Skip to main content

Advertisement

Log in

Spontaneous object recognition and its relevance to schizophrenia: a review of findings from pharmacological, genetic, lesion and developmental rodent models

  • Review
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale

Spontaneous (novel) object recognition (SOR) is one of the most widely used rodent behavioural tests. The opportunity for rapid data collection has made SOR a popular choice in studies that explore cognitive impairment in rodent models of schizophrenia, and that test the efficacy of drugs intended to reverse these deficits.

Objectives

We provide an overview of the many recent studies that have used SOR to explore the mnemonic effects of manipulation of the key transmitter systems relevant to schizophrenia—the dopamine, glutamate, GABA, acetylcholine, serotonin and cannabinoid systems—alone or in combination. We also review the use of SOR in studying memory in genetically modified mouse models of schizophrenia, as well as in neurodevelopmental and lesion models. We end by discussing the construct and predictive validity, and translational relevance, of SOR with respect to cognitive impairment in schizophrenia.

Results

Perturbation of the dopamine or glutamate systems can generate robust and reliable impairment in SOR. Impaired performance is also seen following antagonism of the muscarinic acetylcholine system, or exposure to cannabinoid agonists. Cognitive enhancement has been reported using alpha7-nicotinic acetylcholine receptor agonists and 5-HT6 antagonists. Among non-pharmacological models, neonatal ventral hippocampal lesions and maternal immune activation can impair SOR, while mixed results have been obtained with mice carrying mutations in schizophrenia risk-associated genes, including neuregulin and COMT.

Conclusions

While SOR is not without its limitations, the task represents a useful method for studying manipulations with relevance to cognitive impairment in schizophrenia, as well as the interactions between them.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Notes

  1. There is evidence to suggest that the same structures within the temporal lobe mediate both memory for objects and perceptual discrimination between them (e.g. Cowell et al. 2006; Bussey and Saksida 2005). Thus, perirhinal cortex lesions impair SOR at longer but not shorter delays when standard objects are used, but when perceptually similar objects are used such lesions can produce impairments when there is little or no delay (Bartko et al. 2007). Nevertheless, short delays should be included in experiments using standard objects to rule out gross perceptual (e.g. visual acuity) deficits as a possible reason for impairment at longer delays.

References

  • Abe H, Ishida Y, Iwasaki T (2004) Perirhinal N-methyl-D-aspartate and muscarinic systems participate in object recognition in rats. Neurosci Lett 356:191–194

    Article  PubMed  CAS  Google Scholar 

  • Adler CM, Malhotra AK, Elman I, Goldberg T, Egan M, Pickar D, Breier A (1999) Comparison of ketamine-induced thought disorder in healthy volunteers and thought disorder in schizophrenia. Am J Psychiatry 156:1646–1649

    PubMed  CAS  Google Scholar 

  • Aggleton JP, Brown MW (2006) Interleaving brain systems for episodic and recognition memory. Trends Cogn Sci 10:455–463

    Article  PubMed  Google Scholar 

  • Aggleton JP, Hunt PR, Rawlins JN (1986) The effects of hippocampal lesions upon spatial and non-spatial tests of working memory. Behav Brain Res 19:133–146

    Article  PubMed  CAS  Google Scholar 

  • Aggleton JP, Keen S, Warburton EC, Bussey TJ (1997) Extensive cytotoxic lesions involving both the rhinal cortices and area TE impair recognition but spare spatial alternation in the rat. Brain Res Bull 43:279–287

    Article  PubMed  CAS  Google Scholar 

  • Aisa B, Tordera R, Lasheras B, Del Rio J, Ramirez MJ (2008) Effects of maternal separation on hypothalamic-pituitary-adrenal responses, cognition and vulnerability to stress in adult female rats. Neuroscience 154:1218–1226

    Article  PubMed  CAS  Google Scholar 

  • Akhondzadeh S, Gerami M, Noroozian M, Karamghadiri N, Ghoreishi A, Abbasi SH, Rezazadeh SA (2008) A 12-week, double-blind, placebo-controlled trial of donepezil adjunctive treatment to risperidone in chronic and stable schizophrenia. Prog Neuropsychopharmacol Biol Psychiatr 32:1810–1815

    Article  CAS  Google Scholar 

  • Albuquerque EX, Alkondon M, Pereira EF, Castro NG, Schrattenholz A, Barbosa CT, Bonfante-Cabarcas R, Aracava Y, Eisenberg HM, Maelicke A (1997) Properties of neuronal nicotinic acetylcholine receptors: pharmacological characterization and modulation of synaptic function. J Pharmacol Exp Ther 280:1117–1136

    PubMed  CAS  Google Scholar 

  • Andreasson S, Allebeck P, Engstrom A, Rydberg U (1987) Cannabis and schizophrenia. A longitudinal study of Swedish conscripts. Lancet 2:1483–1486

    Article  PubMed  CAS  Google Scholar 

  • Arnt J, Bang-Andersen B, Grayson B, Bymaster FP, Cohen MP, DeLapp NW, Giethlen B, Kreilgaard M, McKinzie DL, Neill JC, Nelson DL, Nielsen SM, Poulsen MN, Schaus JM, Witten LM (2010) Lu AE58054, a 5-HT(6) antagonist, reverses cognitive impairment induced by subchronic phencyclidine in a novel object recognition test in rats. Int J Neuropsychopharmacol 13:1021–1033

    Article  PubMed  CAS  Google Scholar 

  • Arseneault L, Cannon M, Poulton R, Murray R, Caspi A, Moffitt TE (2002) Cannabis use in adolescence and risk for adult psychosis: longitudinal prospective study. BMJ 325:1212–1213

    Article  PubMed  Google Scholar 

  • Babovic D, O’Tuathaigh CM, O’Connor AM, O’Sullivan GJ, Tighe O, Croke DT, Karayiorgou M, Gogos JA, Cotter D, Waddington JL (2008) Phenotypic characterization of cognition and social behavior in mice with heterozygous versus homozygous deletion of catechol-O-methyltransferase. Neuroscience 155:1021–1029

    Article  PubMed  CAS  Google Scholar 

  • Baker KB, Kim JJ (2002) Effects of stress and hippocampal NMDA receptor antagonism on recognition memory in rats. Learn Mem 9:58–65

    Article  PubMed  Google Scholar 

  • Ballaz SJ, Akil H, Watson SJ (2007) The 5-HT7 receptor: role in novel object discrimination and relation to novelty-seeking behavior. Neuroscience 149:192–202

    Article  PubMed  CAS  Google Scholar 

  • Barker GR, Bashir ZI, Brown MW, Warburton EC (2006) A temporally distinct role for group I and group II metabotropic glutamate receptors in object recognition memory. Learn Mem 13:178–186

    Article  PubMed  CAS  Google Scholar 

  • Barna I, Soproni K, Arszovszki A, Csabai K, Haller J (2007) WIN-55,212-2 chronically implanted into the CA3 region of the dorsal hippocampus impairs learning: a novel method for studying chronic, brain-area-specific effects of cannabinoids. Behav Pharmacol 18:515–520

    Article  PubMed  Google Scholar 

  • Barnett JH, Werners U, Secher SM, Hill KE, Brazil R, Masson K, Pernet DE, Kirkbride JB, Murray GK, Bullmore ET, Jones PB (2007) Substance use in a population-based clinic sample of people with first-episode psychosis. Br J Psychiatry 190:515–520

    Article  PubMed  Google Scholar 

  • Bartko SJ, Winters BD, Cowell RA, Saksida LM, Bussey TJ (2007) Perceptual functions of perirhinal cortex in rats: zero-delay object recognition and simultaneous oddity discriminations. J Neurosci 27:2548–2559

    Article  PubMed  CAS  Google Scholar 

  • Beaulieu JM, Gainetdinov RR (2011) The physiology, signaling and pharmacology of dopamine receptors. Pharmacol Rev 63:182–217

    Article  PubMed  CAS  Google Scholar 

  • Belcher AM, Feinstein EM, O’Dell SJ, Marshall JF (2008) Methamphetamine influences on recognition memory: comparison of escalating and single-day dosing regimens. Neuropsychopharmacology 33:1453–1463

    Article  PubMed  CAS  Google Scholar 

  • Bentley J, Marsden C, Sleight A, Fone K (1999) Effect of the 5-HT6 antagonist, Ro 04–6790, on food consumption in rats trained to a fixed feeding regime. Br J Pharmacol: U38-U38

  • Bernstein HG, Grecksch G, Becker A, Hollt V, Bogerts B (1999) Cellular changes in rat brain areas associated with neonatal hippocampal damage. Neuroreport 10:2307–2311

    Article  PubMed  CAS  Google Scholar 

  • Bhardwaj SK, Baharnoori M, Sharif-Askari B, Kamath A, Williams S, Srivastava LK (2009) Behavioral characterization of dysbindin-1 deficient sandy mice. Behav Brain Res 197:435–441

    Google Scholar 

  • Bianchi M, Fone KF, Azmi N, Heidbreder CA, Hagan JJ, Marsden CA (2006) Isolation rearing induces recognition memory deficits accompanied by cytoskeletal alterations in rat hippocampus. Eur J Neurosci 24:2894–2902

    Article  PubMed  CAS  Google Scholar 

  • Biton B, Bergis OE, Galli F, Nedelec A, Lochead AW, Jegham S, Godet D, Lanneau C, Santamaria R, Chesney F, Leonardon J, Granger P, Debono MW, Bohme GA, Sgard F, Besnard F, Graham D, Coste A, Oblin A, Curet O, Vige X, Voltz C, Rouquier L, Souilhac J, Santucci V, Gueudet C, Francon D, Steinberg R, Griebel G, Oury-Donat F, George P, Avenet P, Scatton B (2007) SSR180711, a novel selective alpha7 nicotinic receptor partial agonist: (1) binding and functional profile. Neuropsychopharmacology 32:1–16

    Article  PubMed  CAS  Google Scholar 

  • Boess FG, De Vry J, Erb C, Flessner T, Hendrix M, Luithle J, Methfessel C, Riedl B, Schnizler K, van der Staay FJ, van Kampen M, Wiese WB, Koenig G (2007) The novel alpha7 nicotinic acetylcholine receptor agonist N-[(3R)-1-azabicyclo[2.2.2]oct-3-yl]-7-[2-(methoxy)phenyl]-1-benzofuran-2-carboxamide improves working and recognition memory in rodents. J Pharmacol Exp Ther 321:716–725

    Article  PubMed  CAS  Google Scholar 

  • Bortolozzi A, Diaz-Mataix L, Toth M, Celada P, Artigas F (2007) In vivo actions of aripiprazole on serotonergic and dopaminergic systems in rodent brain. Psychopharmacology (Berl) 191:745–758

    Article  CAS  Google Scholar 

  • Botton PH, Costa MS, Ardais AP, Mioranzza S, Souza DO, da Rocha JB, Porciuncula LO (2010) Caffeine prevents disruption of memory consolidation in the inhibitory avoidance and novel object recognition tasks by scopolamine in adult mice. Behav Brain Res 214:254–259

    Article  PubMed  CAS  Google Scholar 

  • Boultadakis A, Liakos P, Pitsikas N (2010) The nitric oxide-releasing derivative of ferulic acid NCX 2057 antagonized delay-dependent and scopolamine-induced performance deficits in a recognition memory task in the rat. Prog Neuropsychopharmacol Biol Psychiatr 34:5–9

    Article  CAS  Google Scholar 

  • Bradley SR, Lameh J, Ohrmund L, Son T, Bajpai A, Nguyen D, Friberg M, Burstein ES, Spalding TA, Ott TR, Schiffer HH, Tabatabaei A, McFarland K, Davis RE, Bonhaus DW (2010) AC-260584, an orally bioavailable M(1) muscarinic receptor allosteric agonist, improves cognitive performance in an animal model. Neuropharmacology 58:365–373

    Article  PubMed  CAS  Google Scholar 

  • Bromley E (2005) A collaborative approach to targeted treatment development for schizophrenia: a qualitative evaluation of the NIMH-MATRICS project. Schizophr Bull 31:954–961

    Article  PubMed  Google Scholar 

  • Brown AS (2006) Prenatal infection as a risk factor for schizophrenia. Schizophr Bull 32:200–202

    Article  PubMed  Google Scholar 

  • Brown MW, Bashir ZI (2002) Evidence concerning how neurons of the perirhinal cortex may effect familiarity discrimination. Philos Trans R Soc Lond B Biol Sci 357:1083–1095

    Article  PubMed  CAS  Google Scholar 

  • Brown MW, Xiang JZ (1998) Recognition memory: neuronal substrates of the judgement of prior occurrence. Prog Neurobiol 55:149–189

    Article  PubMed  CAS  Google Scholar 

  • Brown AS, Begg MD, Gravenstein S, Schaefer CA, Wyatt RJ, Bresnahan M, Babulas VP, Susser ES (2004) Serologic evidence of prenatal influenza in the etiology of schizophrenia. Arch Gen Psychiatry 61:774–780

    Article  PubMed  Google Scholar 

  • Buchanan RW, Summerfelt A, Tek C, Gold J (2003) An open-labeled trial of adjunctive donepezil for cognitive impairments in patients with schizophrenia. Schizophr Res 59:29–33

    Article  PubMed  Google Scholar 

  • Buchanan RW, Conley RR, Dickinson D, Ball MP, Feldman S, Gold JM, McMahon RP (2008) Galantamine for the treatment of cognitive impairments in people with schizophrenia. Am J Psychiatry 165:82–89

    Article  PubMed  Google Scholar 

  • Bussey TJ, Saksida LM (2005) Object memory and perception in the medial temporal lobe: an alternative approach. Curr Opin Neurobiol 15:730–737

    Article  PubMed  CAS  Google Scholar 

  • Bussey TJ, Muir JL, Aggleton JP (1999) Functionally dissociating aspects of event memory: the effects of combined perirhinal and postrhinal cortex lesions on object and place memory in the rat. J Neurosci 19:495–502

    PubMed  CAS  Google Scholar 

  • Bussey TJ, Duck J, Muir JL, Aggleton JP (2000) Distinct patterns of behavioural impairments resulting from fornix transection or neurotoxic lesions of the perirhinal and postrhinal cortices in the rat. Behav Brain Res 111:187–202

    Article  PubMed  CAS  Google Scholar 

  • Bussey TJ, Holmes A, Lyon L, Mar AC, McAllister KA, Nithianantharajah J, Oomen CA, Saksida LM (2011) New translational assays for preclinical modelling of cognition in schizophrenia: the touchscreen testing method for mice and rats. Neuropharmacology [Epub ahead of print].

  • Byrne M, Agerbo E, Bennedsen B, Eaton WW, Mortensen PB (2007) Obstetric conditions and risk of first admission with schizophrenia: a Danish national register based study. Schizophr Res 97:51–59

    Article  PubMed  Google Scholar 

  • Calkins ME, Gur RC, Ragland JD, Gur RE (2005) Face recognition memory deficits and visual object memory performance in patients with schizophrenia and their relatives. Am J Psychiatry 162:1963–1966

    Article  PubMed  Google Scholar 

  • Camarasa J, Rodrigo T, Pubill D, Escubedo E (2010) Memantine is a useful drug to prevent the spatial and non-spatial memory deficits induced by methamphetamine in rats. Pharmacol Res 62:450–456

    Article  PubMed  CAS  Google Scholar 

  • Carli M, Bonalumi P, Samanin R (1997) WAY 100635, a 5-HT1A receptor antagonist, prevents the impairment of spatial learning caused by intrahippocampal administration of scopolamine or 7-chloro-kynurenic acid. Brain Res 774:167–174

    Article  PubMed  CAS  Google Scholar 

  • Carlsson A, Lindqvist M (1963) Effect of chlorpromazine or haloperidol on formation of 3-methoxytyramine and normetanephrine in mouse brain. Acta Pharmacol Toxicol (Copenh) 20:140–144

    Article  CAS  Google Scholar 

  • Chan MH, Chiu PH, Sou JH, Chen HH (2008) Attenuation of ketamine-evoked behavioral responses by mGluR5 positive modulators in mice. Psychopharmacology (Berl) 198:141–148

    Article  CAS  Google Scholar 

  • Chiu CQ, Puente N, Grandes P, Castillo PE (2010) Dopaminergic modulation of endocannabinoid-mediated plasticity at GABAergic synapses in the prefrontal cortex. J Neurosci 30:7236–7248

    Article  PubMed  CAS  Google Scholar 

  • Chung YC, Lee CR, Park TW, Yang KH, Kim KW (2009) Effect of donepezil added to atypical antipsychotics on cognition in patients with schizophrenia: an open-label trial. World J Biol Psychiatry 10:156–162

    Article  PubMed  Google Scholar 

  • Clancy B, Darlington RB, Finlay BL (2001) Translating developmental time across mammalian species. Neuroscience 105:7–17

    Article  PubMed  CAS  Google Scholar 

  • Clark RE, Zola SM, Squire LR (2000) Impaired recognition memory in rats after damage to the hippocampus. J Neurosci 20:8853–8860

    PubMed  CAS  Google Scholar 

  • Clark RE, Kuczenski R, Segal DS (2007) Escalating dose, multiple binge methamphetamine regimen does not impair recognition memory in rats. Synapse 61:515–522

    Article  PubMed  CAS  Google Scholar 

  • Clarke JR, Rossato JI, Monteiro S, Bevilaqua LR, Izquierdo I, Cammarota M (2008) Posttraining activation of CB1 cannabinoid receptors in the CA1 region of the dorsal hippocampus impairs object recognition long-term memory. Neurobiol Learn Mem 90:374–381

    Article  PubMed  CAS  Google Scholar 

  • Cowell RA, Bussey TJ, Saksida LM (2006) Why does brain damage impair memory? A connectionist model of object recognition memory in perirhinal cortex. J Neurosci 26:12186–12197

    Article  PubMed  CAS  Google Scholar 

  • Coyle JT (2006) Glutamate and schizophrenia: beyond the dopamine hypothesis. Cell Mol Neurobiol 26:365–384

    Article  PubMed  CAS  Google Scholar 

  • Coyle P, Tran N, Fung JN, Summers BL, Rofe AM (2009) Maternal dietary zinc supplementation prevents aberrant behaviour in an object recognition task in mice offspring exposed to LPS in early pregnancy. Behav Brain Res 197:210–218

    Article  PubMed  CAS  Google Scholar 

  • Crabbe JC, Wahlsten D, Dudek BC (1999) Genetics of mouse behavior: interactions with laboratory environment. Science 284:1670–1672

    Article  PubMed  CAS  Google Scholar 

  • Creese I, Burt DR, Snyder SH (1976) Dopamine receptor binding predicts clinical and pharmacological potencies of antischizophrenic drugs. Science 192:481–483

    Article  PubMed  CAS  Google Scholar 

  • Dalman C, Thomas HV, David AS, Gentz J, Lewis G, Allebeck P (2001) Signs of asphyxia at birth and risk of schizophrenia. Population-based case–control study. Br J Psychiatry 179:403–408

    Article  PubMed  CAS  Google Scholar 

  • Damgaard T, Larsen DB, Hansen SL, Grayson B, Neill JC, Plath N (2010) Positive modulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors reverses sub-chronic PCP-induced deficits in the novel object recognition task in rats. Behav Brain Res 207:144–150

    Article  PubMed  CAS  Google Scholar 

  • Damgaard T, Plath N, Neill JC, Hansen SL (2011) Extrasynaptic GABAA receptor activation reverses recognition memory deficits in an animal model of schizophrenia. Psychopharmacology (Berl) 214:403–413

    Article  CAS  Google Scholar 

  • Danion JM, Huron C, Vidailhet P, Berna F (2007) Functional mechanisms of episodic memory impairment in schizophrenia. Can J Psychiatr 52:693–701

    Google Scholar 

  • Davis KL, Kahn RS, Ko G, Davidson M (1991) Dopamine in schizophrenia: a review and reconceptualization. Am J Psychiatry 148:1474–1486

    PubMed  CAS  Google Scholar 

  • Dawson LA, Li P (2003) Effects of 5-HT(6) receptor blockade on the neurochemical outcome of antidepressant treatment in the frontal cortex of the rat. J Neural Transm 110:577–590

    Article  PubMed  CAS  Google Scholar 

  • Dawson LA, Nguyen HQ, Li P (2000) In vivo effects of the 5-HT(6) antagonist SB-271046 on striatal and frontal cortex extracellular concentrations of noradrenaline, dopamine, 5-HT, glutamate and aspartate. Br J Pharmacol 130:23–26

    Article  PubMed  CAS  Google Scholar 

  • Dawson LA, Nguyen HQ, Li P (2001) The 5-HT(6) receptor antagonist SB-271046 selectively enhances excitatory neurotransmission in the rat frontal cortex and hippocampus. Neuropsychopharmacology 25:662–668

    Article  PubMed  CAS  Google Scholar 

  • de Bruin N, Pouzet B (2006) Beneficial effects of galantamine on performance in the object recognition task in Swiss mice: deficits induced by scopolamine and by prolonging the retention interval. Pharmacol Biochem Behav 85:253–260

    Article  PubMed  CAS  Google Scholar 

  • de Leon J, Diaz FJ (2005) A meta-analysis of worldwide studies demonstrates an association between schizophrenia and tobacco smoking behaviors. Schizophr Res 76:135–157

    Article  PubMed  Google Scholar 

  • de Lima MN, Laranja DC, Bromberg E, Roesler R, Schröder N (2005) Pre- or post-training administration of the NMDA receptor blocker MK-801 impairs object recognition memory in rats. Behav Brain Res 156:139–143

    Article  PubMed  CAS  Google Scholar 

  • Depatie L, O’Driscoll GA, Holahan AL, Atkinson V, Thavundayil JX, Kin NN, Lal S (2002) Nicotine and behavioral markers of risk for schizophrenia: a double-blind, placebo-controlled, cross-over study. Neuropsychopharmacology 27:1056–1070

    Article  PubMed  CAS  Google Scholar 

  • Dere E, Huston JP, De Souza Silva MA (2007) The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neurosci Biobehav Rev 31:673–704

    Article  PubMed  CAS  Google Scholar 

  • Devito LM, Balu DT, Kanter BR, Lykken C, Basu AC, Coyle JT, Eichenbaum H (2010) Serine racemase deletion disrupts memory for order and alters cortical dendritic morphology. Genes Brain Behav 10:210–222

    PubMed  Google Scholar 

  • Dewachter I, Ris L, Jaworski T, Seymour CM, Kremer A, Borghgraef P, De Vijver H, Godaux E, Van Leuven F (2009) GSK3β, a centre-staged kinase in neuropsychiatric disorders, modulates long term memory by inhibitory phosphorylation at serine-9. Neurobiol Dis 35:193–200

    Google Scholar 

  • Diaz-Mataix L, Scorza MC, Bortolozzi A, Toth M, Celada P, Artigas F (2005) Involvement of 5-HT1A receptors in prefrontal cortex in the modulation of dopaminergic activity: role in atypical antipsychotic action. J Neurosci 25:10831–10843

    Article  PubMed  CAS  Google Scholar 

  • Dijk SN, Francis PT, Stratmann GC, Bowen DM (1995) NMDA-induced glutamate and aspartate release from rat cortical pyramidal neurones: evidence for modulation by a 5-HT1A antagonist. Br J Pharmacol 115:1169–1174

    PubMed  CAS  Google Scholar 

  • Dixon L, Haas G, Weiden PJ, Sweeney J, Frances AJ (1991) Drug abuse in schizophrenic patients: clinical correlates and reasons for use. Am J Psychiatry 148:224–230

    PubMed  CAS  Google Scholar 

  • Doleviczenyi Z, Vizi ES, Gacsalyi I, Pallagi K, Volk B, Harsing LG Jr, Halmos G, Lendvai B, Zelles T (2008) 5-HT6/7 receptor antagonists facilitate dopamine release in the cochlea via a GABAergic disinhibitory mechanism. Neurochem Res 33:2364–2372

    Article  PubMed  CAS  Google Scholar 

  • Doniger GM, Foxe JJ, Murray MM, Higgins BA, Javitt DC (2002) Impaired visual object recognition and dorsal/ventral stream interaction in schizophrenia. Arch Gen Psychiatry 59:1011–1020

    Article  PubMed  Google Scholar 

  • Duffy L, Cappas E, Lai D, Boucher AA, Karl T (2010) Cognition in transmembrane domain neuregulin 1 mutant mice. Neuroscience 170:800–807

    Article  PubMed  CAS  Google Scholar 

  • Dyer MA, Freudenreich O, Culhane MA, Pachas GN, Deckersbach T, Murphy E, Goff DC, Evins AE (2008) High-dose galantamine augmentation inferior to placebo on attention, inhibitory control and working memory performance in nonsmokers with schizophrenia. Schizophr Res 102:88–95

    Article  PubMed  Google Scholar 

  • Eacott MJ, Easton A, Zinkivskav A (2005) Recollection in an episodic-like memory task in the rat. Learn Mem 12:221–223

    Article  PubMed  Google Scholar 

  • Ebstein RP, Novick O, Umansky R, Priel B, Osher Y, Blaine D, Bennett ER, Nemanov L, Katz M, Belmaker RH (1996) Dopamine D4 receptor (D4DR) exon III polymorphism associated with the human personality trait of Novelty Seeking. Nat Genet 12:78–80

    Article  PubMed  CAS  Google Scholar 

  • Ehrlichman RS, Luminais SN, White SL, Rudnick ND, Ma N, Dow HC, Kreibich AS, Abel T, Brodkin ES, Hahn CG, Siegel SJ (2009) Neuregulin 1 transgenic mice display reduced mismatch negativity, contextual fear conditioning and social interactions. Brain Res 1294:116–127

    Article  PubMed  CAS  Google Scholar 

  • Ennaceur A, Delacour J (1988) A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav Brain Res 31:47–59

    Article  PubMed  CAS  Google Scholar 

  • Ennaceur A, Neave N, Aggleton JP (1996) Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat. Behav Brain Res 80:9–25

    Article  PubMed  CAS  Google Scholar 

  • Ennaceur A, Neave N, Aggleton JP (1997) Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp Brain Res 113:509–519

    Article  PubMed  CAS  Google Scholar 

  • Fagerlund B, Soholm B, Fink-Jensen A, Lublin H, Glenthoj BY (2007) Effects of donepezil adjunctive treatment to ziprasidone on cognitive deficits in schizophrenia: a double-blind, placebo-controlled study. Clin Neuropharmacol 30:3–12

    Article  PubMed  CAS  Google Scholar 

  • Forwood SE, Winters BD, Bussey TJ (2005) Hippocampal lesions that abolish spatial maze performance spare object recognition memory at delays of up to 48 hours. Hippocampus 15:347–355

    Article  PubMed  CAS  Google Scholar 

  • Franberg O, Marcus MM, Ivanov V, Schilstrom B, Shahid M, Svensson TH (2009) Asenapine elevates cortical dopamine, noradrenaline and serotonin release. Evidence for activation of cortical and subcortical dopamine systems by different mechanisms. Psychopharmacology (Berl) 204:251–264

    Article  CAS  Google Scholar 

  • Freedman R, Leonard S (2001) Genetic linkage to schizophrenia at chromosome 15q14. Am J Med Genet 105:655–657

    Article  PubMed  CAS  Google Scholar 

  • Freedman R, Hall M, Adler LE, Leonard S (1995) Evidence in postmortem brain tissue for decreased numbers of hippocampal nicotinic receptors in schizophrenia. Biol Psychiatry 38:22–33

    Article  PubMed  CAS  Google Scholar 

  • Freedman R, Leonard S, Gault JM, Hopkins J, Cloninger CR, Kaufmann CA, Tsuang MT, Farone SV, Malaspina D, Svrakic DM, Sanders A, Gejman P (2001) Linkage disequilibrium for schizophrenia at the chromosome 15q13–14 locus of the alpha7-nicotinic acetylcholine receptor subunit gene (CHRNA7). Am J Med Genet 105:20–22

    Article  PubMed  CAS  Google Scholar 

  • Freedman R, Olincy A, Buchanan RW, Harris JG, Gold JM, Johnson L, Allensworth D, Guzman-Bonilla A, Clement B, Ball MP, Kutnick J, Pender V, Martin LF, Stevens KE, Wagner BD, Zerbe GO, Soti F, Kem WR (2008) Initial phase 2 trial of a nicotinic agonist in schizophrenia. Am J Psychiatry 165:1040–1047

    Article  PubMed  Google Scholar 

  • Freudenreich O, Herz L, Deckersbach T, Evins AE, Henderson DC, Cather C, Goff DC (2005) Added donepezil for stable schizophrenia: a double-blind, placebo-controlled trial. Psychopharmacology (Berl) 181:358–363

    Article  CAS  Google Scholar 

  • Friedman JI, Adler DN, Howanitz E, Harvey PD, Brenner G, Temporini H, White L, Parrella M, Davis KL (2002) A double blind placebo controlled trial of donepezil adjunctive treatment to risperidone for the cognitive impairment of schizophrenia. Biol Psychiatry 51:349–357

    Article  PubMed  CAS  Google Scholar 

  • Friston KJ, Liddle PF, Frith CD, Hirsch SR, Frackowiak RS (1992) The left medial temporal region and schizophrenia. A PET study. Brain 115(Pt 2):367–382

    Article  PubMed  Google Scholar 

  • Gaffan D (1974) Recognition impaired and association intact in the memory of monkeys after transection of the fornix. J Comp Physiol Psychol 86:1100–1109

    Article  PubMed  CAS  Google Scholar 

  • Gardiner JM (1988) Recognition failures and free-recall failures: implications for the relation between recall and recognition. Mem Cognit 16:446–451

    Article  PubMed  CAS  Google Scholar 

  • Goff DC, Herz L, Posever T, Shih V, Tsai G, Henderson DC, Freudenreich O, Evins AE, Yovel I, Zhang H, Schoenfeld D (2005) A six-month, placebo-controlled trial of D-cycloserine co-administered with conventional antipsychotics in schizophrenia patients. Psychopharmacology (Berl) 179:144–150

    Article  CAS  Google Scholar 

  • Goldman-Rakic PS (1994) Working memory dysfunction in schizophrenia. J Neuropsychiatry Clin Neurosci 6:348–357

    PubMed  CAS  Google Scholar 

  • Grayson B, Idris NF, Neill JC (2007) Atypical antipsychotics attenuate a sub-chronic PCP-induced cognitive deficit in the novel object recognition task in the rat. Behav Brain Res 184:31–38

    Article  PubMed  CAS  Google Scholar 

  • Green MF (2006) Cognitive impairment and functional outcome in schizophrenia and bipolar disorder. J Clin Psychiatr 67:e12

    Article  Google Scholar 

  • Greene R (2001) Circuit analysis of NMDAR hypofunction in the hippocampus, in vitro, and psychosis of schizophrenia. Hippocampus 11:569–577

    Article  PubMed  CAS  Google Scholar 

  • Grunze HC, Rainnie DG, Hasselmo ME, Barkai E, Hearn EF, McCarley RW, Greene RW (1996) NMDA-dependent modulation of CA1 local circuit inhibition. J Neurosci 16:2034–2043

    PubMed  CAS  Google Scholar 

  • Guo Y, Zhang H, Chen X, Cai W, Cheng J, Yang Y, Jin G, Zhen X (2009) Evaluation of the antipsychotic effect of bi-acetylated l-stepholidine (l-SPD-A), a novel dopamine and serotonin receptor dual ligand. Schizophr Res 115:41–49

    Article  PubMed  Google Scholar 

  • Hannesson DK, Vacca G, Howland JG, Phillips AG (2004) Medial prefrontal cortex is involved in spatial temporal order memory but not spatial recognition memory in tests relying on spontaneous exploration in rats. Behav Brain Res 153:273–285

    Article  PubMed  CAS  Google Scholar 

  • Harris JG, Kongs S, Allensworth D, Martin L, Tregellas J, Sullivan B, Zerbe G, Freedman R (2004) Effects of nicotine on cognitive deficits in schizophrenia. Neuropsychopharmacology 29:1378–1385

    Article  PubMed  CAS  Google Scholar 

  • Harrison PJ, Weinberger DR (2005) Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatr 10:40–68, image 5

    Article  CAS  Google Scholar 

  • Harvey PD, Moriarty PJ, Friedman JI, White L, Parrella M, Mohs RC, Davis KL (2000) Differential preservation of cognitive functions in geriatric patients with lifelong chronic schizophrenia: less impairment in reading compared with other skill areas. Biol Psychiatry 47:962–968

    Article  PubMed  CAS  Google Scholar 

  • Hashimoto K, Fujita Y, Shimizu E, Iyo M (2005) Phencyclidine-induced cognitive deficits in mice are improved by subsequent subchronic administration of clozapine, but not haloperidol. Eur J Pharmacol 519:114–117

    Article  PubMed  CAS  Google Scholar 

  • Hashimoto K, Ishima T, Fujita Y, Matsuo M, Kobashi T, Takahagi M, Tsukada H, Iyo M (2008) Phencyclidine-induced cognitive deficits in mice are improved by subsequent subchronic administration of the novel selective alpha7 nicotinic receptor agonist SSR180711. Biol Psychiatry 63:92–97

    Article  PubMed  CAS  Google Scholar 

  • Hauser TA, Kucinski A, Jordan KG, Gatto GJ, Wersinger SR, Hesse RA, Stachowiak EK, Stachowiak MK, Papke RL, Lippiello PM, Bencherif M (2009) TC-5619: an alpha7 neuronal nicotinic receptor-selective agonist that demonstrates efficacy in animal models of the positive and negative symptoms and cognitive dysfunction of schizophrenia. Biochem Pharmacol 78:803–812

    Article  PubMed  CAS  Google Scholar 

  • Haydar SN, Yun H, Andrae PM, Mattes J, Zhang J, Kramer A, Smith DL, Huselton C, Graf R, Aschmies S, Schechter LE, Comery TA, Robichaud AJ (2010) 5-Cyclic amine-3-arylsulfonylindazoles as novel 5-HT6 receptor antagonists. J Med Chem 53:2521–2527

    Article  PubMed  CAS  Google Scholar 

  • Heckers S, Rauch SL, Goff D, Savage CR, Schacter DL, Fischman AJ, Alpert NM (1998) Impaired recruitment of the hippocampus during conscious recollection in schizophrenia. Nat Neurosci 1:318–323

    Article  PubMed  CAS  Google Scholar 

  • Heckers S, Curran T, Goff D, Rauch SL, Fischman AJ, Alpert NM, Schacter DL (2000) Abnormalities in the thalamus and prefrontal cortex during episodic object recognition in schizophrenia. Biol Psychiatry 48:651–657

    Article  PubMed  CAS  Google Scholar 

  • Herring NR, Schaefer TL, Gudelsky GA, Vorhees CV, Williams MT (2008) Effect of +−methamphetamine on path integration learning, novel object recognition, and neurotoxicity in rats. Psychopharmacology (Berl) 199:637–650

    Article  CAS  Google Scholar 

  • Hersi AI, Richard JW, Gaudreau P, Quirion R (1995) Local modulation of hippocampal acetylcholine release by dopamine D1 receptors: a combined receptor autoradiography and in vivo dialysis study. J Neurosci 15:7150–7157

    PubMed  CAS  Google Scholar 

  • Higuera-Matas A, Botreau F, Miguens M, Del Olmo N, Borcel E, Perez-Alvarez L, Garcia-Lecumberri C, Ambrosio E (2009) Chronic periadolescent cannabinoid treatment enhances adult hippocampal PSA-NCAM expression in male Wistar rats but only has marginal effects on anxiety, learning and memory. Pharmacol Biochem Behav 93:482–490

    Article  PubMed  CAS  Google Scholar 

  • Hirst WD, Stean TO, Rogers DC, Sunter D, Pugh P, Moss SF, Bromidge SM, Riley G, Smith DR, Bartlett S, Heidbreder CA, Atkins AR, Lacroix LP, Dawson LA, Foley AG, Regan CM, Upton N (2006) SB-399885 is a potent, selective 5-HT6 receptor antagonist with cognitive enhancing properties in aged rat water maze and novel object recognition models. Eur J Pharmacol 553:109–119

    Article  PubMed  CAS  Google Scholar 

  • Hirst WD, Andree TH, Aschmies S, Childers WE, Comery TA, Dawson LA, Day M, Feingold IB, Grauer SM, Harrison BL, Hughes ZA, Kao J, Kelly MG, van der Lee H, Rosenzweig-Lipson S, Saab AL, Smith DL, Sullivan K, Rizzo SJ, Tio C, Zhang MY, Schechter LE (2008) Correlating efficacy in rodent cognition models with in vivo 5-hydroxytryptamine1a receptor occupancy by a novel antagonist, (R)-N-(2-methyl-(4-indolyl-1-piperazinyl)ethyl)-N-(2-pyridinyl)-cyclohexan e carboxamide (WAY-101405). J Pharmacol Exp Ther 325:134–145

    Article  PubMed  CAS  Google Scholar 

  • Hong LE, Schroeder M, Ross TJ, Buchholz B, Salmeron BJ, Wonodi I, Thaker GK, Stein EA (2011) Nicotine enhances but does not normalize visual sustained attention and the associated brain network in schizophrenia. Schizophr Bull 37:416–425

    Article  PubMed  Google Scholar 

  • Hori SE, Powell KJ, Robertson GS (2007) Darbepoetin alfa (Aranesp) improves recognition memory in adult rats that have sustained bilateral ventral hippocampal lesions as neonates or young adults. Neuroscience 144:1–7

    Article  PubMed  CAS  Google Scholar 

  • Hu JH, Ma YH, Jiang J, Yang N, Duan SH, Jiang ZH, Mei ZT, Fei J, Guo LH (2004) Cognitive impairment in mice over-expressing gamma-aminobutyric acid transporter 1 (GAT1). Neuroreport 15:9–12

    Article  PubMed  Google Scholar 

  • Huang M, Li Z, Dai J, Shahid M, Wong EH, Meltzer HY (2008) Asenapine increases dopamine, norepinephrine, and acetylcholine efflux in the rat medial prefrontal cortex and hippocampus. Neuropsychopharmacology 33:2934–2945

    Article  PubMed  CAS  Google Scholar 

  • Hultman CM, Sparen P, Takei N, Murray RM, Cnattingius S (1999) Prenatal and perinatal risk factors for schizophrenia, affective psychosis, and reactive psychosis of early onset: case–control study. BMJ 318:421–426

    Article  PubMed  CAS  Google Scholar 

  • Ibi D, Nagai T, Koike H, Kitahara Y, Mizoguchi H, Niwa M, Jaaro-Peled H, Nitta A, Yoneda Y, Nabeshima T, Sawa A, Yamada K (2010) Combined effect of neonatal immune activation and mutant DISC1 on phenotypic changes in adulthood. Behav Brain Res 206:32–37

    Article  PubMed  CAS  Google Scholar 

  • Ichikawa J, Li Z, Dai J, Meltzer HY (2002) Atypical antipsychotic drugs, quetiapine, iloperidone, and melperone, preferentially increase dopamine and acetylcholine release in rat medial prefrontal cortex: role of 5-HT1A receptor agonism. Brain Res 956:349–357

    Article  PubMed  CAS  Google Scholar 

  • Ito HT, Smith SE, Hsiao E, Patterson PH (2010) Maternal immune activation alters nonspatial information processing in the hippocampus of the adult offspring. Brain Behav Immun 24:930–941

    Article  PubMed  Google Scholar 

  • Jackson ME, Homayoun H, Moghaddam B (2004) NMDA receptor hypofunction produces concomitant firing rate potentiation and burst activity reduction in the prefrontal cortex. Proc Natl Acad Sci USA 101:8467–8472

    Article  PubMed  CAS  Google Scholar 

  • Javitt DC (2009) Sensory processing in schizophrenia: neither simple nor intact. Schizophr Bull 35:1059–1064

    Article  PubMed  Google Scholar 

  • Jenkins TA, Harte MK, Stenson G, Reynolds GP (2009) Neonatal lipopolysaccharide induces pathological changes in parvalbumin immunoreactivity in the hippocampus of the rat. Behav Brain Res 205:355–359

    Article  PubMed  CAS  Google Scholar 

  • Johnson DJ, Forbes IT, Watson SP, Garzya V, Stevenson GI, Walker GR, Mudhar HS, Flynn ST, Wyman PA, Smith PW, Murkitt GS, Lucas AJ, Mookherjee CR, Watson JM, Gartlon JE, Bradford AM, Brown F (2010) The discovery of a series of N-substituted 3-(4-piperidinyl)-1,3-benzoxazolinones and oxindoles as highly brain penetrant, selective muscarinic M1 agonists. Bioorg Med Chem Lett 20:5434–5438

    Article  PubMed  CAS  Google Scholar 

  • Jones DN, Higgins GA (1995) Effect of scopolamine on visual attention in rats. Psychopharmacology (Berl) 120:142–149

    Article  CAS  Google Scholar 

  • Jones CA, Brown AM, Auer DP, Fone KC (2010) The mGluR2/3 agonist LY379268 reverses post-weaning social isolation-induced recognition memory deficits in the rat. Psychopharmacology (Berl) 214:269–283

    Article  CAS  Google Scholar 

  • Kalechstein AD, Newton TF, Green M (2003) Methamphetamine dependence is associated with neurocognitive impairment in the initial phases of abstinence. J Neuropsychiatry Clin Neurosci 15:215–220

    Article  PubMed  CAS  Google Scholar 

  • Kamei H, Nagai T, Nakano H, Togan Y, Takayanagi M, Takahashi K, Kobayashi K, Yoshida S, Maeda K, Takuma K, Nabeshima T, Yamada K (2006) Repeated methamphetamine treatment impairs recognition memory through a failure of novelty-induced ERK1/2 activation in the prefrontal cortex of mice. Biol Psychiatry 59:75–84

    Article  PubMed  CAS  Google Scholar 

  • Kapur S, Remington G (2001) Dopamine D(2) receptors and their role in atypical antipsychotic action: still necessary and may even be sufficient. Biol Psychiatry 50:873–883

    Article  PubMed  CAS  Google Scholar 

  • Karasawa J, Hashimoto K, Chaki S (2008) D-Serine and a glycine transporter inhibitor improve MK-801-induced cognitive deficits in a novel object recognition test in rats. Behav Brain Res 186:78–83

    Article  PubMed  CAS  Google Scholar 

  • Keefe RS, Bilder RM, Davis SM, Harvey PD, Palmer BW, Gold JM, Meltzer HY, Green MF, Capuano G, Stroup TS, McEvoy JP, Swartz MS, Rosenheck RA, Perkins DO, Davis CE, Hsiao JK, Lieberman JA (2007) Neurocognitive effects of antipsychotic medications in patients with chronic schizophrenia in the CATIE Trial. Arch Gen Psychiatry 64:633–647

    Article  PubMed  CAS  Google Scholar 

  • Keefe RS, Malhotra AK, Meltzer HY, Kane JM, Buchanan RW, Murthy A, Sovel M, Li C, Goldman R (2008) Efficacy and safety of donepezil in patients with schizophrenia or schizoaffective disorder: significant placebo/practice effects in a 12-week, randomized, double-blind, placebo-controlled trial. Neuropsychopharmacology 33:1217–1228

    Article  PubMed  CAS  Google Scholar 

  • Kendall I, Slotten HA, Codony X, Burgueno J, Pauwels PJ, Vela JM, Fone KC (2011) E-6801, a 5-HT6 receptor agonist, improves recognition memory by combined modulation of cholinergic and glutamatergic neurotransmission in the rat. Psychopharmacology (Berl) 213:413–430

    Article  CAS  Google Scholar 

  • King MV, Sleight AJ, Woolley ML, Topham IA, Marsden CA, Fone KC (2004) 5-HT6 receptor antagonists reverse delay-dependent deficits in novel object discrimination by enhancing consolidation--an effect sensitive to NMDA receptor antagonism. Neuropharmacology 47:195–204

    Google Scholar 

  • King MV, Spicer CH, Sleight AJ, Marsden CA, Fone KC (2009) Impact of regional 5-HT depletion on the cognitive enhancing effects of a typical 5-ht(6) receptor antagonist, Ro 04–6790, in the Novel Object Discrimination task. Psychopharmacology (Berl) 202:111–123

    Article  CAS  Google Scholar 

  • Krivoy A, Weizman A, Laor L, Hellinger N, Zemishlany Z, Fischel T (2008) Addition of memantine to antipsychotic treatment in schizophrenia inpatients with residual symptoms: a preliminary study. Eur Neuropsychopharmacol 18:117–121

    Article  PubMed  CAS  Google Scholar 

  • Krystal JH, Karper LP, Seibyl JP, Freeman GK, Delaney R, Bremner JD, Heninger GR, Bowers MB, Charney DS (1994) Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Arch Gen Psychiatry 51:199–214

    Article  PubMed  CAS  Google Scholar 

  • Krystal JH, D’Souza DC, Madonick S, Petrakis IL (1999) Toward a rational pharmacotherapy of comorbid substance abuse in schizophrenic patients. Schizophr Res 35(Suppl):S35–S49

    Article  PubMed  Google Scholar 

  • Kunitachi S, Fujita Y, Ishima T, Kohno M, Horio M, Tanibuchi Y, Shirayama Y, Iyo M, Hashimoto K (2009) Phencyclidine-induced cognitive deficits in mice are ameliorated by subsequent subchronic administration of donepezil: role of sigma-1 receptors. Brain Res 1279:189–196

    Article  PubMed  CAS  Google Scholar 

  • Lahti AC, Koffel B, LaPorte D, Tamminga CA (1995) Subanesthetic doses of ketamine stimulate psychosis in schizophrenia. Neuropsychopharmacology 13:9–19

    Article  PubMed  CAS  Google Scholar 

  • Lane HY, Huang CL, Wu PL, Liu YC, Chang YC, Lin PY, Chen PW, Tsai G (2006) Glycine transporter I inhibitor, N-methylglycine (sarcosine), added to clozapine for the treatment of schizophrenia. Biol Psychiatry 60:645–649

    Article  PubMed  CAS  Google Scholar 

  • Lane HY, Lin CH, Huang YJ, Liao CH, Chang YC, Tsai GE (2010) A randomized, double-blind, placebo-controlled comparison study of sarcosine (N-methylglycine) and D-serine add-on treatment for schizophrenia. Int J Neuropsychopharmacol 13:451–460

    Article  PubMed  CAS  Google Scholar 

  • Lee SW, Lee JG, Lee BJ, Kim YH (2007) A 12-week, double-blind, placebo-controlled trial of galantamine adjunctive treatment to conventional antipsychotics for the cognitive impairments in chronic schizophrenia. Int Clin Psychopharmacol 22:63–68

    Article  PubMed  CAS  Google Scholar 

  • Leonard S, Gault J, Moore T, Hopkins J, Robinson M, Olincy A, Adler LE, Cloninger CR, Kaufmann CA, Tsuang MT, Faraone SV, Malaspina D, Svrakic DM, Freedman R (1998) Further investigation of a chromosome 15 locus in schizophrenia: analysis of affected sibpairs from the NIMH Genetics Initiative. Am J Med Genet 81:308–312

    Article  PubMed  CAS  Google Scholar 

  • Levin ED, Rezvani AH (2006) Nicotinic-antipsychotic drug interactions and cognitive function. EXS 98:185–205

    PubMed  CAS  Google Scholar 

  • Levin ED, Rose JE (1995) Acute and chronic nicotinic interactions with dopamine systems and working memory performance. Ann N Y Acad Sci 757:245–252

    Article  PubMed  CAS  Google Scholar 

  • Levin ED, Simon BB (1998) Nicotinic acetylcholine involvement in cognitive function in animals. Psychopharmacology (Berl) 138:217–230

    Article  CAS  Google Scholar 

  • Levin ED, Wilson W, Rose JE, McEvoy J (1996) Nicotine–haloperidol interactions and cognitive performance in schizophrenics. Neuropsychopharmacology 15:429–436

    Article  PubMed  CAS  Google Scholar 

  • Levine S, Berkenbosch F, Suchecki D, Tilders FJ (1994) Pituitary–adrenal and interleukin-6 responses to recombinant interleukin-1 in neonatal rats. Psychoneuroendocrinology 19:143–153

    Article  PubMed  CAS  Google Scholar 

  • Lewis DA, Hashimoto T, Volk DW (2005) Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6:312–324

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Snigdha S, Roseman AS, Dai J, Meltzer HY (2008) Effect of muscarinic receptor agonists xanomeline and sabcomeline on acetylcholine and dopamine efflux in the rat brain; comparison with effects of 4-[3-(4-butylpiperidin-1-yl)-propyl]-7-fluoro-4H-benzo[1,4]oxazin-3-one (AC260584) and N-desmethylclozapine. Eur J Pharmacol 596:89–97

    Article  PubMed  CAS  Google Scholar 

  • Lieben CK, Blokland A, Sik A, Sung E, van Nieuwenhuizen P, Schreiber R (2005) The selective 5-HT6 receptor antagonist Ro4368554 restores memory performance in cholinergic and serotonergic models of memory deficiency in the rat. Neuropsychopharmacology 30:2169–2179

    Article  PubMed  CAS  Google Scholar 

  • Lieberman JA, Papadakis K, Csernansky J, Litman R, Volavka J, Jia XD, Gage A (2009) A randomized, placebo-controlled study of memantine as adjunctive treatment in patients with schizophrenia. Neuropsychopharmacology 34:1322–1329

    Article  PubMed  CAS  Google Scholar 

  • Lipska BK, Jaskiw GE, Weinberger DR (1993) Postpubertal emergence of hyperresponsiveness to stress and to amphetamine after neonatal excitotoxic hippocampal damage: a potential animal model of schizophrenia. Neuropsychopharmacology 9:67–75

    PubMed  CAS  Google Scholar 

  • Lipska BK, Aultman JM, Verma A, Weinberger DR, Moghaddam B (2002) Neonatal damage of the ventral hippocampus impairs working memory in the rat. Neuropsychopharmacology 27:47–54

    Article  PubMed  Google Scholar 

  • Liu F, Grauer S, Kelley C, Navarra R, Graf R, Zhang G, Atkinson PJ, Popiolek M, Wantuch C, Khawaja X, Smith D, Olsen M, Kouranova E, Lai M, Pruthi F, Pulicicchio C, Day M, Gilbert A, Pausch MH, Brandon NJ, Beyer CE, Comery TA, Logue S, Rosenzweig-Lipson S, Marquis KL (2008) ADX47273 [S-(4-fluoro-phenyl)-{3-[3-(4-fluoro-phenyl)-[1,2,4]-oxadiazol-5-yl]-piperidin-1-yl}-methanone]: a novel metabotropic glutamate receptor 5-selective positive allosteric modulator with preclinical antipsychotic-like and procognitive activities. J Pharmacol Exp Ther 327:827–839

    Article  PubMed  CAS  Google Scholar 

  • Long LE, Chesworth R, Arnold JC, Karl T (2010) A follow-up study: acute behavioural effects of Delta(9)-THC in female heterozygous neuregulin 1 transmembrane domain mutant mice. Psychopharmacology (Berl) 211:277–289

    Article  CAS  Google Scholar 

  • Lung FW, Shu BC, Kao WT, Chen CN, Ku YC, Tzeng DS (2009) Association of DRD4 uVNTR and TP53 codon 72 polymorphisms with schizophrenia: a case–control study. BMC Med Genet 10:147

    Article  PubMed  CAS  Google Scholar 

  • MacEwan GW, Ehmann TS, Khanbhai I, Wrixon C (2001) Donepezil in schizophrenia—is it helpful? An experimental design case study. Acta Psychiatr Scand 104:469–472

    Article  PubMed  CAS  Google Scholar 

  • Macor JE, Gurley D, Lanthorn T, Loch J, Mack RA, Mullen G, Tran O, Wright N, Gordon JC (2001) The 5-HT3 antagonist tropisetron (ICS 205–930) is a potent and selective alpha7 nicotinic receptor partial agonist. Bioorg Med Chem Lett 11:319–321

    Article  PubMed  CAS  Google Scholar 

  • Maia L, de Mendonca A (2002) Does caffeine intake protect from Alzheimer’s disease? Eur J Neurol 9:377–382

    Article  PubMed  CAS  Google Scholar 

  • Malaspina D, Harkavy-Friedman J, Corcoran C, Mujica-Parodi L, Printz D, Gorman JM, Van Heertum R (2004) Resting neural activity distinguishes subgroups of schizophrenia patients. Biol Psychiatry 56:931–937

    Article  PubMed  Google Scholar 

  • Manns JR, Stark CE, Squire LR (2000) The visual paired-comparison task as a measure of declarative memory. Proc Natl Acad Sci USA 97:12375–12379

    Article  PubMed  CAS  Google Scholar 

  • Marcos B, Gil-Bea FJ, Hirst WD, Garcia-Alloza M, Ramirez MJ (2006) Lack of localization of 5-HT6 receptors on cholinergic neurons: implication of multiple neurotransmitter systems in 5-HT6 receptor-mediated acetylcholine release. Eur J Neurosci 24:1299–1306

    Article  PubMed  Google Scholar 

  • Marutle A, Zhang X, Court J, Piggott M, Johnson M, Perry R, Perry E, Nordberg A (2001) Laminar distribution of nicotinic receptor subtypes in cortical regions in schizophrenia. J Chem Neuroanat 22:115–126

    Article  PubMed  CAS  Google Scholar 

  • Massey PV, Bhabra G, Cho K, Brown MW, Bashir ZI (2001) Activation of muscarinic receptors induces protein synthesis-dependent long-lasting depression in the perirhinal cortex. Eur J Neurosci 14:145–152

    Article  PubMed  CAS  Google Scholar 

  • Mattay VS, Goldberg TE, Fera F, Hariri AR, Tessitore A, Egan MF, Kolachana B, Callicott JH, Weinberger DR (2003) Catechol O-methyltransferase val158-met genotype and individual variation in the brain response to amphetamine. Proc Natl Acad Sci USA 100:6186–6191

    Article  PubMed  CAS  Google Scholar 

  • McCreary AC, Glennon JC, Ashby CR Jr, Meltzer HY, Li Z, Reinders JH, Hesselink MB, Long SK, Herremans AH, van Stuivenberg H, Feenstra RW, Kruse CG (2007) SLV313 (1-(2,3-dihydro-benzo[1,4]dioxin-5-yl)-4- [5-(4-fluoro-phenyl)-pyridin-3-ylmethyl]-piperazine monohydrochloride): a novel dopamine D2 receptor antagonist and 5-HT1A receptor agonist potential antipsychotic drug. Neuropsychopharmacology 32:78–94

    Article  PubMed  CAS  Google Scholar 

  • McKee RD, Squire LR (1993) On the development of declarative memory. J Exp Psychol Learn Mem Cogn 19:397–404

    Article  PubMed  CAS  Google Scholar 

  • McKibben CE, Jenkins TA, Adams HN, Harte MK, Reynolds GP (2010) Effect of pretreatment with risperidone on phencyclidine-induced disruptions in object recognition memory and prefrontal cortex parvalbumin immunoreactivity in the rat. Behav Brain Res 208:132–136

    Article  PubMed  CAS  Google Scholar 

  • McLean SL, Woolley ML, Thomas D, Neill JC (2009) Role of 5-HT receptor mechanisms in sub-chronic PCP-induced reversal learning deficits in the rat. Psychopharmacology (Berl) 206:403–414

    Article  CAS  Google Scholar 

  • McLean SL, Grayson B, Idris NF, Lesage AS, Pemberton DJ, Mackie C, Neill JC (2011) Activation of alpha7 nicotinic receptors improves phencyclidine-induced deficits in cognitive tasks in rats: implications for therapy of cognitive dysfunction in schizophrenia. Eur Neuropsychopharmacol 21:333–343

    Article  PubMed  CAS  Google Scholar 

  • Messier C (1997) Object recognition in mice: improvement of memory by glucose. Neurobiol Learn Mem 67:172–175

    Article  PubMed  CAS  Google Scholar 

  • Meyer U, Feldon J (2010) Epidemiology-driven neurodevelopmental animal models of schizophrenia. Prog Neurobiol 90:285–326

    Article  PubMed  Google Scholar 

  • Millan MJ, Mannoury la Cour C, Novi F, Maggio R, Audinot V, Newman-Tancredi A, Cussac D, Pasteau V, Boutin JA, Dubuffet T, Lavielle G (2008) S33138 [N-[4-[2-[(3aS,9bR)-8-cyano-1,3a,4,9b-tetrahydro[1]-benzopyrano[3,4-c]pyrr ol-2(3H)-yl)-ethyl]phenylacetamide], a preferential dopamine D3 versus D2 receptor antagonist and potential antipsychotic agent: I. Receptor-binding profile and functional actions at G-protein-coupled receptors. J Pharmacol Exp Ther 324:587–599

    Article  PubMed  CAS  Google Scholar 

  • Millan MJ, Buccafusco JJ, Loiseau F, Watson DJ, Decamp E, Fone KC, Thomasson-Perret N, Hill M, Mocaer E, Schneider JS (2010) The dopamine D(3) receptor antagonist, S33138, counters cognitive impairment in a range of rodent and primate procedures. Int J Neuropsychopharmacol 13:1035–1051

    Article  PubMed  CAS  Google Scholar 

  • Minzenberg MJ, Poole JH, Benton C, Vinogradov S (2004) Association of anticholinergic load with impairment of complex attention and memory in schizophrenia. Am J Psychiatry 161:116–124

    Article  PubMed  Google Scholar 

  • Mishkin M, Delacour J (1975) An analysis of short-term visual memory in the monkey. J Exp Psychol Anim Behav Process 1:326–334

    Article  PubMed  CAS  Google Scholar 

  • Mitchell JB, Laiacona J (1998) The medial frontal cortex and temporal memory: tests using spontaneous exploratory behaviour in the rat. Behav Brain Res 97:107–113

    Article  PubMed  CAS  Google Scholar 

  • Mitchell ES, Neumaier JF (2005) 5-HT6 receptors: a novel target for cognitive enhancement. Pharmacol Ther 108:320–333

    Article  PubMed  CAS  Google Scholar 

  • Moghaddam B, Adams BW (1998) Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats. Science 281:1349–1352

    Article  PubMed  CAS  Google Scholar 

  • Moore TH, Zammit S, Lingford-Hughes A, Barnes TR, Jones PB, Burke M, Lewis G (2007) Cannabis use and risk of psychotic or affective mental health outcomes: a systematic review. Lancet 370:319–328

    Article  PubMed  Google Scholar 

  • Morales P, Simola N, Bustamante D, Lisboa F, Fiedler J, Gebicke-Haerter PJ, Morelli M, Tasker RA, Herrera-Marschitz M (2010) Nicotinamide prevents the long-term effects of perinatal asphyxia on apoptosis, non-spatial working memory and anxiety in rats. Exp Brain Res 202:1–14

    Article  PubMed  CAS  Google Scholar 

  • Mumby DG, Pinel JP, Wood ER (1990) Nonrecurring-items nonmatching-to-sample in rats: a new paradigm for testing non-spatial working memory. Psychobiology 18:321–326

    Google Scholar 

  • Myers CS, Robles O, Kakoyannis AN, Sherr JD, Avila MT, Blaxton TA, Thaker GK (2004) Nicotine improves delayed recognition in schizophrenic patients. Psychopharmacology (Berl) 174:334–340

    Article  CAS  Google Scholar 

  • Nagai T, Takuma K, Dohniwa M, Ibi D, Mizoguchi H, Kamei H, Nabeshima T, Yamada K (2007) Repeated methamphetamine treatment impairs spatial working memory in rats: reversal by clozapine but not haloperidol. Psychopharmacology (Berl) 194:21–32

    Article  CAS  Google Scholar 

  • Nagai T, Murai R, Matsui K, Kamei H, Noda Y, Furukawa H, Nabeshima T (2009) Aripiprazole ameliorates phencyclidine-induced impairment of recognition memory through dopamine D1 and serotonin 5-HT1A receptors. Psychopharmacology (Berl) 202:315–328

    Article  CAS  Google Scholar 

  • Nemanic S, Alvarado MC, Bachevalier J (2004) The hippocampal/parahippocampal regions and recognition memory: insights from visual paired comparison versus object-delayed nonmatching in monkeys. J Neurosci 24:2013–2026

    Article  PubMed  CAS  Google Scholar 

  • Nilsson M, Hansson S, Carlsson A, Carlsson ML (2007) Differential effects of the N-methyl-d-aspartate receptor antagonist MK-801 on different stages of object recognition memory in mice. Neuroscience 149:123–130

    Article  PubMed  CAS  Google Scholar 

  • Niwa M, Matsumoto Y, Mouri A, Ozaki N, Nabeshima T (2011) Vulnerability in early life to changes in the rearing environment plays a crucial role in the aetiopathology of psychiatric disorders. Int J Neuropsychopharmacol 14:459–477

    Article  PubMed  Google Scholar 

  • Noda Y, Mouri A, Ando Y, Waki Y, Yamada SN, Yoshimi A, Yamada K, Ozaki N, Wang D, Nabeshima T (2010) Galantamine ameliorates the impairment of recognition memory in mice repeatedly treated with methamphetamine: involvement of allosteric potentiation of nicotinic acetylcholine receptors and dopaminergic-ERK1/2 systems. Int J Neuropsychopharmacol 13:1343–1354

    Article  PubMed  CAS  Google Scholar 

  • Olincy A, Harris JG, Johnson LL, Pender V, Kongs S, Allensworth D, Ellis J, Zerbe GO, Leonard S, Stevens KE, Stevens JO, Martin L, Adler LE, Soti F, Kem WR, Freedman R (2006) Proof-of-concept trial of an alpha7 nicotinic agonist in schizophrenia. Arch Gen Psychiatry 63:630–638

    Article  PubMed  CAS  Google Scholar 

  • O’Tuathaigh CM, O’Sullivan GJ, Kinsella A, Harvey RP, Tighe O, Croke DT, Waddington JL (2006) Sexually dimorphic changes in the exploratory and habituation profiles of heterozygous neuregulin-1 knockout mice. Neuroreport 17:79–83

    Article  PubMed  Google Scholar 

  • O’Tuathaigh CM, Hryniewiecka M, Behan A, Tighe O, Coughlan C, Desbonnet L, Cannon M, Karayiorgou M, Gogos JA, Cotter DR, Waddington JL (2010) Chronic adolescent exposure to Delta-9-tetrahydrocannabinol in COMT mutant mice: impact on psychosis-related and other phenotypes. Neuropsychopharmacology 35:2262–2273

    Article  PubMed  CAS  Google Scholar 

  • Overman WH, Bachevalier J, Sewell F, Drew J (1993) A comparison of children’s performance on two recognition memory tasks: delayed nonmatch-to-sample versus visual paired-comparison. Dev Psychobiol 26:345–357

    Article  PubMed  CAS  Google Scholar 

  • Owens DG, Johnstone EC (2006) Precursors and prodromata of schizophrenia: findings from the Edinburgh High Risk Study and their literature context. Psychol Med 36:1501–1514

    Google Scholar 

  • Ozawa K, Hashimoto K, Kishimoto T, Shimizu E, Ishikura H, Iyo M (2006) Immune activation during pregnancy in mice leads to dopaminergic hyperfunction and cognitive impairment in the offspring: a neurodevelopmental animal model of schizophrenia. Biol Psychiatry 59:546–554

    Article  PubMed  CAS  Google Scholar 

  • Papaleo F, Crawley JN, Song J, Lipska BK, Pickel J, Weinberger DR, Chen J (2008) Genetic dissection of the role of catechol-O-methyltransferase in cognition and stress reactivity in mice. J Neurosci 28:8709–8723

    Article  PubMed  CAS  Google Scholar 

  • Pascalis O, Hunkin NM, Holdstock JS, Isaac CL, Mayes AR (2004) Visual paired comparison performance is impaired in a patient with selective hippocampal lesions and relatively intact item recognition. Neuropsychologia 42:1293–1300

    Article  PubMed  CAS  Google Scholar 

  • Patil ST, Zhang L, Martenyi F, Lowe SL, Jackson KA, Andreev BV, Avedisova AS, Bardenstein LM, Gurovich IY, Morozova MA, Mosolov SN, Neznanov NG, Reznik AM, Smulevich AB, Tochilov VA, Johnson BG, Monn JA, Schoepp DD (2007) Activation of mGlu2/3 receptors as a new approach to treat schizophrenia: a randomized phase 2 clinical trial. Nat Med 13:1102–1107

    Article  PubMed  CAS  Google Scholar 

  • Pelletier M, Achim AM, Montoya A, Lal S, Lepage M (2005) Cognitive and clinical moderators of recognition memory in schizophrenia: a meta-analysis. Schizophr Res 74:233–252

    Article  PubMed  Google Scholar 

  • Pereira LO, Strapasson AC, Nabinger PM, Achaval M, Netto CA (2008) Early enriched housing results in partial recovery of memory deficits in female, but not in male, rats after neonatal hypoxia–ischemia. Brain Res 1218:257–266

    Article  PubMed  CAS  Google Scholar 

  • Pichat P, Bergis OE, Terranova JP, Urani A, Duarte C, Santucci V, Gueudet C, Voltz C, Steinberg R, Stemmelin J, Oury-Donat F, Avenet P, Griebel G, Scatton B (2007) SSR180711, a novel selective alpha7 nicotinic receptor partial agonist: (II) efficacy in experimental models predictive of activity against cognitive symptoms of schizophrenia. Neuropsychopharmacology 32:17–34

    Article  PubMed  CAS  Google Scholar 

  • Pietá Dias C, Martins de Lima MN, Presti-Torres J, Dornelles A, Garcia VA, Siciliani Scalco F, Rewsaat Guimarães M, Constantino L, Budni P, Dal-Pizzol F, Schröder N (2007) Memantine reduces oxidative damage and enhances long-term recognition memory in aged rats. Neuroscience 146:1719–1725

    Article  PubMed  CAS  Google Scholar 

  • Pitsikas N, Rigamonti AE, Cella SG, Muller EE (2003) The 5-HT 1A receptor antagonist WAY 100635 improves rats performance in different models of amnesia evaluated by the object recognition task. Brain Res 983:215–222

    Article  PubMed  CAS  Google Scholar 

  • Prast H, Philippu A (2001) Nitric oxide as modulator of neuronal function. Prog Neurobiol 64:51–68

    Article  PubMed  CAS  Google Scholar 

  • Puma C, Bizot JC (1998) Intraseptal infusions of a low dose of AP5, a NMDA receptor antagonist, improves memory in an object recognition task in rats. Neurosci Lett 248:183–186

    Article  PubMed  CAS  Google Scholar 

  • Quinn HR, Matsumoto I, Callaghan PD, Long LE, Arnold JC, Gunasekaran N, Thompson MR, Dawson B, Mallet PE, Kashem MA, Matsuda-Matsumoto H, Iwazaki T, McGregor IS (2008) Adolescent rats find repeated Delta(9)-THC less aversive than adult rats but display greater residual cognitive deficits and changes in hippocampal protein expression following exposure. Neuropsychopharmacology 33:1113–1126

    Article  PubMed  Google Scholar 

  • Radcliffe KA, Dani JA (1998) Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J Neurosci 18:7075–7083

    PubMed  CAS  Google Scholar 

  • Radyushkin K, El-Kordi A, Boretius S, Castaneda S, Ronnenberg A, Reim K, Bickeböller H, Frahm J, Brose N, Ehrenreich H (2010) Complexin2 null mutation requires a ‘second hit’ for induction of phenotypic changes relevant to schizophrenia. Genes Brain Behav 9:592–602

    Google Scholar 

  • Raedler TJ, Bymaster FP, Tandon R, Copolov D, Dean B (2007) Towards a muscarinic hypothesis of schizophrenia. Mol Psychiatr 12:232–246

    CAS  Google Scholar 

  • Rammsayer TH (2001) Effects of pharmacologically induced changes in NMDA-receptor activity on long-term memory in humans. Learn Mem 8:20–25

    Article  PubMed  CAS  Google Scholar 

  • Rasmusson DD (2000) The role of acetylcholine in cortical synaptic plasticity. Behav Brain Res 115:205–218

    Article  PubMed  CAS  Google Scholar 

  • Reichel CM, Schwendt M, McGinty JF, Foster Olive M, See RE (2011) Loss of object recognition memory produced by extended access to methamphetamine self-administration is reversed by positive allosteric modulation of metabotropic glutamate receptor 5. Neuropsychopharmacology 36:782–792

    Article  PubMed  CAS  Google Scholar 

  • Riedel W, Hogervorst E, Leboux R, Verhey F, van Praag H, Jolles J (1995) Caffeine attenuates scopolamine-induced memory impairment in humans. Psychopharmacology (Berl) 122:158–168

    Article  CAS  Google Scholar 

  • Riemer C, Borroni E, Levet-Trafit B, Martin JR, Poli S, Porter RH, Bos M (2003) Influence of the 5-HT6 receptor on acetylcholine release in the cortex: pharmacological characterization of 4-(2-bromo-6-pyrrolidin-1-ylpyridine-4-sulfonyl)phenylamine, a potent and selective 5-HT6 receptor antagonist. J Med Chem 46:1273–1276

    Article  PubMed  CAS  Google Scholar 

  • Riley BP, Makoff A, Mogudi-Carter M, Jenkins T, Williamson R, Collier D, Murray R (2000) Haplotype transmission disequilibrium and evidence for linkage of the CHRNA7 gene region to schizophrenia in Southern African Bantu families. Am J Med Genet 96:196–201

    Article  PubMed  CAS  Google Scholar 

  • Risch SC, McGurk S, Horner MD, Nahas Z, Owens SD, Molloy M, Gilliard C, Christie S, Markowitz JS, DeVane CL, Mintzer J, George MS (2001) A double-blind placebo-controlled case study of the use of donepezil to improve cognition in a schizoaffective disorder patient: functional MRI correlates. Neurocase 7:105–110

    Article  PubMed  CAS  Google Scholar 

  • Ritchie K, Carriere I, de Mendonca A, Portet F, Dartigues JF, Rouaud O, Barberger-Gateau P, Ancelin ML (2007) The neuroprotective effects of caffeine: a prospective population study (the Three City Study). Neurology 69:536–545

    Article  PubMed  CAS  Google Scholar 

  • Robbins TW (2005) Synthesizing schizophrenia: a bottom-up, symptomatic approach. Schizophr Bull 31:854–864

    Article  PubMed  Google Scholar 

  • Rollema H, Lu Y, Schmidt AW, Zorn SH (1997) Clozapine increases dopamine release in prefrontal cortex by 5-HT1A receptor activation. Eur J Pharmacol 338:R3–R5

    Article  PubMed  CAS  Google Scholar 

  • Roncarati R, Scali C, Comery TA, Grauer SM, Aschmi S, Bothmann H, Jow B, Kowal D, Gianfriddo M, Kelley C, Zanelli U, Ghiron C, Haydar S, Dunlop J, Terstappen GC (2009) Procognitive and neuroprotective activity of a novel alpha7 nicotinic acetylcholine receptor agonist for treatment of neurodegenerative and cognitive disorders. J Pharmacol Exp Ther 329:459–468

    Article  PubMed  CAS  Google Scholar 

  • Rothblat LA, Hayes LL (1987) Short-term object recognition memory in the rat: nonmatching with trial-unique junk stimuli. Behav Neurosci 101:587–590

    Article  PubMed  CAS  Google Scholar 

  • Sambeth A, Riedel WJ, Smits LT, Blokland A (2007) Cholinergic drugs affect novel object recognition in rats: relation with hippocampal EEG? Eur J Pharmacol 572:151–159

    Article  PubMed  CAS  Google Scholar 

  • Sams-Dodd F, Lipska BK, Weinberger DR (1997) Neonatal lesions of the rat ventral hippocampus result in hyperlocomotion and deficits in social behaviour in adulthood. Psychopharmacology (Berl) 132:303–310

    Article  CAS  Google Scholar 

  • Sarter M, Bruno JP (1997) Trans-synaptic stimulation of cortical acetylcholine and enhancement of attentional functions: a rational approach for the development of cognition enhancers. Behav Brain Res 83:7–14

    Article  PubMed  CAS  Google Scholar 

  • Schiapparelli L, Simon AM, Del Rio J, Frechilla D (2006) Opposing effects of AMPA and 5-HT1A receptor blockade on passive avoidance and object recognition performance: correlation with AMPA receptor subunit expression in rat hippocampus. Neuropharmacology 50:897–907

    Article  PubMed  CAS  Google Scholar 

  • Schneider M, Koch M (2003) Chronic pubertal, but not adult chronic cannabinoid treatment impairs sensorimotor gating, recognition memory, and the performance in a progressive ratio task in adult rats. Neuropsychopharmacology 28:1760–1769

    Article  PubMed  CAS  Google Scholar 

  • Schreiber R, Vivian J, Hedley L, Szczepanski K, Secchi RL, Zuzow M, van Laarhoven S, Moreau JL, Martin JR, Sik A, Blokland A (2007) Effects of the novel 5-HT(6) receptor antagonist RO4368554 in rat models for cognition and sensorimotor gating. Eur Neuropsychopharmacol 17:277–288

    Article  PubMed  CAS  Google Scholar 

  • Schroder N, O’Dell SJ, Marshall JF (2003) Neurotoxic methamphetamine regimen severely impairs recognition memory in rats. Synapse 49:89–96

    Article  PubMed  CAS  Google Scholar 

  • Schubert MH, Young KA, Hicks PB (2006) Galantamine improves cognition in schizophrenic patients stabilized on risperidone. Biol Psychiatry 60:530–533

    Article  PubMed  CAS  Google Scholar 

  • Scott JC, Woods SP, Matt GE, Meyer RA, Heaton RK, Atkinson JH, Grant I (2007) Neurocognitive effects of methamphetamine: a critical review and meta-analysis. Neuropsychol Rev 17:275–297

    Article  PubMed  Google Scholar 

  • Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11–21

    Article  PubMed  CAS  Google Scholar 

  • Seeman P, Lee T (1975) Antipsychotic drugs: direct correlation between clinical potency and presynaptic action on dopamine neurons. Science 188:1217–1219

    Article  PubMed  CAS  Google Scholar 

  • Seeman P, Guan HC, Van Tol HH (1993) Dopamine D4 receptors elevated in schizophrenia. Nature 365:441–445

    Article  PubMed  CAS  Google Scholar 

  • Seidman LJ, Lanca M, Kremen WS, Faraone SV, Tsuang MT (2003) Organizational and visual memory deficits in schizophrenia and bipolar psychoses using the Rey–Osterrieth complex figure: effects of duration of illness. J Clin Exp Neuropsychol 25:949–964

    Article  PubMed  Google Scholar 

  • Shiina A, Shirayama Y, Niitsu T, Hashimoto T, Yoshida T, Hasegawa T, Haraguchi T, Kanahara N, Shiraishi T, Fujisaki M, Fukami G, Nakazato M, Iyo M, Hashimoto K (2010) A randomised, double-blind, placebo-controlled trial of tropisetron in patients with schizophrenia. Ann Gen Psychiatr 9:27

    Article  Google Scholar 

  • Shirayama Y, Yamamoto A, Nishimura T, Katayama S, Kawahara R (2007) Subsequent exposure to the choline uptake enhancer MKC-231 antagonizes phencyclidine-induced behavioral deficits and reduction in septal cholinergic neurons in rats. Eur Neuropsychopharmacol 17:616–626

    Article  PubMed  CAS  Google Scholar 

  • Shirazi-Southall S, Rodriguez DE, Nomikos GG (2002) Effects of typical and atypical antipsychotics and receptor selective compounds on acetylcholine efflux in the hippocampus of the rat. Neuropsychopharmacology 26:583–594

    Article  PubMed  CAS  Google Scholar 

  • Simola N, Bustamante D, Pinna A, Pontis S, Morales P, Morelli M, Herrera-Marschitz M (2008) Acute perinatal asphyxia impairs non-spatial memory and alters motor coordination in adult male rats. Exp Brain Res 185:595–601

    Article  PubMed  Google Scholar 

  • Singer P, Boison D, Möhler H, Feldon J, Yee BK (2007) Enhanced recognition memory following glycine transporter 1 deletion in forebrain neurons. Behav Neurosci 121:815–825

    Article  PubMed  Google Scholar 

  • Singer JM, Wilson MW, Johnson PD, Graham SR, Cooke LW, Roof RL, Boxer PA, Gold LH, Meltzer LT, Janssen A, Roush N, Campbell JE, Su TZ, Hurst SI, Stoner CL, Schwarz JB (2009) Synthesis and SAR of tolylamine 5-HT6 antagonists. Bioorg Med Chem Lett 19:2409–2412

    Article  PubMed  CAS  Google Scholar 

  • Smith RC, Warner-Cohen J, Matute M, Butler E, Kelly E, Vaidhyanathaswamy S, Khan A (2006) Effects of nicotine nasal spray on cognitive function in schizophrenia. Neuropsychopharmacology 31:637–643

    Article  PubMed  CAS  Google Scholar 

  • Smith RC, Lindenmayer JP, Davis JM, Cornwell J, Noth K, Gupta S, Sershen H, Lajtha A (2009a) Cognitive and antismoking effects of varenicline in patients with schizophrenia or schizoaffective disorder. Schizophr Res 110:149–155

    Article  PubMed  Google Scholar 

  • Smith SM, Uslaner JM, Yao L, Mullins CM, Surles NO, Huszar SL, McNaughton CH, Pascarella DM, Kandebo M, Hinchliffe RM, Sparey T, Brandon NJ, Jones B, Venkatraman S, Young MB, Sachs N, Jacobson MA, Hutson PH (2009b) The behavioral and neurochemical effects of a novel D-amino acid oxidase inhibitor compound 8 [4H-thieno [3,2-b]pyrrole-5-carboxylic acid] and D-serine. J Pharmacol Exp Ther 328:921–930

    Article  PubMed  CAS  Google Scholar 

  • Snigdha S, Idris N, Grayson B, Shahid M, Neill JC (2010) Asenapine improves phencyclidine-induced object recognition deficits in the rat: evidence for engagement of a dopamine D(1) receptor mechanism. Psychopharmacology (Berl) 214:843–853

    Article  CAS  Google Scholar 

  • Sood P, Idris NF, Cole S, Grayson B, Neill JC, Young AM (2010) PD168077, a D4 receptor agonist, reverses object recognition deficits in rats: potential role for D4 receptor mechanisms in improving cognitive dysfunction in schizophrenia. J Psychopharmacol 25:792–800

    Article  PubMed  CAS  Google Scholar 

  • Steckler T, Sahgal A (1995) The role of serotonergic–cholinergic interactions in the mediation of cognitive behaviour. Behav Brain Res 67:165–199

    Article  PubMed  CAS  Google Scholar 

  • Stober G, Saar K, Ruschendorf F, Meyer J, Nurnberg G, Jatzke S, Franzek E, Reis A, Lesch KP, Wienker TF, Beckmann H (2000) Splitting schizophrenia: periodic catatonia-susceptibility locus on chromosome 15q15. Am J Hum Genet 67:1201–1207

    PubMed  CAS  Google Scholar 

  • Sullivan EV, Mathalon DH, Ha CN, Zipursky RB, Pfefferbaum A (1992) The contribution of constructional accuracy and organizational strategy to nonverbal recall in schizophrenia and chronic alcoholism. Biol Psychiatry 32:312–333

    Article  PubMed  CAS  Google Scholar 

  • Sullivan PF, Kendler KS, Neale MC (2003) Schizophrenia as a complex trait: evidence from a meta-analysis of twin studies. Arch Gen Psychiatry 60:1187–1192

    Article  PubMed  Google Scholar 

  • Sydserff S, Sutton EJ, Song D, Quirk MC, Maciag C, Li C, Jonak G, Gurley D, Gordon JC, Christian EP, Doherty JJ, Hudzik T, Johnson E, Mrzljak L, Piser T, Smagin GN, Wang Y, Widzowski D, Smith JS (2009) Selective alpha7 nicotinic receptor activation by AZD0328 enhances cortical dopamine release and improves learning and attentional processes. Biochem Pharmacol 78:880–888

    Article  PubMed  CAS  Google Scholar 

  • Taylor SB, Markham JA, Taylor AR, Kanaskie BZ, Koenig JI (2011) Sex-specific neuroendocrine and behavioral phenotypes in hypomorphic Type II Neuregulin 1 rats. Behav Brain Res 224:223–232

    Article  PubMed  CAS  Google Scholar 

  • Tordera RM, Totterdell S, Wojcik SM, Brose N, Elizalde N, Lasheras B, Del Rio J (2007) Enhanced anxiety, depressive-like behaviour and impaired recognition memory in mice with reduced expression of the vesicular glutamate transporter 1 (VGLUT1). Eur J Neurosci 25:281–290

    Google Scholar 

  • Tretter V, Revilla-Sanchez R, Houston C, Terunuma M, Havekes R, Florian C, Jurd R, Vithlani M, Michels G, Couve A, Sieghart W, Brandon N, Abel T, Smart TG, Moss SJ (2009) Deficits in spatial memory correlate with modified {gamma}-aminobutyric acid type A receptor tyrosine phosphorylation in the hippocampus. Proc Natl Acad Sci USA 106:20039–20044

    PubMed  CAS  Google Scholar 

  • Tsai G, Yang P, Chung LC, Lange N, Coyle JT (1998) D-serine added to antipsychotics for the treatment of schizophrenia. Biol Psychiatry 44:1081–1089

    Article  PubMed  CAS  Google Scholar 

  • Tugal O, Yazici KM, Anil Yagcioglu AE, Gogus A (2004) A double-blind, placebo controlled, cross-over trial of adjunctive donepezil for cognitive impairment in schizophrenia. Int J Neuropsychopharmacol 7:117–123

    Article  PubMed  CAS  Google Scholar 

  • Tulving E (1985) How many memory systems are there? Am Psychol 40:385–398

    Article  Google Scholar 

  • Uslaner JM, Parmentier-Batteur S, Flick RB, Surles NO, Lam JS, McNaughton CH, Jacobson MA, Hutson PH (2009) Dose-dependent effect of CDPPB, the mGluR5 positive allosteric modulator, on recognition memory is associated with GluR1 and CREB phosphorylation in the prefrontal cortex and hippocampus. Neuropharmacology 57:531–538

    Article  PubMed  CAS  Google Scholar 

  • van der Stelt M, Di Marzo V (2003) The endocannabinoid system in the basal ganglia and in the mesolimbic reward system: implications for neurological and psychiatric disorders. Eur J Pharmacol 480:133–150

    Article  PubMed  CAS  Google Scholar 

  • Van Dort CJ, Baghdoyan HA, Lydic R (2009) Adenosine A(1) and A(2A) receptors in mouse prefrontal cortex modulate acetylcholine release and behavioral arousal. J Neurosci 29:871–881

    Article  PubMed  CAS  Google Scholar 

  • Vigano D, Guidali C, Petrosino S, Realini N, Rubino T, Di Marzo V, Parolaro D (2009) Involvement of the endocannabinoid system in phencyclidine-induced cognitive deficits modelling schizophrenia. Int J Neuropsychopharmacol 12:599–614

    Article  PubMed  CAS  Google Scholar 

  • Vijayraghavan S, Wang M, Birnbaum SG, Williams GV, Arnsten AF (2007) Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory. Nat Neurosci 10:376–384

    Article  PubMed  CAS  Google Scholar 

  • Wallace TL, Callahan PM, Tehim A, Bertrand D, Tombaugh G, Wang S, Xie W, Rowe WB, Ong V, Graham E, Terry AV Jr, Rodefer JS, Herbert B, Murray M, Porter R, Santarelli L, Lowe DA (2011) RG3487, a novel nicotinic alpha7 receptor partial agonist, improves cognition and sensorimotor gating in rodents. J Pharmacol Exp Ther 336:242–253

    Article  PubMed  CAS  Google Scholar 

  • Warburton EC, Koder T, Cho K, Massey PV, Duguid G, Barker GR, Aggleton JP, Bashir ZI, Brown MW (2003) Cholinergic neurotransmission is essential for perirhinal cortical plasticity and recognition memory. Neuron 38:987–996

    Article  PubMed  CAS  Google Scholar 

  • Weiser M, Reichenberg A, Grotto I, Yasvitzky R, Rabinowitz J, Lubin G, Nahon D, Knobler HY, Davidson M (2004) Higher rates of cigarette smoking in male adolescents before the onset of schizophrenia: a historical-prospective cohort study. Am J Psychiatry 161:1219–1223

    Article  PubMed  Google Scholar 

  • West PJ, Marcy VR, Marino MJ, Schaffhauser H (2009) Activation of the 5-HT(6) receptor attenuates long-term potentiation and facilitates GABAergic neurotransmission in rat hippocampus. Neuroscience 164:692–701

    Article  PubMed  CAS  Google Scholar 

  • Winters BD, Bussey TJ (2005a) Glutamate receptors in perirhinal cortex mediate encoding, retrieval, and consolidation of object recognition memory. J Neurosci 25:4243–4251

    Article  PubMed  CAS  Google Scholar 

  • Winters BD, Bussey TJ (2005b) Removal of cholinergic input to perirhinal cortex disrupts object recognition but not spatial working memory in the rat. Eur J Neurosci 21:2263–2270

    Article  PubMed  Google Scholar 

  • Winters BD, Forwood SE, Cowell RA, Saksida LM, Bussey TJ (2004) Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: heterogeneity of function within the temporal lobe. J Neurosci 24:5901–5908

    Article  PubMed  CAS  Google Scholar 

  • Winters BD, Saksida LM, Bussey TJ (2006) Paradoxical facilitation of object recognition memory after infusion of scopolamine into perirhinal cortex: implications for cholinergic system function. J Neurosci 26:9520–9529

    Article  PubMed  CAS  Google Scholar 

  • Winters BD, Saksida LM, Bussey TJ (2008) Object recognition memory: neurobiological mechanisms of encoding, consolidation and retrieval. Neurosci Biobehav Rev 32:1055–1070

    Article  PubMed  Google Scholar 

  • Winters BD, Bartko SJ, Saksida LM, Bussey TJ (2010) Muscimol, AP5, or scopolamine infused into perirhinal cortex impairs two-choice visual discrimination learning in rats. Neurobiol Learn Mem 93:221–228

    Article  PubMed  CAS  Google Scholar 

  • Wishka DG, Walker DP, Yates KM, Reitz SC, Jia S, Myers JK, Olson KL, Jacobsen EJ, Wolfe ML, Groppi VE, Hanchar AJ, Thornburgh BA, Cortes-Burgos LA, Wong EH, Staton BA, Raub TJ, Higdon NR, Wall TM, Hurst RS, Walters RR, Hoffmann WE, Hajos M, Franklin S, Carey G, Gold LH, Cook KK, Sands SB, Zhao SX, Soglia JR, Kalgutkar AS, Arneric SP, Rogers BN (2006) Discovery of N-[(3R)-1-azabicyclo[2.2.2]oct-3-yl]furo[2,3-c]pyridine-5-carboxamide, an agonist of the alpha7 nicotinic acetylcholine receptor, for the potential treatment of cognitive deficits in schizophrenia: synthesis and structure–activity relationship. J Med Chem 49:4425–4436

    Article  PubMed  CAS  Google Scholar 

  • Woo TU, Miller JL, Lewis DA (1997) Schizophrenia and the parvalbumin-containing class of cortical local circuit neurons. Am J Psychiatry 154:1013–1015

    PubMed  CAS  Google Scholar 

  • Woolley M, Marsden C, Sleight A, Fone K (2000) Reversal of a scopolamine-induced deficit in object discrimination by a selective 5-HT6 receptor antagonist, Ro 046790, in rats. Br J Pharmacol: U39-U39.

  • Woolley ML, Marsden CA, Sleight AJ, Fone KC (2003) Reversal of a cholinergic-induced deficit in a rodent model of recognition memory by the selective 5-HT6 receptor antagonist, Ro 04–6790. Psychopharmacology (Berl) 170:358–367

    Article  CAS  Google Scholar 

  • Woolley ML, Waters KA, Reavill C, Bull S, Lacroix LP, Martyn AJ, Hutcheson DM, Valerio E, Bate S, Jones DN, Dawson LA (2008) Selective dopamine D4 receptor agonist (A-412997) improves cognitive performance and stimulates motor activity without influencing reward-related behaviour in rat. Behav Pharmacol 19:765–776

    Article  PubMed  CAS  Google Scholar 

  • Yonelinas AP, Aly M, Wang WC, Koen JD (2010) Recollection and familiarity: examining controversial assumptions and new directions. Hippocampus 20:1178–1194

    Article  PubMed  Google Scholar 

  • Young JW, Powell SB, Risbrough V, Marston HM, Geyer MA (2009) Using the MATRICS to guide development of a preclinical cognitive test battery for research in schizophrenia. Pharmacol Ther 122:150–202

    Article  PubMed  CAS  Google Scholar 

  • Zamberletti E, Vigano D, Guidali C, Rubino T, Parolaro D (2010) Long-lasting recovery of psychotic-like symptoms in isolation-reared rats after chronic but not acute treatment with the cannabinoid antagonist AM251. Int J Neuropsychopharmacol: 1–14.

  • Zanassi P, Paolillo M, Feliciello A, Avvedimento EV, Gallo V, Schinelli S (2001) cAMP-dependent protein kinase induces cAMP-response element-binding protein phosphorylation via an intracellular calcium release/ERK-dependent pathway in striatal neurons. J Biol Chem 276:11487–11495

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Sun J, Reynolds GP (2002) A selective reduction in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia patients. Chin Med J (Engl) 115:819–823

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank Prof. Trevor Robbins and Dr. Mark Tricklebank for comments on an earlier version of the manuscript. This work has received support from the Innovative Medicine Initiative Joint Undertaking under grant agreement n° 115008 of which resources are composed of EFPIA in‐kind contribution and financial contribution from the European Union’s Seventh Framework Programme (FP7/2007‐2013).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. J. Bussey.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lyon, L., Saksida, L.M. & Bussey, T.J. Spontaneous object recognition and its relevance to schizophrenia: a review of findings from pharmacological, genetic, lesion and developmental rodent models. Psychopharmacology 220, 647–672 (2012). https://doi.org/10.1007/s00213-011-2536-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-011-2536-5

Keywords

Navigation