lopez-Bendito G . Spontaneous activity in developing thalamic and cortical sensory networks. Neuron. 2021; 109(16):2519-2534. PMC: 7611560. DOI: 10.1016/j.neuron.2021.06.026. View

Buck L, Axel R . A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 1991; 65(1):175-87. DOI: 10.1016/0092-8674(91)90418-x. View

Katz L, Shatz C . Synaptic activity and the construction of cortical circuits. Science. 1996; 274(5290):1133-8. DOI: 10.1126/science.274.5290.1133. View

Malnic B, Hirono J, Sato T, Buck L . Combinatorial receptor codes for odors. Cell. 1999; 96(5):713-23. DOI: 10.1016/s0092-8674(00)80581-4. View

Yu C, Power J, Barnea G, ODonnell S, Brown H, Osborne J . Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron. 2004; 42(4):553-66. DOI: 10.1016/s0896-6273(04)00224-7. View

St John J, Clarris H, McKeown S, Royal S, Key B . Sorting and convergence of primary olfactory axons are independent of the olfactory bulb. J Comp Neurol. 2003; 464(2):131-40. DOI: 10.1002/cne.10777. View

Meister M, Wong R, Baylor D, Shatz C . Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science. 1991; 252(5008):939-43. DOI: 10.1126/science.2035024. View

Xing Y, Zan C, Liu L . Recent advances in understanding neuronal diversity and neural circuit complexity across different brain regions using single-cell sequencing. Front Neural Circuits. 2023; 17:1007755. PMC: 10097998. DOI: 10.3389/fncir.2023.1007755. View

Vaddadi N, Iversen K, Raja R, Phen A, Brignall A, Dumontier E . Kirrel2 is differentially required in populations of olfactory sensory neurons for the targeting of axons in the olfactory bulb. Development. 2019; 146(11). DOI: 10.1242/dev.173310. View

10.

Williams E, Sickles H, Dooley A, Palumbos S, Bisogni A, Lin D . Delta Protocadherin 10 is Regulated by Activity in the Mouse Main Olfactory System. Front Neural Circuits. 2011; 5:9. PMC: 3159872. DOI: 10.3389/fncir.2011.00009. View

11.

Sakano H . Neural map formation in the mouse olfactory system. Neuron. 2010; 67(4):530-42. DOI: 10.1016/j.neuron.2010.07.003. View

12.

Mizuno H, Ikezoe K, Nakazawa S, Sato T, Kitamura K, Iwasato T . Patchwork-Type Spontaneous Activity in Neonatal Barrel Cortex Layer 4 Transmitted via Thalamocortical Projections. Cell Rep. 2018; 22(1):123-135. DOI: 10.1016/j.celrep.2017.12.012. View

13.

Anton-Bolanos N, Sempere-Ferrandez A, Guillamon-Vivancos T, Martini F, Perez-Saiz L, Gezelius H . Prenatal activity from thalamic neurons governs the emergence of functional cortical maps in mice. Science. 2019; 364(6444):987-990. PMC: 7611000. DOI: 10.1126/science.aav7617. View

14.

Zhang J, Ackman J, Xu H, Crair M . Visual map development depends on the temporal pattern of binocular activity in mice. Nat Neurosci. 2011; 15(2):298-307. PMC: 3267873. DOI: 10.1038/nn.3007. View

15.

Mombaerts P, Wang F, Dulac C, CHAO S, Nemes A, Mendelsohn M . Visualizing an olfactory sensory map. Cell. 1996; 87(4):675-86. DOI: 10.1016/s0092-8674(00)81387-2. View

16.

Feinstein P, Mombaerts P . A contextual model for axonal sorting into glomeruli in the mouse olfactory system. Cell. 2004; 117(6):817-31. DOI: 10.1016/j.cell.2004.05.011. View

17.

Spitzer N . Electrical activity in early neuronal development. Nature. 2006; 444(7120):707-12. DOI: 10.1038/nature05300. View

18.

Wong R, Meister M, Shatz C . Transient period of correlated bursting activity during development of the mammalian retina. Neuron. 1993; 11(5):923-38. DOI: 10.1016/0896-6273(93)90122-8. View

19.

Piwecka M, Rajewsky N, Rybak-Wolf A . Single-cell and spatial transcriptomics: deciphering brain complexity in health and disease. Nat Rev Neurol. 2023; 19(6):346-362. PMC: 10191412. DOI: 10.1038/s41582-023-00809-y. View

20.

Francia S, Lodovichi C . The role of the odorant receptors in the formation of the sensory map. BMC Biol. 2021; 19(1):174. PMC: 8394594. DOI: 10.1186/s12915-021-01116-y. View