NGF is Essential for Hippocampal Plasticity and Learning

Overview

Journal J Neurosci

Specialty Neurology

Date 2009 Sep 4

PMID 19726646

Citations 80

Authors

James M Conner

Kevin M Franks

Andrea K Titterness

Kyle Russell

David A Merrill

Brian R Christie

Terrence J Sejnowski

Mark H Tuszynski

Affiliations

Soon will be listed here.

Abstract

Nerve growth factor (NGF) is produced in the hippocampus throughout life and is retrogradely trafficked to septal cholinergic neurons, providing a potential mechanism for modulating cholinergic inputs and, thereby, hippocampal plasticity. To explore NGF modulation of hippocampal plasticity and function, NGF levels were augmented or blocked in intact adult rats, and subsequent in vivo effects on cholinergic neurons, hippocampal long-term potentiation (LTP), and learning were examined. NGF augmentation significantly enhanced cholinergic neuronal markers and facilitated induction of hippocampal LTP. Blockade of endogenous NGF significantly reduced hippocampal LTP and impaired retention of spatial memory. These findings reveal an essential role for NGF in regulating biological mechanisms related to plasticity and memory in the intact adult brain.

Citing Articles

The Neurotrophin System in the Postnatal Brain-An Introduction.

von Bohlen Und Halbach O, Klausch M Biology (Basel). 2024; 13(8).

PMID: 39194496 PMC: 11352095. DOI: 10.3390/biology13080558.

Combination Therapy with Platelet-Rich Plasma and Epidermal Neural Crest Stem Cells Increases Treatment Efficacy in Vascular Dementia.

Akbari S, Haghani M, Ghobadi M, Hooshmandi E, Haghighi A, Salehi M Stem Cells Int. 2023; 2023:3784843.

PMID: 38146481 PMC: 10749736. DOI: 10.1155/2023/3784843.

Neurotrophic and Neuroprotective Effects of .

Szucko-Kociuba I, Trzeciak-Ryczek A, Kupnicka P, Chlubek D Int J Mol Sci. 2023; 24(21).

PMID: 37958943 PMC: 10650066. DOI: 10.3390/ijms242115960.

Neural plasticity and depression treatment.

Wang Y, Song N, Ding Y, Zhang L IBRO Neurosci Rep. 2023; 14:160-184.

PMID: 37388497 PMC: 10300479. DOI: 10.1016/j.ibneur.2022.09.001.

A Three-Fold Integrated Perspective on Healthy Development: An Opinion Paper.

Paoletti P, Pellegrino M, Ben-Soussan T Brain Sci. 2023; 13(6).

PMID: 37371337 PMC: 10296304. DOI: 10.3390/brainsci13060857.

References

Book A, Wiley R, Schweitzer J . 192 IgG-saporin: I. Specific lethality for cholinergic neurons in the basal forebrain of the rat. J Neuropathol Exp Neurol. 1994; 53(1):95-102. DOI: 10.1097/00005072-199401000-00012. View

Morris R . Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods. 1984; 11(1):47-60. DOI: 10.1016/0165-0270(84)90007-4. View

Koliatsos V, Nauta H, Clatterbuck R, Holtzman D, Mobley W, Price D . Mouse nerve growth factor prevents degeneration of axotomized basal forebrain cholinergic neurons in the monkey. J Neurosci. 1990; 10(12):3801-13. PMC: 6570054. View

Berse B, Lopez-Coviella I, Blusztajn J . Activation of TrkA by nerve growth factor upregulates expression of the cholinergic gene locus but attenuates the response to ciliary neurotrophic growth factor. Biochem J. 1999; 342 ( Pt 2):301-8. PMC: 1220465. View

Huang E, Reichardt L . Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem. 2003; 72:609-42. DOI: 10.1146/annurev.biochem.72.121801.161629. View

Scali C, Casamenti F, Pazzagli M, Bartolini L, Pepeu G . Nerve growth factor increases extracellular acetylcholine levels in the parietal cortex and hippocampus of aged rats and restores object recognition. Neurosci Lett. 1994; 170(1):117-20. DOI: 10.1016/0304-3940(94)90253-4. View

Huerta P, Lisman J . Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature. 1993; 364(6439):723-5. DOI: 10.1038/364723a0. View

Gage F, Batchelor P, Chen K, Chin D, Higgins G, Koh S . NGF receptor reexpression and NGF-mediated cholinergic neuronal hypertrophy in the damaged adult neostriatum. Neuron. 1989; 2(2):1177-84. DOI: 10.1016/0896-6273(89)90184-0. View

Large T, Bodary S, Clegg D, Weskamp G, Otten U, Reichardt L . Nerve growth factor gene expression in the developing rat brain. Science. 1986; 234(4774):352-5. DOI: 10.1126/science.3764415. View

10.

Fonnum F . A rapid radiochemical method for the determination of choline acetyltransferase. J Neurochem. 1975; 24(2):407-9. DOI: 10.1111/j.1471-4159.1975.tb11895.x. View

11.

Brooks A, Cory-Slechta D, Federoff H . Gene-experience interaction alters the cholinergic septohippocampal pathway of mice. Proc Natl Acad Sci U S A. 2000; 97(24):13378-83. PMC: 27232. DOI: 10.1073/pnas.230169397. View

12.

Hirotsu I, Hori N, Katsuda N, Ishihara T . Effect of anticholinergic drug on long-term potentiation in rat hippocampal slices. Brain Res. 1989; 482(1):194-7. DOI: 10.1016/0006-8993(89)90561-1. View

13.

Squire L, Alvarez P . Retrograde amnesia and memory consolidation: a neurobiological perspective. Curr Opin Neurobiol. 1995; 5(2):169-77. DOI: 10.1016/0959-4388(95)80023-9. View

14.

Bergado J, Fernandez C, Gonzalez O . Chronic intraventricular infusion with NGF improves LTP in old cognitively-impaired rats. Brain Res. 1998; 770(1-2):1-9. DOI: 10.1016/s0006-8993(97)00610-0. View

15.

Lynch G, Rex C, Chen L, Gall C . The substrates of memory: defects, treatments, and enhancement. Eur J Pharmacol. 2008; 585(1):2-13. PMC: 2427007. DOI: 10.1016/j.ejphar.2007.11.082. View

16.

Kelly A, Conroy S, Lynch M . Evidence that nerve growth factor plays a role in long-term potentiation in the rat dentate gyrus. Neuropharmacology. 1998; 37(4-5):561-70. DOI: 10.1016/s0028-3908(98)00048-3. View

17.

Van der Zee C, Lourenssen S, Stanisz J, Diamond J . NGF deprivation of adult rat brain results in cholinergic hypofunction and selective impairments in spatial learning. Eur J Neurosci. 1995; 7(1):160-8. DOI: 10.1111/j.1460-9568.1995.tb01030.x. View

18.

Tuszynski M, Gage F . Bridging grafts and transient nerve growth factor infusions promote long-term central nervous system neuronal rescue and partial functional recovery. Proc Natl Acad Sci U S A. 1995; 92(10):4621-5. PMC: 41996. DOI: 10.1073/pnas.92.10.4621. View

19.

Fischer W, Wictorin K, Bjorklund A, Williams L, Varon S, Gage F . Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature. 1987; 329(6134):65-8. DOI: 10.1038/329065a0. View

20.

Wiley R, Oeltmann T, Lappi D . Immunolesioning: selective destruction of neurons using immunotoxin to rat NGF receptor. Brain Res. 1991; 562(1):149-53. DOI: 10.1016/0006-8993(91)91199-b. View