Age-related Enhancement of a Protein Synthesis-dependent Late Phase of LTP Induced by Low Frequency Paired-pulse Stimulation in Hippocampus

Overview

Journal Learn Mem

Specialty Neurology

Date 2006 Jun 3

PMID 16741282

Citations 19

Authors

Yan-You Huang

Eric R Kandel

Affiliations

Soon will be listed here.

Abstract

Protein synthesis-dependent late phase of LTP (L-LTP) is typically induced by repeated high-frequency stimulation (HFS). This form of L-LTP is reduced in the aged animal and is positively correlated with age-related memory loss. Here we report a novel form of protein synthesis-dependent late phase of LTP in the CA1 region of hippocampus induced by a brief 1-Hz paired-pulse stimulation (PP-1 Hz, 1 min). In contrast to L-LTP induced by HFS, the late phase of PP-1 Hz LTP does not exist in young adult animals. Rather, it emerges and becomes enhanced in an age-related way. Thus, in 1.5- to 2-mo-old mice, a brief PP-1 Hz stimulation induces only a short lasting LTP, decaying to baseline in about 90 min. By contrast, PP-1 Hz stimulation induces an enduring and protein synthesis dependent LTP in 12- to 18-mo-old mice. The PP-1 Hz-induced L-LTP is dependent on NMDA receptor activation, requires voltage-dependent calcium channels, and is modulated by dopamine D1/D5 receptors. Because memory ability declines with aging, the age-related enhancement of L-LTP induced by PP-1 Hz stimulation indicates that this form of L-LTP appears to be inversely correlated with memory ability.

Citing Articles

Entorhinal cortex-hippocampal circuit connectivity in health and disease.

Hernandez-Frausto M, Vivar C Front Hum Neurosci. 2024; 18:1448791.

PMID: 39372192 PMC: 11449717. DOI: 10.3389/fnhum.2024.1448791.

Neural ageing and synaptic plasticity: prioritizing brain health in healthy longevity.

Navakkode S, Kennedy B Front Aging Neurosci. 2024; 16:1428244.

PMID: 39161341 PMC: 11330810. DOI: 10.3389/fnagi.2024.1428244.

Rho-associated kinases contribute to the regulation of tau phosphorylation and amyloid metabolism during neuronal plasticity.

Saray H, Suer C, Kosar B, Tan B, Dursun N Pharmacol Rep. 2021; 73(5):1303-1314.

PMID: 34060063 DOI: 10.1007/s43440-021-00279-3.

Novel Players in the Aging Synapse: Impact on Cognition.

Temido-Ferreira M, Coelho J, Pousinha P, Lopes L J Caffeine Adenosine Res. 2019; 9(3):104-127.

PMID: 31559391 PMC: 6761599. DOI: 10.1089/caff.2019.0013.

Astrocyte HIF-2α supports learning in a passive avoidance paradigm under hypoxic stress.

Leiton C, Chen E, Cutrone A, Conn K, Mellanson K, Malik D Hypoxia (Auckl). 2018; 6:35-56.

PMID: 30519596 PMC: 6234990. DOI: 10.2147/HP.S173589.

References

Alarcon J, Hodgman R, Theis M, Huang Y, Kandel E, Richter J . Selective modulation of some forms of schaffer collateral-CA1 synaptic plasticity in mice with a disruption of the CPEB-1 gene. Learn Mem. 2004; 11(3):318-27. PMC: 419735. DOI: 10.1101/lm.72704. View

Nguyen P, Kandel E . Brief theta-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus. Learn Mem. 1997; 4(2):230-43. DOI: 10.1101/lm.4.2.230. View

Shouval H, Bear M, Cooper L . A unified model of NMDA receptor-dependent bidirectional synaptic plasticity. Proc Natl Acad Sci U S A. 2002; 99(16):10831-6. PMC: 125058. DOI: 10.1073/pnas.152343099. View

Woodruff-Pak D, Chi J, Li Y, Pak M, Fanelli R . Nimodipine ameliorates impaired eyeblink classical conditioning in older rabbits in the long-delay paradigm. Neurobiol Aging. 1998; 18(6):641-9. DOI: 10.1016/s0197-4580(97)00159-0. View

Huang Y, Pittenger C, Kandel E . A form of long-lasting, learning-related synaptic plasticity in the hippocampus induced by heterosynaptic low-frequency pairing. Proc Natl Acad Sci U S A. 2004; 101(3):859-64. PMC: 321771. DOI: 10.1073/pnas.2237201100. View

Campbell L, Hao S, Thibault O, Blalock E, Landfield P . Aging changes in voltage-gated calcium currents in hippocampal CA1 neurons. J Neurosci. 1996; 16(19):6286-95. PMC: 6579167. View

Wood M, Kaplan M, Park A, Blanchard E, Oliveira A, Lombardi T . Transgenic mice expressing a truncated form of CREB-binding protein (CBP) exhibit deficits in hippocampal synaptic plasticity and memory storage. Learn Mem. 2005; 12(2):111-9. PMC: 1074328. DOI: 10.1101/lm.86605. View

Hsu K, Huang C, Liang Y, Wu H, Chen Y, Lo S . Alterations in the balance of protein kinase and phosphatase activities and age-related impairments of synaptic transmission and long-term potentiation. Hippocampus. 2003; 12(6):787-802. DOI: 10.1002/hipo.10032. View

Kingston A, Ornstein P, Wright R, Johnson B, Mayne N, Burnett J . LY341495 is a nanomolar potent and selective antagonist of group II metabotropic glutamate receptors. Neuropharmacology. 1998; 37(1):1-12. DOI: 10.1016/s0028-3908(97)00191-3. View

10.

Huber K, Gallagher S, Warren S, Bear M . Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc Natl Acad Sci U S A. 2002; 99(11):7746-50. PMC: 124340. DOI: 10.1073/pnas.122205699. View

11.

Malenka R, Bear M . LTP and LTD: an embarrassment of riches. Neuron. 2004; 44(1):5-21. DOI: 10.1016/j.neuron.2004.09.012. View

12.

Pittenger C, Huang Y, Paletzki R, Bourtchouladze R, Scanlin H, Vronskaya S . Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory. Neuron. 2002; 34(3):447-62. DOI: 10.1016/s0896-6273(02)00684-0. View

13.

Matthies H, Becker A, Schroeder H, Kraus J, Hollt V, Krug M . Dopamine D1-deficient mutant mice do not express the late phase of hippocampal long-term potentiation. Neuroreport. 1998; 8(16):3533-5. DOI: 10.1097/00001756-199711100-00023. View

14.

Zakharenko S, Zablow L, Siegelbaum S . Altered presynaptic vesicle release and cycling during mGluR-dependent LTD. Neuron. 2002; 35(6):1099-110. DOI: 10.1016/s0896-6273(02)00898-x. View

15.

Kang H, Sun L, Atkins C, Soderling T, Wilson M, Tonegawa S . An important role of neural activity-dependent CaMKIV signaling in the consolidation of long-term memory. Cell. 2001; 106(6):771-83. DOI: 10.1016/s0092-8674(01)00497-4. View

16.

Bach M, Barad M, Son H, Zhuo M, Lu Y, Shih R . Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway. Proc Natl Acad Sci U S A. 1999; 96(9):5280-5. PMC: 21855. DOI: 10.1073/pnas.96.9.5280. View

17.

Thomas M, Watabe A, Moody T, Makhinson M, ODell T . Postsynaptic complex spike bursting enables the induction of LTP by theta frequency synaptic stimulation. J Neurosci. 1998; 18(18):7118-26. PMC: 6793261. View

18.

Wu J, Rowan M, Anwyl R . An NMDAR-independent LTP mediated by group II metabotropic glutamate receptors and p42/44 MAP kinase in the dentate gyrus in vitro. Neuropharmacology. 2004; 46(3):311-7. DOI: 10.1016/j.neuropharm.2003.09.014. View

19.

Castellani G, Quinlan E, Bersani F, Cooper L, Shouval H . A model of bidirectional synaptic plasticity: from signaling network to channel conductance. Learn Mem. 2005; 12(4):423-32. PMC: 1183261. DOI: 10.1101/lm.80705. View

20.

Luine V, Bowling D, Hearns M . Spatial memory deficits in aged rats: contributions of monoaminergic systems. Brain Res. 1990; 537(1-2):271-8. DOI: 10.1016/0006-8993(90)90368-l. View