Spatial Memory Formation Requires Netrin-1 Expression by Neurons in the Adult Mammalian Brain

Overview

Journal Learn Mem

Specialty Neurology

Date 2019 Feb 17

PMID 30770464

Citations 13

Authors

Edwin W Wong

Stephen D Glasgow

Lianne J Trigiani

Daryan Chitsaz

Vladimir Rymar

Abbas Sadikot

Edward S Ruthazer

Edith Hamel

Timothy E Kennedy

Affiliations

Soon will be listed here.

Abstract

Netrin-1 was initially characterized as an axon guidance molecule that is essential for normal embryonic neural development; however, many types of neurons continue to express netrin-1 in the postnatal and adult mammalian brain. Netrin-1 and the netrin receptor DCC are both enriched at synapses. In the adult hippocampus, activity-dependent secretion of netrin-1 by neurons potentiates glutamatergic synapse function, and is critical for long-term potentiation, an experimental cellular model of learning and memory. Here, we assessed the impact of neuronal expression of netrin-1 in the adult brain on behavior using tests of learning and memory. We show that adult mice exhibit impaired spatial memory following conditional deletion of netrin-1 from glutamatergic neurons in the hippocampus and neocortex. Further, we provide evidence that mice with conditional deletion of netrin-1 do not display aberrant anxiety-like phenotypes and show a reduction in self-grooming behavior. These findings reveal a critical role for netrin-1 expressed by neurons in the regulation of spatial memory formation.

Citing Articles

Netrin-1 signaling pathway mechanisms in neurodegenerative diseases.

Zhu K, Wang H, Ye K, Chen G, Zhang Z Neural Regen Res. 2024; 20(4):960-972.

PMID: 38989931 PMC: 11438344. DOI: 10.4103/NRR.NRR-D-23-01573.

The E3 ubiquitin ligase TRIM9 regulates synaptic function and actin dynamics in response to netrin-1.

McCormick L, Evans E, Barker N, Herring L, Diering G, Gupton S Mol Biol Cell. 2024; 35(5):ar67.

PMID: 38507236 PMC: 11151106. DOI: 10.1091/mbc.E23-12-0476.

The E3 ubiquitin ligase TRIM9 regulates synaptic function and actin dynamics.

McCormick L, Evans E, Barker N, Herring L, Diering G, Gupton S bioRxiv. 2024; .

PMID: 38260647 PMC: 10802335. DOI: 10.1101/2023.12.31.573790.

Regulation of AMPA receptor trafficking by secreted protein factors.

Rennich B, Luth E, Moores S, Juo P Front Cell Neurosci. 2023; 17:1271169.

PMID: 38089145 PMC: 10711074. DOI: 10.3389/fncel.2023.1271169.

Shared genetic architecture of COVID-19 and Alzheimer's disease.

Matveeva N, Kiselev I, Baulina N, Semina E, Kakotkin V, Agapov M Front Aging Neurosci. 2023; 15:1287322.

PMID: 37927339 PMC: 10625425. DOI: 10.3389/fnagi.2023.1287322.

References

Brun V, Ytterbo K, Morris R, Moser M, Moser E . Retrograde amnesia for spatial memory induced by NMDA receptor-mediated long-term potentiation. J Neurosci. 2001; 21(1):356-62. PMC: 6762446. View

Louie K, Wilson M . Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron. 2001; 29(1):145-56. DOI: 10.1016/s0896-6273(01)00186-6. View

DHooge R, De Deyn P . Applications of the Morris water maze in the study of learning and memory. Brain Res Brain Res Rev. 2001; 36(1):60-90. DOI: 10.1016/s0165-0173(01)00067-4. View

Vinogradova O . Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus. 2001; 11(5):578-98. DOI: 10.1002/hipo.1073. View

Buzsaki G . Theta oscillations in the hippocampus. Neuron. 2002; 33(3):325-40. DOI: 10.1016/s0896-6273(02)00586-x. View

Nakazawa K, McHugh T, Wilson M, Tonegawa S . NMDA receptors, place cells and hippocampal spatial memory. Nat Rev Neurosci. 2004; 5(5):361-72. DOI: 10.1038/nrn1385. View

Flores C, Manitt C, Rodaros D, Thompson K, Rajabi H, Luk K . Netrin receptor deficient mice exhibit functional reorganization of dopaminergic systems and do not sensitize to amphetamine. Mol Psychiatry. 2004; 10(6):606-12. DOI: 10.1038/sj.mp.4001607. View

Clark R, Martin S . Interrogating rodents regarding their object and spatial memory. Curr Opin Neurobiol. 2005; 15(5):593-8. DOI: 10.1016/j.conb.2005.08.014. View

Brody D, Holtzman D . Morris water maze search strategy analysis in PDAPP mice before and after experimental traumatic brain injury. Exp Neurol. 2005; 197(2):330-40. PMC: 1913184. DOI: 10.1016/j.expneurol.2005.10.020. View

10.

ONeill J, Senior T, Csicsvari J . Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron. 2006; 49(1):143-55. DOI: 10.1016/j.neuron.2005.10.037. View

11.

Deacon R, Rawlins J . T-maze alternation in the rodent. Nat Protoc. 2007; 1(1):7-12. DOI: 10.1038/nprot.2006.2. View

12.

McFarlane H, Kusek G, Yang M, Phoenix J, Bolivar V, Crawley J . Autism-like behavioral phenotypes in BTBR T+tf/J mice. Genes Brain Behav. 2007; 7(2):152-63. DOI: 10.1111/j.1601-183X.2007.00330.x. View

13.

Vago D, Kesner R . Disruption of the direct perforant path input to the CA1 subregion of the dorsal hippocampus interferes with spatial working memory and novelty detection. Behav Brain Res. 2008; 189(2):273-83. PMC: 2421012. DOI: 10.1016/j.bbr.2008.01.002. View

14.

Montgomery S, Sirota A, Buzsaki G . Theta and gamma coordination of hippocampal networks during waking and rapid eye movement sleep. J Neurosci. 2008; 28(26):6731-41. PMC: 2596978. DOI: 10.1523/JNEUROSCI.1227-08.2008. View

15.

Harrison F, Hosseini A, McDonald M . Endogenous anxiety and stress responses in water maze and Barnes maze spatial memory tasks. Behav Brain Res. 2008; 198(1):247-51. PMC: 2663577. DOI: 10.1016/j.bbr.2008.10.015. View

16.

Kumaran D, Maguire E . Novelty signals: a window into hippocampal information processing. Trends Cogn Sci. 2009; 13(2):47-54. DOI: 10.1016/j.tics.2008.11.004. View

17.

Isaac J, Buchanan K, Muller R, Mellor J . Hippocampal place cell firing patterns can induce long-term synaptic plasticity in vitro. J Neurosci. 2009; 29(21):6840-50. PMC: 2692101. DOI: 10.1523/JNEUROSCI.0731-09.2009. View

18.

Silverman J, Tolu S, Barkan C, Crawley J . Repetitive self-grooming behavior in the BTBR mouse model of autism is blocked by the mGluR5 antagonist MPEP. Neuropsychopharmacology. 2009; 35(4):976-89. PMC: 2827881. DOI: 10.1038/npp.2009.201. View

19.

Roberts T, Tschida K, Klein M, Mooney R . Rapid spine stabilization and synaptic enhancement at the onset of behavioural learning. Nature. 2010; 463(7283):948-52. PMC: 2918377. DOI: 10.1038/nature08759. View

20.

Shen K, Cowan C . Guidance molecules in synapse formation and plasticity. Cold Spring Harb Perspect Biol. 2010; 2(4):a001842. PMC: 2845208. DOI: 10.1101/cshperspect.a001842. View