Skip to main content

Advertisement

SpringerLink
Log in

Accumulated hippocampal formaldehyde induces age-dependent memory decline

  • Published:
AGE Aims and scope Submit manuscript

Abstract

Aging is an important factor in memory decline in aged animals and humans and in Alzheimer’s disease and is associated with the impairment of hippocampal long-term potentiation (LTP) and down-regulation of NR1/NR2B expression. Gaseous formaldehyde exposure is known to induce animal memory loss and human cognitive decline; however, it is unclear whether the concentrations of endogenous formaldehyde are elevated in the hippocampus and how excess formaldehyde affects LTP and memory formation during the aging process. In the present study, we report that hippocampal formaldehyde accumulated in memory-deteriorating diseases such as age-related dementia. Spatial memory performance was gradually impaired in normal Sprague–Dawley rats by persistent intraperitoneal injection with formaldehyde. Furthermore, excess formaldehyde treatment suppressed the hippocampal LTP formation by blocking N-methyl-d-aspartate (NMDA) receptor. Chronic excess formaldehyde treatment over a period of 30 days markedly decreased the viability of the hippocampus and down-regulated the expression of the NR1 and NR2B subunits of the NMDA receptor. Our results indicate that excess endogenous formaldehyde is a critical factor in memory loss in age-related memory-deteriorating diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abu-Abeeleh M, Bani Ismail ZA, Alzaben KR, Abu-Halaweh SA, Aloweidi AS, Al-Ammouri IA, Al-Essa MK, Jabaiti SK, Abu-Abeeleh J, Alsmady MM (2010) A preliminary study of the use of human adipose tissue-derived stem cells for the treatment of streptozotocin-induced diabetes mellitus in a rat model. Comp Clin Pathol 19(1):1–4

    Article  Google Scholar 

  • Almaguer W, Estupiņán B, Uwe Frey J, Bergado JA (2002) Aging impairs amygdala–hippocampus interactions involved in hippocampal LTP. Neurobiology of aging 23(2):319–324

    Article  PubMed  Google Scholar 

  • Amada N, Aihara K, Ravid R, Horie M (2005) Reduction of NR1 and phosphorylated Ca2+/calmodulin-dependent protein kinase II levels in Alzheimer's disease. Neuroreport 16(16):1809

    Article  CAS  PubMed  Google Scholar 

  • Asaka Y, Jugloff DGM, Zhang L, Eubanks JH, Fitzsimonds RM (2006) Hippocampal synaptic plasticity is impaired in the Mecp2-null mouse model of Rett syndrome. Neurobiol Dis 21(1):217–227

    Article  CAS  PubMed  Google Scholar 

  • Blevins T, Mirshahi T, Chandler LJ, Woodward JJ (1997) Effects of acute and chronic ethanol exposure on heteromeric N-methyl-d-aspartate receptors expressed in HEK 293 cells. J Neurochem 69(6):2345–2354

    Article  CAS  PubMed  Google Scholar 

  • Brioni JD, McGaugh JL, Izquierdo I (1989) Amnesia induced by short-term treatment with ethanol: attenuation by pretest oxotremorine. Pharmacol Biochem Behav 33(1):27–29

    Article  CAS  PubMed  Google Scholar 

  • Burke WJ, McLaughlin JR, Chung HD, Gillespie KN, Grossberg GT, Luque FA, Zimmerman J (1994) Occurrence of cancer in Alzheimer and elderly control patients: an epidemiologic necropsy study. Alzheimer Disease & Associated Disorders 8(1):22

    Article  CAS  Google Scholar 

  • Chapman PF, White GL, Jones MW, Cooper-Blacketer D, Marshall VJ, Irizarry M, Younkin L, Good MA, Bliss T, Hyman BT (1999) Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 2(3):271–276

    Article  CAS  PubMed  Google Scholar 

  • Chen K, Maley J, Yu PH (2006) Potential implications of endogenous aldehydes in β-amyloid misfolding, oligomerization and fibrillogenesis. J Neurochem 99(5):1413–1424

    Article  CAS  PubMed  Google Scholar 

  • Chen KL, Wang SSS, Yang YY, Yuan RY, Chen RM, Hu CJ (2009) The epigenetic effects of amyloid-[beta] 1–40 on global DNA and neprilysin genes in murine cerebral endothelial cells. Biochem Biophys Res Commun 378(1):57–61

    Article  CAS  PubMed  Google Scholar 

  • Cheng L, Yin WJ, Zhang JF, Qi JS (2009) Amyloid beta-protein fragments 25–35 and 31–35 potentiate long-term depression in hippocampal CA1 region of rats in vivo. Synapse 63(3):206–214

    Article  CAS  PubMed  Google Scholar 

  • Clayton DA, Mesches MH, Alvarez E, Bickford PC, Browning MD (2002) A hippocampal NR2B deficit can mimic age-related changes in long-term potentiation and spatial learning in the Fischer 344 rat. J Neurosci 22(9):3628–3637

    CAS  PubMed  Google Scholar 

  • Connelly CA, Chen LC, Colquhoun SD (2000) Metabolic activity of cultured rat brainstem, hippocampal and spinal cord slices. Journal of neuroscience methods 99(1–2):1–7

    Article  CAS  PubMed  Google Scholar 

  • Coppedè F (2010) One-carbon metabolism and Alzheimer's disease: focus on epigenetics. Current genomics 11(4):246–260

    Article  PubMed Central  PubMed  Google Scholar 

  • Cui X (1996) Inhaled formaldehyde on the effects of GSH level and distribution of formaldehyde. China J PrevMed 3:186

    Google Scholar 

  • Cummings JL (2008) The black book of Alzheimer's disease, part 1. Primary Psychiatry 15(2):66–76

    Google Scholar 

  • Denk H, Moldeus PW, Schulz RA, Schenkman JB, Keyes SR, Cinti DL (1976) Hepatic organelle interaction. IV. Mechanism of succinate enhancement of formaldehyde accumulation from endoplasmic reticulum N-dealkylations. The Journal of cell biology 69(3):589–598

    Article  CAS  PubMed  Google Scholar 

  • Dewachter I, Filipkowski R, Priller C, Ris L, Neyton J, Croes S, Terwel D, Gysemans M, Devijver H, Borghgraef P (2009) Deregulation of NMDA-receptor function and down-stream signaling in APP [V717I] transgenic mice. Neurobiology of aging 30(2):241–256

    Article  CAS  PubMed  Google Scholar 

  • Dildy JE, Leslie SW (1989) Ethanol inhibits NMDA-induced increases in free intracellular Ca2+ in dissociated brain cells. Brain research 499(2):383–387

    Article  CAS  PubMed  Google Scholar 

  • Drachman DA (2006) Aging of the brain, entropy, and Alzheimer disease. Neurology 67(8):1340–1352

    Article  CAS  PubMed  Google Scholar 

  • Ely J (2001) Mercury induced Alzheimer's disease: accelerating incidence? Bull Environ Contam Toxicol 67(6):800–806

    Article  CAS  PubMed  Google Scholar 

  • Gaunitz C, Schüttler A, Gillen C, Allgaier C (2002) Formalin-induced changes of NMDA receptor subunit expression in the spinal cord of the rat. Amino Acids 23(1):177–182

    Article  CAS  PubMed  Google Scholar 

  • Gengler S, Hamilton A, Hölscher C (2010) Synaptic plasticity in the hippocampus of a APP/PS1 mouse model of Alzheimer's disease is impaired in old but not young mice. PLoS One 5(3):e9764

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Grönvall JLE, Garpenstrand H, Oreland L, Ekblom J (1998) Autoradiographic imaging of formaldehyde adducts in mice: possible relevance for vascular damage in diabetes. Life Sci 63(9):759–768

    Article  PubMed  Google Scholar 

  • Gurel A, Coskun O, Armutcu F, Kanter M, Ozen OA (2005) Vitamin E against oxidative damage caused by formaldehyde in frontal cortex and hippocampus: biochemical and histological studies. J Chem Neuroanat 29(3):173–178

    Article  CAS  PubMed  Google Scholar 

  • Gureviciene I, Ikonen S, Gurevicius K, Sarkaki A, Van Groen T, Pussinen R, Ylinen A, Tanila H (2004) Normal induction but accelerated decay of LTP in APP + PS1 transgenic mice. Neurobiol Dis 15(2):188–195

    Article  CAS  PubMed  Google Scholar 

  • He R, Lu J, Miao J (2010) Formaldehyde stress. Science China Life Sciences 53(12):1399–1404

    Article  CAS  PubMed  Google Scholar 

  • Heck HDA, White EL, Casanova-Schmitz M (1982) Determination of formaldehyde in biological tissues by gas chromatography/mass spectrometry. Biological Mass Spectrometry 9(8):347–353

    Article  CAS  Google Scholar 

  • Henniger MSH, Wotjak CT, Hölter SM (2003) Long-term voluntary ethanol drinking increases expression of NMDA receptor 2B subunits in rat frontal cortex. Eur J Pharmacol 470(1–2):33–36

    Article  CAS  PubMed  Google Scholar 

  • Herin GA, Du S, Aizenman E (2001) The neuroprotective agent ebselen modifies NMDA receptor function via the redox modulatory site. J Neurochem 78(6):1307–1314

    Article  CAS  PubMed  Google Scholar 

  • Hynd MR, Scott HL, Dodd PR (2004) Differential expression of N-methyl-d-aspartate receptor NR2 isoforms in Alzheimer's disease. J Neurochem 90(4):913–919

    Article  CAS  PubMed  Google Scholar 

  • Kalapos MP (1999) A possible evolutionary role of formaldehyde. Experimental & molecular medicine 31(1):1–4

    Article  CAS  Google Scholar 

  • Kalász H (2003) Biological role of formaldehyde, and cycles related to methylation, demethylation, and formaldehyde production. Mini reviews in medicinal chemistry 3(3):175–192

    Article  PubMed  Google Scholar 

  • Kalluri HSG, Mehta AK, Ticku MK (1998) Up-regulation of NMDA receptor subunits in rat brain following chronic ethanol treatment. Molecular brain research 58(1–2):221–224

    Article  CAS  PubMed  Google Scholar 

  • Kamal A, Biessels GJ, Ramakers GMJ, Hendrik Gispen W (2005) The effect of short duration streptozotocin-induced diabetes mellitus on the late phase and threshold of long-term potentiation induction in the rat. Brain research 1053(1–2):126–130

    Article  CAS  PubMed  Google Scholar 

  • Karuppagounder SS, Pinto JT, Xu H, Chen HL, Beal MF, Gibson GE (2009) Dietary supplementation with resveratrol reduces plaque pathology in a transgenic model of Alzheimer's disease. Neurochem Int 54(2):111–118

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kilburn KH (1994) Neurobehavioral impairment and seizures from formaldehyde. Archives of Environmental Health: An International Journal 49(1):37–44

    Article  CAS  Google Scholar 

  • Kilburn KH, Warshaw R, Thornton JC (1987) Formaldehyde impairs memory, equilibrium, and dexterity in histology technicians: effects which persist for days after exposure. Archives of Environmental Health: An International Journal 42(2):117–120

    Article  CAS  Google Scholar 

  • Kollau A, Hofer A, Russwurm M, Koesling D, Keung WM, Schmidt K, Brunner F, Mayer B (2005) Contribution of aldehyde dehydrogenase to mitochondrial bioactivation of nitroglycerin: evidence for the activation of purified soluble guanylate cyclase through direct formation of nitric oxide. Biochem J 385(Pt 3):769

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lee S, Kim W, Ham BJ, Chen W, Bear MF, Yoon BJ (2008) Activity-dependent NR2B expression is mediated by MeCP2-dependent epigenetic regulation. Biochem Biophys Res Commun 377(3):930–934

    Article  CAS  PubMed  Google Scholar 

  • Liu L, van Groen T, Kadish I, Tollefsbol TO (2009) DNA methylation impacts on learning and memory in aging. Neurobiology of aging 30(4):549–560

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu Q, Yang L, Gong C, Tao G, Huang H, Liu J, Zhang H, Wu D, Xia B, Hu G (2011) Effects of long-term low-dose formaldehyde exposure on global genomic hypomethylation in 16HBE cells. Toxicol Lett 205(3):235–240

    Article  CAS  PubMed  Google Scholar 

  • López-Ramos JC, Jurado-Parras MT, Sanfeliu C, Acuña-Castroviejo D, Delgado-García JM (2012) Learning capabilities and CA1-prefrontal synaptic plasticity in a mice model of accelerated senescence. Neurobiology of aging 33(3):627, e13–26

    Article  PubMed  Google Scholar 

  • Lu J, Miao J, Pan R, He R (2011) Formaldehyde-mediated hyperphosphorylation disturbs the interaction between Tau protein and DNA. Progress in Biochemistry and Biophysics 38(12):1113–1120

    Article  CAS  Google Scholar 

  • Luo W, Li H, Zhang Y, Ang CYW (2001) Determination of formaldehyde in blood plasma by high-performance liquid chromatography with fluorescence detection. J Chromatogr B: Biomed Sci Appl 753(2):253–257

    Article  CAS  Google Scholar 

  • Malek FA, Möritz KU, Fanghänel J (2003) A study on the effect of inhalative formaldehyde exposure on water labyrinth test performance in rats. Annals of Anatomy-Anatomischer Anzeiger 185(3):277–285

    Article  CAS  Google Scholar 

  • McGahon BM, Martin DSD, Horrobin DF, Lynch MA (1999) Age-related changes in LTP and antioxidant defenses are reversed by an [alpha]-lipoic acid-enriched diet. Neurobiology of aging 20(6):655–664

    Article  CAS  PubMed  Google Scholar 

  • McKenna JE, Melzack R (2001) Blocking NMDA receptors in the hippocampal dentate gyrus with AP5 produces analgesia in the formalin pain test. Exp Neurol 172(1):92–99

    Article  CAS  PubMed  Google Scholar 

  • Mesches MH, Gemma C, Veng LM, Allgeier C, Young DA, Browning MD, Bickford PC (2004) Sulindac improves memory and increases NMDA receptor subunits in aged Fischer 344 rats. Neurobiology of aging 25(3):315–324

    Article  CAS  PubMed  Google Scholar 

  • Metz B, Kersten GFA, Baart GJE, de Jong A, Meiring H, ten Hove J, van Steenbergen MJ, Hennink WE, Crommelin DJA, Jiskoot W (2006) Identification of formaldehyde-induced modifications in proteins: reactions with insulin. Bioconjugate chemistry 17(3):815–822

    Article  CAS  PubMed  Google Scholar 

  • Mori O, Haseba T, Kameyama K, Shimizu H, Kudoh M, Ohaki Y, Arai Y, Yamazaki M, Asano G (2000) Histological distribution of class III alcohol dehydrogenase in human brain. Brain research 852(1):186–190

    Article  CAS  PubMed  Google Scholar 

  • Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. Journal of neuroscience methods 11(1):47–60

    Article  CAS  PubMed  Google Scholar 

  • Nakazawa K, McHugh TJ, Wilson MA, Tonegawa S (2004) NMDA receptors, place cells and hippocampal spatial memory. Nat Rev Neurosci 5(5):361–372

    Article  CAS  PubMed  Google Scholar 

  • Nie C, Wang X, Liu Y, Perrett S, He R (2007a) Amyloid-like aggregates of neuronal tau induced by formaldehyde promote apoptosis of neuronal cells. BMC Neurosci 8(1):9

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nie C, Wei Y, Chen X, Liu Y, Dui W, Liu Y, Davies MC, Tendler SJB, He R (2007b) Formaldehyde at low concentration induces protein tau into globular amyloid-like aggregates in vitro and in vivo. PLoS One 2(7):e629

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ohsawa I, Nishimaki K, Murakami Y, Suzuki Y, Ishikawa M, Ohta S (2008) Age-dependent neurodegeneration accompanying memory loss in transgenic mice defective in mitochondrial aldehyde dehydrogenase 2 activity. J Neurosci 28(24):6239–6249

    Article  CAS  PubMed  Google Scholar 

  • Patra SK, Patra A, Rizzi F, Ghosh TC, Bettuzzi S (2008) Demethylation of (Cytosine-5-C-methyl) DNA and regulation of transcription in the epigenetic pathways of cancer development. Cancer Metastasis Rev 27(2):315–334

    Article  CAS  PubMed  Google Scholar 

  • Perna RB, Bordini EJ, Deinzer-Lifrak M (2001) A case of claimed persistent neuropsychological sequelae of chronic formaldehyde exposure: clinical, psychometric, and functional findings. Arch Clin Neuropsychol 16(1):33–44

    Article  CAS  PubMed  Google Scholar 

  • Reisi P, Alaei H, Babri S, Sharifi MR, Mohaddes G (2009) Effects of treadmill running on spatial learning and memory in streptozotocin-induced diabetic rats. Neurosci Lett 455(2):79–83

    Article  CAS  PubMed  Google Scholar 

  • Reisi P, Babri S, Alaei H, Sharifi MR, Mohaddes G, Noorbakhsh SM, Lashgari R (2010) Treadmill running improves long-term potentiation (LTP) defects in streptozotocin-induced diabetes at dentate gyrus in rats. Pathophysiology 17(1):33–38

    Article  PubMed  Google Scholar 

  • Retfalvi T, Nemeth Z, Sarudi I, Albert L (1998) Alteration of endogenous formaldehyde level following mercury accumulation in different pig tissues. Acta biologica Hungarica 49(2–4):375

    CAS  PubMed  Google Scholar 

  • Rondi-Reig L, Petit GH, Tobin C, Tonegawa S, Mariani J, Berthoz A (2006) Impaired Sequential egocentric and allocentric memories in forebrain-specific-NMDA receptor knock-out mice during a new task dissociating strategies of navigation. J Neurosci 26(15):4071–4081

    Article  CAS  PubMed  Google Scholar 

  • Shcherbakova L, Tel'Pukhov V, Trenin S, Bashilov I, Lapkina T (1986) Permeability of the blood–brain barrier to intra-arterial formaldehyde. Biull Eksp Biol Med 102(11):573–575

    CAS  PubMed  Google Scholar 

  • Song MS, Baker GB, Dursun SM, Todd KG (2010) The antidepressant phenelzine protects neurons and astrocytes against formaldehyde-induced toxicity. J Neurochem 114(5):1405–1413

    CAS  PubMed  Google Scholar 

  • Sun AY, Wang Q, Simonyi A, Sun GY (2010) Resveratrol as a therapeutic agent for neurodegenerative diseases. Mol Neurobiol 41(2):375–383

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Szende B, Tyihák E, Trézl L, Szöke E, László I, Kátay G, Király-Véghely Z (1998) Formaldehyde generators and capturers as influencing factors of mitotic and apoptotic processes. Acta biologica Hungarica 49(2–4):323

    CAS  PubMed  Google Scholar 

  • Tang YP, Shimizu E, Dube GR, Rampon C, Kerchner GA, Zhuo M, Liu G, Tsien JZ (1999) Genetic enhancement of learning and memory in mice. Nature 401(6748):63–69

    Article  CAS  PubMed  Google Scholar 

  • Teng S, Beard K, Pourahmad J, Moridani M, Easson E, Poon R, O'Brien PJ (2001) The formaldehyde metabolic detoxification enzyme systems and molecular cytotoxic mechanism in isolated rat hepatocytes. Chemico-Biological Interactions 130:285–296

    Article  PubMed  Google Scholar 

  • Toews J, Rogalski JC, Clark TJ, Kast J (2008) Mass spectrometric identification of formaldehyde-induced peptide modifications under in vivo protein cross-linking conditions. Anal Chim Acta 618(2):168–183

    Article  CAS  PubMed  Google Scholar 

  • Tokuda K, Zorumski CF, Izumi Y (2007) Modulation of hippocampal long-term potentiation by slow increases in ethanol concentration. Neuroscience 146(1):340–349

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tong Z, Luo W, Wang Y, Yang F, Han Y, Li H, Luo H, Duan B, Xu T, Maoying Q (2010) Tumor tissue-derived formaldehyde and acidic microenvironment synergistically induce bone cancer pain. PLoS One 5(4):e10234

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tong Z, Zhang J, Luo W, Wang W, Li F, Li H, Luo H, Lu J, Zhou J, Wan Y, He R (2011) Urine formaldehyde level is inversely correlated to mini mental state examination scores in senile dementia. Neurobiology of aging 32(1):31–41

    Article  CAS  PubMed  Google Scholar 

  • Trézl L, Csiba A, Juhasz S, Szentgyörgyi M, Lombai G, Hullán L, Juhász A (1997) Endogenous formaldehyde level of foods and its biological significance. Zeitschrift für Lebensmitteluntersuchung und -Forschung A 205(4):300–304

    Article  Google Scholar 

  • Tyihák E, Albert L, Németh ZI, Kátay G, Király-Véghely Z, Szende B (1998) Formaldehyde cycle and the natural formaldehyde generators and capturers. Acta biologica Hungarica 49(2–4):225–238

    PubMed  Google Scholar 

  • Wang RS, Nakajima T, Kawamoto T, Honma T (2002) Effects of aldehyde dehydrogenase-2 genetic polymorphisms on metabolism of structurally different aldehydes in human liver. Drug metabolism and disposition 30(1):69–73

    Article  PubMed  Google Scholar 

  • Wang B, Wang J, Zhou S, Tan S, He X, Yang Z, Xie YC, Li S, Zheng C, Ma X (2008) The association of mitochondrial aldehyde dehydrogenase gene (ALDH2) polymorphism with susceptibility to late-onset Alzheimer's disease in Chinese. J Neurol Sci 268(1–2):172–175

    Article  CAS  PubMed  Google Scholar 

  • Wirkner K, Poelchen W, Köles L, Mühlberg K, Scheibler P, Allgaier C, Illes P (1999) Ethanol-induced inhibition of NMDA receptor channels. Neurochem Int 35(2):153–162

    Article  CAS  PubMed  Google Scholar 

  • Wu SC, Zhang Y (2010) Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol 11(9):607–620

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang JF, Qi JS, Qiao JT (2009) Protein kinase C mediates amyloid [beta]-protein fragment 31-35-induced suppression of hippocampal late-phase long-term potentiation in vivo. Neurobiol Learn Mem 91(3):226–234

    Article  CAS  PubMed  Google Scholar 

  • Zhu Y, Carvey PM, Ling Z (2006) Age-related changes in glutathione and glutathione-related enzymes in rat brain. Brain research 1090(1):35–44

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by grants from the Chinese Postdoctoral Fund 20090460047, the Natural Scientific Foundation of China NSFC (31171080, 30970695), the 973 Program (2010CB912303; 2012CB911004), the QCAS Biotechnology Fund (GJHZ1131), CAS-KSCX2-YW-R-119, KSCX2-YW-R-256, QCAS GJHZ1131, and the Johnson & Johnson Corporate Office of Science & Technology.

Author information

Authors and Affiliations

  1. State Key Laboratory of Brain and Cognitive Sciences, Institute of Biophysics, Chinese Academy of Sciences, Graduate University of the Chinese Academy of Sciences, Beijing, 100101, China

    Zhiqian Tong & Chanshuai Han

  2. Central Laboratory, Shantou University Medical College, Guangdong, 515041, China

    Wenhong Luo, Hui Li & Hongjun Luo

  3. University of Science and Technology of China, Anhui, 230026, China

    Jiangning Zhou

  4. Department of Neurobiology and National Key Discipline of Physiology, Shanxi Medical University, Taiyuan, 030001, China

    Xiaohui Wang & Jinshun Qi

  5. State Key Laboratory of Brain and Cognitive Sciences, Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China

    Rongqiao He

  6. Key Lab of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, 100101, China

    Rongqiao He

Authors
  1. Zhiqian Tong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chanshuai Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wenhong Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaohui Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hui Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hongjun Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jiangning Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jinshun Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Rongqiao He
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jinshun Qi or Rongqiao He.

Additional information

Zhiqian Tong, Chanshuai Han, Wenhong Luo, and Xiaohui Wang contributed equally to this work.

About this article

Cite this article

Tong, Z., Han, C., Luo, W. et al. Accumulated hippocampal formaldehyde induces age-dependent memory decline. AGE 35, 583–596 (2013). https://doi.org/10.1007/s11357-012-9388-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11357-012-9388-8

Keywords

Search

Navigation