Young Adult Born Neurons Enhance Hippocampal Dependent Performance Via Influences on Bilateral Networks

Overview

Journal Elife

Specialty Biology

Date 2016 Dec 4

PMID 27914197

Citations 25

Authors

Jia-Min Zhuo

Hua-An Tseng

Mitul Desai

Mark E Bucklin

Ali I Mohammed

Nick Tm Robinson

Edward S Boyden

Lara M Rangel

Alan P Jasanoff

Howard J Gritton

Xue Han

Affiliations

Soon will be listed here.

Abstract

Adult neurogenesis supports performance in many hippocampal dependent tasks. Considering the small number of adult-born neurons generated at any given time, it is surprising that this sparse population of cells can substantially influence behavior. Recent studies have demonstrated that heightened excitability and plasticity may be critical for the contribution of young adult-born cells for certain tasks. What is not well understood is how these unique biophysical and synaptic properties may translate to networks that support behavioral function. Here we employed a location discrimination task in mice while using optogenetics to transiently silence adult-born neurons at different ages. We discovered that adult-born neurons promote location discrimination during early stages of development but only if they undergo maturation during task acquisition. Silencing of young adult-born neurons also produced changes extending to the contralateral hippocampus, detectable by both electrophysiology and fMRI measurements, suggesting young neurons may modulate location discrimination through influences on bilateral hippocampal networks.

Citing Articles

The longitudinal behavioral effects of acute exposure to galactic cosmic radiation in female C57BL/6J mice: Implications for deep space missions, female crews, and potential antioxidant countermeasures.

Yun S, Kiffer F, Bancroft G, Guzman C, Soler I, Haas H J Neurochem. 2024; 169(1):e16225.

PMID: 39318241 PMC: 11658192. DOI: 10.1111/jnc.16225.

Genetic deletion of α7 nAChRs reduces hippocampal granule and pyramidal cell number in both sexes but impairs pattern separation in males only.

Letsinger A, Nacer S, Stevanovic K, Larson G, DeFilipp J, Cushman J Front Neurosci. 2023; 17:1244118.

PMID: 37746145 PMC: 10513752. DOI: 10.3389/fnins.2023.1244118.

Competition on presynaptic resources enhances the discrimination of interfering memories.

Fung C, Fukai T PNAS Nexus. 2023; 2(6):pgad161.

PMID: 37275260 PMC: 10235910. DOI: 10.1093/pnasnexus/pgad161.

Optimizing memory performance and emotional states: multi-level enhancement of adult hippocampal neurogenesis.

Li Y, Luo Y, Song J Curr Opin Neurobiol. 2023; 79:102693.

PMID: 36822141 PMC: 10023407. DOI: 10.1016/j.conb.2023.102693.

Chromatin Remodeling Factor SMARCA5 is Essential for Hippocampal Memory Maintenance via Metabolic Pathways in Mice.

Qu Y, Zhou N, Zhang X, Li Y, Xu X Neurosci Bull. 2023; 39(7):1087-1104.

PMID: 36807260 PMC: 10313638. DOI: 10.1007/s12264-023-01032-x.

References

Tashiro A, Makino H, Gage F . Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J Neurosci. 2007; 27(12):3252-9. PMC: 6672473. DOI: 10.1523/JNEUROSCI.4941-06.2007. View

Buzsaki G . Neural syntax: cell assemblies, synapsembles, and readers. Neuron. 2010; 68(3):362-85. PMC: 3005627. DOI: 10.1016/j.neuron.2010.09.023. View

Desai M, Kahn I, Knoblich U, Bernstein J, Atallah H, Yang A . Mapping brain networks in awake mice using combined optical neural control and fMRI. J Neurophysiol. 2010; 105(3):1393-405. PMC: 3074423. DOI: 10.1152/jn.00828.2010. View

Kropff E, Yang S, Schinder A . Dynamic role of adult-born dentate granule cells in memory processing. Curr Opin Neurobiol. 2015; 35:21-6. PMC: 4641801. DOI: 10.1016/j.conb.2015.06.002. View

McHugh T, Jones M, Quinn J, Balthasar N, Coppari R, Elmquist J . Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science. 2007; 317(5834):94-9. DOI: 10.1126/science.1140263. View

Han X, Chow B, Zhou H, Klapoetke N, Chuong A, Rajimehr R . A high-light sensitivity optical neural silencer: development and application to optogenetic control of non-human primate cortex. Front Syst Neurosci. 2011; 5:18. PMC: 3082132. DOI: 10.3389/fnsys.2011.00018. View

Dayer A, Ford A, Cleaver K, Yassaee M, Cameron H . Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol. 2003; 460(4):563-72. DOI: 10.1002/cne.10675. View

Rangel L, Quinn L, Chiba A, Gage F, Aimone J . A hypothesis for temporal coding of young and mature granule cells. Front Neurosci. 2013; 7:75. PMC: 3653099. DOI: 10.3389/fnins.2013.00075. View

Han X, Qian X, Bernstein J, Zhou H, Talei Franzesi G, Stern P . Millisecond-timescale optical control of neural dynamics in the nonhuman primate brain. Neuron. 2009; 62(2):191-8. PMC: 2830644. DOI: 10.1016/j.neuron.2009.03.011. View

10.

Spalding K, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner H . Dynamics of hippocampal neurogenesis in adult humans. Cell. 2013; 153(6):1219-1227. PMC: 4394608. DOI: 10.1016/j.cell.2013.05.002. View

11.

Sahay A, Scobie K, Hill A, OCarroll C, Kheirbek M, Burghardt N . Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature. 2011; 472(7344):466-70. PMC: 3084370. DOI: 10.1038/nature09817. View

12.

Amaral D, Scharfman H, Lavenex P . The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res. 2007; 163:3-22. PMC: 2492885. DOI: 10.1016/S0079-6123(07)63001-5. View

13.

Zhao C, Teng E, Summers Jr R, Ming G, Gage F . Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci. 2006; 26(1):3-11. PMC: 6674324. DOI: 10.1523/JNEUROSCI.3648-05.2006. View

14.

Burghardt N, Park E, Hen R, Fenton A . Adult-born hippocampal neurons promote cognitive flexibility in mice. Hippocampus. 2012; 22(9):1795-808. PMC: 4784987. DOI: 10.1002/hipo.22013. View

15.

Dery N, Pilgrim M, Gibala M, Gillen J, Martin Wojtowicz J, MacQueen G . Adult hippocampal neurogenesis reduces memory interference in humans: opposing effects of aerobic exercise and depression. Front Neurosci. 2013; 7:66. PMC: 3639381. DOI: 10.3389/fnins.2013.00066. View

16.

Kheirbek M, Klemenhagen K, Sahay A, Hen R . Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat Neurosci. 2012; 15(12):1613-20. PMC: 3638121. DOI: 10.1038/nn.3262. View

17.

Kesner R, Hui X, Sommer T, Wright C, Barrera V, Fanselow M . The role of postnatal neurogenesis in supporting remote memory and spatial metric processing. Hippocampus. 2014; 24(12):1663-71. DOI: 10.1002/hipo.22346. View

18.

Rangel L, Alexander A, Aimone J, Wiles J, Gage F, Chiba A . Temporally selective contextual encoding in the dentate gyrus of the hippocampus. Nat Commun. 2014; 5:3181. PMC: 3929785. DOI: 10.1038/ncomms4181. View

19.

Christie I, Wells J, Southern P, Marina N, Kasparov S, Gourine A . fMRI response to blue light delivery in the naïve brain: implications for combined optogenetic fMRI studies. Neuroimage. 2012; 66:634-41. DOI: 10.1016/j.neuroimage.2012.10.074. View

20.

Toni N, Laplagne D, Zhao C, Lombardi G, Ribak C, Gage F . Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci. 2008; 11(8):901-7. PMC: 2572641. DOI: 10.1038/nn.2156. View