Skip to main content
SpringerLink
Log in

Blueberry supplementation induces spatial memory improvements and region-specific regulation of hippocampal BDNF mRNA expression in young rats

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale

Flavonoid-rich foods have been shown to be able to reverse age-related cognitive deficits in memory and learning in both animals and humans. However, to date, there have been only a limited number of studies investigating the effects of flavonoid-rich foods on cognition in young/healthy animals.

Objectives

The aim of this study was to investigate the effects of a blueberry-rich diet in young animals using a spatial working memory paradigm, the delayed non-match task, using an eight-arm radial maze. Furthermore, the mechanisms underlying such behavioural effects were investigated.

Results

We show that a 7-week supplementation with a blueberry diet (2 % w/w) improves the spatial memory performance of young rats (2 months old). Blueberry-fed animals also exhibited a faster rate of learning compared to those on the control diet. These behavioural outputs were accompanied by the activation of extracellular signal-related kinase (ERK1/2), increases in total cAMP-response element-binding protein (CREB) and elevated levels of pro- and mature brain-derived neurotrophic factor (BDNF) in the hippocampus. Changes in hippocampal CREB correlated well with memory performance. Further regional analysis of BDNF gene expression in the hippocampus revealed a specific increase in BDNF mRNA in the dentate gyrus and CA1 areas of hippocampi of blueberry-fed animals.

Conclusions

The present study suggests that consumption of flavonoid-rich blueberries has a positive impact on spatial learning performance in young healthy animals, and these improvements are linked to the activation of ERK–CREB–BDNF pathway in the hippocampus.

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

Similar content being viewed by others

References

  • Aberg MA, Aberg ND, Hedbacker H, Oscarsson J, Eriksson PS (2000) Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J Neurosci 20:2896–2903

    PubMed  CAS  Google Scholar 

  • Andres-Lacueva C, Shukitt-Hale B, Galli RL, Jauregui O, Lamuela-Raventos RM, Joseph JA (2005) Anthocyanins in aged blueberry-fed rats are found centrally and may enhance memory. Nutr Neurosci 8:111–120

    Article  PubMed  CAS  Google Scholar 

  • Banerjee S, Smallwood A, Chambers AE, Nicolaides K (2003) Quantitative recovery of immunoreactive proteins from clinical samples following RNA and DNA isolation. Biotechniques 35:450–456

    PubMed  CAS  Google Scholar 

  • Beking K, Vieira A (2011) Flavonoid intake and disability-adjusted life years due to Alzheimer’s and related dementias: a population-based study involving twenty-three developed countries. Public Health Nutr 13:1403–1409

    Article  Google Scholar 

  • Bekinschtein P, Cammarota M, Igaz LM, Bevilaqua LR, Izquierdo I, Medina JH (2007) Persistence of long-term memory storage requires a late protein synthesis- and BDNF-dependent phase in the hippocampus. Neuron 53:261–277

    Article  PubMed  CAS  Google Scholar 

  • Bhutada P, Mundhada Y, Bansod K, Ubgade A, Quazi M, Umathe S, Mundhada D (2010) Reversal by quercetin of corticotrophin releasing factor induced anxiety- and depression-like effect in mice. Prog Neuropsychopharmacol Biol Psychiatry 34:955–960

    Article  PubMed  CAS  Google Scholar 

  • Bito H (1998) A potential mechanism for long-term memory: CREB signaling between the synapse and the nucleus. Seikagaku 70:466–471

    PubMed  CAS  Google Scholar 

  • Brightwell JJ, Smith CA, Neve RL, Colombo PJ (2007) Long-term memory for place learning is facilitated by expression of cAMP response element-binding protein in the dorsal hippocampus. Learn Mem 14:195–199

    Article  PubMed  Google Scholar 

  • Casadesus G, Shukitt-Hale B, Stellwagen HM, Zhu X, Lee HG, Smith MA, Joseph JA (2004) Modulation of hippocampal plasticity and cognitive behavior by short-term blueberry supplementation in aged rats. Nutr Neurosci 7:309–316

    Article  PubMed  CAS  Google Scholar 

  • Chan YC, Hosoda K, Tsai CJ, Yamamoto S, Wang MF (2006) Favorable effects of tea on reducing the cognitive deficits and brain morphological changes in senescence-accelerated mice. J Nutr Sci Vitaminol (Tokyo). 52(4):266–73

    Google Scholar 

  • Choy KH, de Visser Y, Nichols NR, van den Buuse M (2008) Combined neonatal stress and young–adult glucocorticoid stimulation in rats reduce BDNF expression in hippocampus: effects on learning and memory. Hippocampus 18:655–667

    Article  PubMed  CAS  Google Scholar 

  • Cohen-Cory S, Fraser SE (1995) Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature 378:192–196

    Article  PubMed  CAS  Google Scholar 

  • Conkright MD, Guzman E, Flechner L, Su AI, Hogenesch JB, Montminy M (2003) Genome-wide analysis of CREB target genes reveals a core promoter requirement for cAMP responsiveness. Mol Cell 11:1101–1108

    Article  PubMed  CAS  Google Scholar 

  • Conner JM, Lauterborn JC, Yan Q, Gall CM, Varon S (1997) Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J Neurosci 17:2295–2313

    PubMed  CAS  Google Scholar 

  • Countryman RA, Gold PE (2007) Rapid forgetting of social transmission of food preferences in aged rats: relationship to hippocampal CREB activation. Learn Mem 14:350–358

    Article  PubMed  Google Scholar 

  • Cunha C, Brambilla R, Thomas KL (2010) A simple role for BDNF in learning and memory? Front Mol Neurosci 3:1

    PubMed  Google Scholar 

  • Dinges DF (2006) Cocoa flavanols, cerebral blood flow, cognition, and health: going forward. J Cardiovasc Pharmacol 47(Suppl 2):S221–S223

    PubMed  CAS  Google Scholar 

  • Duffy KB, Spangler EL, Devan BD, Guo Z, Bowker JL, Janas AM, Hagepanos A, Minor RK, Decabo R, Mouton PR, Shukitt-Hale B, Joseph JA, Ingram DK (2007) A blueberry-enriched diet provides cellular protection against oxidative stress and reduces a kainate-induced learning impairment in rats. Neurobiol Aging

  • Falkenberg T, Mohammed AK, Henriksson B, Persson H, Winblad B, Lindefors N (1992) Increased expression of brain-derived neurotrophic factor mRNA in rat hippocampus is associated with improved spatial memory and enriched environment. Neurosci Lett 138:153–156

    Article  PubMed  CAS  Google Scholar 

  • Fisher ND, Sorond FA, Hollenberg NK (2006) Cocoa flavanols and brain perfusion. J Cardiovasc Pharmacol 47(Suppl 2):S210–S214

    Article  PubMed  CAS  Google Scholar 

  • Francis ST, Head K, Morris PG, Macdonald IA (2006) The effect of flavanol-rich cocoa on the fMRI response to a cognitive task in healthy young people. J Cardiovasc Pharmacol 47(Suppl 2):S215–S220

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Pinilla F (2008) Brain foods: the effects of nutrients on brain function. Nat Rev Neurosci 9:568–578

    Article  PubMed  CAS  Google Scholar 

  • Goyarzu P, Malin DH, Lau FC, Taglialatela G, Moon WD, Jennings R, Moy E, Moy D, Lippold S, Shukitt-Hale B, Joseph JA (2004) Blueberry supplemented diet: effects on object recognition memory and nuclear factor-kappa B levels in aged rats. Nutr Neurosci 7:75–83

    Article  PubMed  Google Scholar 

  • Haque AM, Hashimoto M, Katakura M, Tanabe Y, Hara Y, Shido O (2006) Long-term administration of green tea catechins improves spatial cognition learning ability in rats. J Nutr 136:1043–1047

    PubMed  CAS  Google Scholar 

  • Hartman RE, Shah A, Fagan AM, Schwetye KE, Parsadanian M, Schulman RN, Finn MB, Holtzman DM (2006) Pomegranate juice decreases amyloid load and improves behavior in a mouse model of Alzheimer’s disease. Neurobiol Dis 24(3):506–15

    Google Scholar 

  • Hoffman JR, Donato A, Robbins SJ (2004) Ginkgo biloba promotes short-term retention of spatial memory in rats. Pharmacol Biochem Behav 77:533–539

    Article  PubMed  CAS  Google Scholar 

  • Hou Y, Aboukhatwa MA, Lei DL, Manaye K, Khan I, Luo Y (2010) Anti-depressant natural flavonols modulate BDNF and beta amyloid in neurons and hippocampus of double TgAD mice. Neuropharmacology 58:911–920

    Article  PubMed  CAS  Google Scholar 

  • Jeon SJ, Rhee SY, Seo JE, Bak HR, Lee SH, Ryu JH, Cheong JH, Shin CY, Kim GH, Lee YS, Ko KH (2011) Oroxylin A increases BDNF production by activation of MAPK-CREB pathway in rat primary cortical neuronal culture. Neurosci Res 69:214–222

    Article  PubMed  CAS  Google Scholar 

  • Jerman T, Kesner RP (2006) Disconnection analysis of CA3 and DG in mediating encoding but not retrieval in a spatial maze learning task. Learn Mem 13:458–464

    Google Scholar 

  • Joseph JA, Shukitt-Hale B, Denisova NA, Prior RL, Cao G, Martin A, Taglialatela G, Bickford PC (1998) Long-term dietary strawberry, spinach, or vitamin E supplementation retards the onset of age-related neuronal signal-transduction and cognitive behavioral deficits. J Neurosci 18:8047–8055

    PubMed  CAS  Google Scholar 

  • Joseph JA, Shukitt-Hale B, Denisova NA, Bielinski D, Martin A, McEwen JJ, Bickford PC (1999) Reversals of age-related declines in neuronal signal transduction, cognitive, and motor behavioral deficits with blueberry, spinach, or strawberry dietary supplementation. J Neurosci 19:8114–8121

    PubMed  CAS  Google Scholar 

  • Joseph JA, Denisova NA, Arendash G, Gordon M, Diamond D, Shukitt-Hale B, Morgan D (2003) Blueberry supplementation enhances signaling and prevents behavioral deficits in an Alzheimer disease model. Nutr Neurosci 6:153–162

    Article  PubMed  CAS  Google Scholar 

  • Kaur T, Pathak CM, Pandhi P, Khanduja KL (2008) Effects of green tea extract on learning, memory, behavior and acetylcholinesterase activity in young and old male rats. Brain Cogn 67(1):25–30

    Google Scholar 

  • Kelleher RJ 3rd, Govindarajan A, Tonegawa S (2004) Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 44:59–73

    Article  PubMed  CAS  Google Scholar 

  • Krikorian R, Shidler MD, Nash TA, Kalt W, Vinqvist-Tymchuk MR, Shukitt-Hale B, Joseph JA (2010) Blueberry supplementation improves memory in older adults. J Agric Food Chem 58:3996–4000

    Article  PubMed  CAS  Google Scholar 

  • Kromhout D, Menotti A, Kesteloot H, Sans S (2002) Prevention of coronary heart disease by diet and lifestyle: evidence from prospective cross-cultural, cohort, and intervention studies. Circulation 105:893–898

    Article  PubMed  Google Scholar 

  • Kuriyama S, Hozawa A, Ohmori K, Shimazu T, Matsui T, Ebihara S, Awata S, Nagatomi R, Arai H, Tsuji I (2006) Green tea consumption and cognitive function: a cross-sectional study from the Tsurugaya Project 1. Am J Clin Nutr 83(2):355–361

    Google Scholar 

  • Lai HC, Chao WT, Chen YT, Yang VC (2004) Effect of EGCG, a major component of green tea, on the expression of Ets-1, c-Fos, and c-Jun during angiogenesis in vitro. Cancer Lett 213(2):181–188

    Google Scholar 

  • Lassalle JM, Bataille T, Halley H (2000) Reversible inactivation of the hippocampal mossy fiber synapses in mice impairs spatial learning, but neither consolidation nor memory retrieval, in the Morris navigation task. Neurobiology of learning and memory 73(3):243–257

    Google Scholar 

  • Lee I, Kesner RP (2003) Differential roles of dorsal hippocampal subregions in spatial working memory with short versus intermediate delay. Behav Neurosci 117:1044–1053

    Article  PubMed  Google Scholar 

  • Lee I, Kesner RP (2004) Encoding versus retrieval of spatial memory: double dissociation between the dentate gyrus and the perforant path inputs into CA3 in the dorsal hippocampus. Hippocampus 14(1):66–76

    Google Scholar 

  • Letenneur L, Proust-Lima C, Le Gouge A, Dartigues JF, Barberger-Gateau P (2007) Flavonoid intake and cognitive decline over a 10-year period. Am J Epidemiol 165:1364–1371

    Article  PubMed  CAS  Google Scholar 

  • Leutgeb S, Leutgeb JK, Treves A, Moser MB, Moser EI (2004) Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305:1295–1298

    Article  PubMed  CAS  Google Scholar 

  • Li Q, Zhao HF, Zhang ZF, Liu ZG, Pei XR, Wang JB, Cai MY, Li Y (2009a) Long-term administration of green tea catechins prevents age-related spatial learning and memory decline in C57BL/6 J mice by regulating hippocampal cyclic amp-response element binding protein signaling cascade. Neuroscience 159:1208–1215

    Article  PubMed  CAS  Google Scholar 

  • Li Q, Zhao HF, Zhang ZF, Liu ZG, Pei XR, Wang JB, Li Y (2009b) Long-term green tea catechin administration prevents spatial learning and memory impairment in senescence-accelerated mouse prone-8 mice by decreasing Abeta1-42 oligomers and upregulating synaptic plasticity-related proteins in the hippocampus. Neuroscience 163:741–749

    Article  PubMed  CAS  Google Scholar 

  • Liu RY, Fioravante D, Shah S, Byrne JH (2008) cAMP response element-binding protein 1 feedback loop is necessary for consolidation of long-term synaptic facilitation in Aplysia. J Neurosci 28:1970–1976

    Article  PubMed  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Macready AL, Kennedy OB, Ellis JA, Williams CM, Spencer JP, Butler LT (2009) Flavonoids and cognitive function: a review of human randomized controlled trial studies and recommendations for future studies. Genes Nutr 4:227–242

    Article  PubMed  CAS  Google Scholar 

  • McAllister AK, Katz LC, Lo DC (1999) Neurotrophins and synaptic plasticity. Annu Rev Neurosci 22:295–318

    Article  PubMed  CAS  Google Scholar 

  • Mizuno M, Yamada K, Olariu A, Nawa H, Nabeshima T (2000) Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J Neurosci 20:7116–7121

    PubMed  CAS  Google Scholar 

  • Mohamed HA, Yao W, Fioravante D, Smolen PD, Byrne JH (2005) cAMP-response elements in Aplysia creb1, creb2, and Ap-uch promoters: implications for feedback loops modulating long-term memory. J Biol Chem 280:27035–27043

    Article  PubMed  CAS  Google Scholar 

  • Nakamura EM, da Silva EA, Concilio GV, Wilkinson DA, Masur J (1991) Reversible effects of acute and long-term administration of delta-9-tetrahydrocannabinol (THC) on memory in the rat. Drug Alcohol Depend 28:167–175

    Article  PubMed  CAS  Google Scholar 

  • Oliveira DR, Sanada PF, Saragossa Filho AC, Innocenti LR, Oler G, Cerutti JM, Cerutti SM (2009) Neuromodulatory property of standardized extract Ginkgo biloba L. (EGb 761) on memory: behavioral and molecular evidence. Brain Res 1269:68–89

    Article  PubMed  CAS  Google Scholar 

  • Olton DS, Papas BC (1979) Spatial memory and hippocampal function. Neuropsychologia 17:669–682

    Article  PubMed  CAS  Google Scholar 

  • Olton DS, Samuelson RJ (1976) Remembrance of places passed—spatial memory in rats. J Exp Psychol Anim Behav Process 2:97–116

    Article  Google Scholar 

  • Parrott MD, Greenwood CE (2007) Dietary influences on cognitive function with aging: from high-fat diets to healthful eating. Ann N Y Acad Sci 1114:389–397

    Article  PubMed  CAS  Google Scholar 

  • Phillips HS, Hains JM, Laramee GR, Rosenthal A, Winslow JW (1990) Widespread expression of BDNF but not NT3 by target areas of basal forebrain cholinergic neurons. Science 250:290–294

    Article  PubMed  CAS  Google Scholar 

  • Ramirez MR, Izquierdo I, do Carmo Bassols Raseira M, Zuanazzi JA, Barros D, Henriques AT (2005) Effect of lyophilised Vaccinium berries on memory, anxiety and locomotion in adult rats. Pharmacol Res 52:457–462

    Article  PubMed  Google Scholar 

  • Rattray M, Michael GJ, Lee J, Wotherspoon G, Bendotti C, Priestley JV (1999) Intraregional variation in expression of serotonin transporter messenger RNA by 5-hydroxytryptamine neurons. Neuroscience 88:169–183

    Article  PubMed  CAS  Google Scholar 

  • Rendeiro C, Spencer JP, Vauzour D, Butler LT, Ellis JA, Williams CM (2009) The impact of flavonoids on spatial memory in rodents: from behaviour to underlying hippocampal mechanisms. Genes Nutr 4(4):251–270

    Article  PubMed  CAS  Google Scholar 

  • Ried K, Sullivan T, Fakler P, Frank OR, Stocks NP (2010) Does chocolate reduce blood pressure? A meta-analysis. BMC Med 8:39

    Article  PubMed  Google Scholar 

  • Robbins RJ, Leonczak J, Johnson JC, Li J, Kwik-Uribe C, Prior RL, Gu L (2009) Method performance and multi-laboratory assessment of a normal phase high pressure liquid chromatography-fluorescence detection method for the quantitation of flavanols and procyanidins in cocoa and chocolate containing samples. J Chromatogr A 1216:4831–4840

    Article  PubMed  CAS  Google Scholar 

  • Rolls ET, Kesner RP (2006) A computational theory of hippocampal function, and empirical tests of the theory. Prog Neurobiol 79:1–48

    Article  PubMed  CAS  Google Scholar 

  • Schaaf MJ, Workel JO, Lesscher HM, Vreugdenhil E, Oitzl MS, de Kloet ER (2001) Correlation between hippocampal BDNF mRNA expression and memory performance in senescent rats. Brain Res 915:227–233

    Article  PubMed  CAS  Google Scholar 

  • Schroeter H, Bahia P, Spencer JP, Sheppard O, Rattray M, Cadenas E, Rice-Evans C, Williams RJ (2007) (−)Epicatechin stimulates ERK-dependent cyclic AMP response element activity and up-regulates GluR2 in cortical neurons. J Neurochem 101:1596–1606

    Article  PubMed  CAS  Google Scholar 

  • Sekeres MJ, Neve RL, Frankland PW, Josselyn SA (2010) Dorsal hippocampal CREB is both necessary and sufficient for spatial memory. Learn Mem 17:280–283

    Article  PubMed  CAS  Google Scholar 

  • Shif O, Gillette K, Damkaoutis CM, Carrano C, Robbins SJ, Hoffman JR (2006) Effects of Ginkgo biloba administered after spatial learning on water maze and radial arm maze performance in young adult rats. Pharmacol Biochem Behav 84:17–25

    Article  PubMed  CAS  Google Scholar 

  • Shukitt-Hale B, Lau FC, Carey AN, Galli RL, Spangler EL, Ingram DK, Joseph JA (2008) Blueberry polyphenols attenuate kainic acid-induced decrements in cognition and alter inflammatory gene expression in rat hippocampus. Nutr Neurosci 11:172–182

    Article  PubMed  CAS  Google Scholar 

  • Silhol M, Arancibia S, Maurice T, Tapia-Arancibia L (2007) Spatial memory training modifies the expression of brain-derived neurotrophic factor tyrosine kinase receptors in young and aged rats. Neuroscience 146:962–973

    Article  PubMed  CAS  Google Scholar 

  • Spencer JP (2008) Flavonoids: modulators of brain function? Br J Nutr 99 E Suppl 1:ES60–77

    Google Scholar 

  • Sweatt JD (2001) The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76:1–10

    Article  PubMed  CAS  Google Scholar 

  • Sweatt JD (2004) Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 14:311–317

    Article  PubMed  CAS  Google Scholar 

  • Tao X, Finkbeiner S, Arnold DB, Shaywitz AJ, Greenberg ME (1998) Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20:709–726

    Article  PubMed  CAS  Google Scholar 

  • Unno K, Takabayashi F, Yoshida H, Choba D, Fukutomi R, Kikunaga N, Kishido T, Oku N, Hoshino M (2007) Daily consumption of green tea catechin delays memory regression in aged mice. Biogerontology 8(2):89–95

    Google Scholar 

  • Vago DR, Kesner RP (2005) An electrophysiological and behavioural characterization of the temporoammonic pathway: disruption produces deficits in retrieval and spatial mismatch. Soc Neurosci Abstr 647:5

    Google Scholar 

  • van Praag H (2008) Neurogenesis and exercise: past and future directions. Neuromolecular Med 10:128–140

    Article  PubMed  Google Scholar 

  • van Praag H (2009) Exercise and the brain: something to chew on. Trends Neurosci 32:283–290

    Article  PubMed  Google Scholar 

  • van Praag H, Lucero MJ, Yeo GW, Stecker K, Heivand N, Zhao C, Yip E, Afanador M, Schroeter H, Hammerstone J, Gage FH (2007) Plant-derived flavanol (−)epicatechin enhances angiogenesis and retention of spatial memory in mice. J Neurosci 27:5869–5878

    Article  PubMed  Google Scholar 

  • Vauzour D, Vafeiadou K, Rice-Evans C, Williams RJ, Spencer JP (2007) Activation of pro-survival Akt and ERK1/2 signalling pathways underlie the anti-apoptotic effects of flavanones in cortical neurons. J Neurochem 103(4):1355–1367

    Google Scholar 

  • Vignes M, Maurice T, Lante F, Nedjar M, Thethi K, Guiramand J, Recasens M (2006) Anxiolytic properties of green tea polyphenol (−)-epigallocatechin gallate (EGCG). Brain Res 1110:102–115

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Wang L, Wu J, Cai J (2006) The in vivo synaptic plasticity mechanism of EGb 761-induced enhancement of spatial learning and memory in aged rats. Br J Pharmacol 148:147–153

    Article  PubMed  CAS  Google Scholar 

  • Ward CP, Redd K, Williams BM, Caler JR, Luo Y, McCoy JG (2002) Ginkgo biloba extract: cognitive enhancer or antistress buffer. Pharmacol Biochem Behav 72:913–922

    Article  PubMed  CAS  Google Scholar 

  • Williams CM, El Mohsen MA, Vauzour D, Rendeiro C, Butler LT, Ellis JA, Whiteman M, Spencer JP (2008) Blueberry-induced changes in spatial working memory correlate with changes in hippocampal CREB phosphorylation and brain-derived neurotrophic factor (BDNF) levels. Free Radic Biol Med 45:295–305

    Article  PubMed  CAS  Google Scholar 

  • Williams RJ, Spencer JP, Rice-Evans C (2004) Flavonoids: antioxidants or signalling molecules? Free Radic Biol Med 36(7):838–49

    Google Scholar 

  • Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132:645–660

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Biotechnology and Biological Sciences Research Council (grant: BB/F008953/1) and the Fundação para a Ciência e a Tecnologia (grant: SFRH/BD/69711/2010) and they were greatly appreciated.

Author information

Authors and Affiliations

  1. Molecular Nutrition Group, School of Chemistry, Food and Pharmacy, University of Reading, Reading, RG6 6AP, UK

    Catarina Rendeiro & Jeremy P. E. Spencer

  2. Department of Nutrition, Norwich Medical School, Faculty of Medicine and Health Sciences, University of East Anglia, Norwich, NR4 7TJ, UK

    David Vauzour

  3. School of Psychology and Clinical Language Sciences, University of Reading, Harry Pitt Building Earley Gate, Reading, RG6 7BE, UK

    Catarina Rendeiro, Rebecca J. Kean, Laurie T. Butler & Claire M. Williams

  4. Reading School of Pharmacy, University of Reading, Reading, RG6 6UB, UK

    Marcus Rattray

Authors
  1. Catarina Rendeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David Vauzour
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rebecca J. Kean
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Laurie T. Butler
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marcus Rattray
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jeremy P. E. Spencer
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Claire M. Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claire M. Williams.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rendeiro, C., Vauzour, D., Kean, R.J. et al. Blueberry supplementation induces spatial memory improvements and region-specific regulation of hippocampal BDNF mRNA expression in young rats. Psychopharmacology 223, 319–330 (2012). https://doi.org/10.1007/s00213-012-2719-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-012-2719-8

Keywords

Search

Navigation