Influence of social isolation in the rat on serotonergic function and memory - Relevance to models of schizophrenia and the role of 5-HT6 receptors

Neuropharmacology

Volumn 61, Issue 3, 2011, Pages 400-407

  Marsden, Charles A ^a   King, Madeleine V ^a   Fone, Kevin C F ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

5 Hydroxytryptamine; Cognition; Glutamate; Isolation rearing; Learning and memory; Novel object discrimination; Schizophrenia; Serotonin

Indexed keywords

4 AMINO 2 OXABICYCLO[3.1.0]HEXANE 4,6 DICARBOXYLIC ACID; 4 AMINO N [2,6 BIS(METHYLAMINO) 4 PYRIMIDINYL]BENZENESULFONAMIDE; BRAIN DERIVED NEUROTROPHIC FACTOR; CLOZAPINE; DIZOCILPINE; GLUTAMIC ACID; N (3,5 DICHLORO 2 METHOXYPHENYL) 4 METHOXY 3 (1 PIPERAZINYL)BENZENESULFONAMIDE; PRX 07034; PRX 07037; RO 4368554; RO 65 7199; SEROTONIN; SEROTONIN 6 ANTAGONIST; SEROTONIN 6 RECEPTOR; UNCLASSIFIED DRUG; 2 METHYL 6 (PHENYLETHYNYL)PYRIDINE; 4 AMINOBUTYRIC ACID; ATYPICAL ANTIPSYCHOTIC AGENT; E 6801; NEUROTRANSMITTER; SEROTONIN AGONIST; ST 1936; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2; VESICULAR GLUTAMATE TRANSPORTER 3; WAY 181187;

ANIMAL BEHAVIOR; BEHAVIORAL SCIENCE; BRAIN ATROPHY; BRAIN CORTEX; BRAIN REGION; DISEASE ASSOCIATION; DRUG ANTAGONISM; DRUG TARGETING; HIPPOCAMPUS; MEMORY DISORDER; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; REVIEW; SCHIZOPHRENIA; SEROTONINERGIC SYSTEM; SOCIAL ISOLATION; ACETYLCHOLINE RELEASE; AMNESIA; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN NERVE CELL; CELL ACTIVITY; CHOLINERGIC TRANSMISSION; COGNITION; COGNITIVE DEFECT; CONFERENCE PAPER; DISEASE CONTROL; DRUG MECHANISM; ENVIRONMENTAL FACTOR; EPISODIC MEMORY; EXPERIMENTAL MOUSE; EXPERIMENTAL RAT; FUNCTIONAL STATUS; GABAERGIC TRANSMISSION; LEARNING DISORDER; NERVE CELL DEGENERATION; NERVE CELL DIFFERENTIATION; NEUROBIOLOGY; PATTERN RECOGNITION; PLACE PREFERENCE; PREPULSE INHIBITION; PROTEIN FUNCTION; REARING; REWARD; SEROTONIN RELEASE; SEROTONINERGIC TRANSMISSION; VISUAL DISCRIMINATION; VISUAL MEMORY;

ANIMALS; BEHAVIOR, ANIMAL; CEREBRUM; COGNITION DISORDERS; HUMANS; MEMORY DISORDERS; NERVE TISSUE PROTEINS; NEURONS; RATS; RECEPTORS, SEROTONIN; SCHIZOPHRENIA; SEROTONIN; SEROTONIN ANTAGONISTS; SOCIAL ISOLATION;

EID: 79958144364     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2011.03.003     Document Type: Review

References (107)

1. V.P. Bakshi, and M.A. Geyer Ontogeny of isolation rearing-induced deficits in sensorimotor gating in rats Physiology & Behavior 67 1999 385 392 (Pubitemid 29469542)
2. S.J. Ballaz, H. Akil, and S.J. Watson Analysis of 5-HT6 and 5-HT7 receptor gene expression in rats showing differences in novelty-seeking behavior Neuroscience 147 2007 428 438 (Pubitemid 46907454)
3. G.R.I. Barker, F. Bird, V. Alexander, and E.C. Warburton Recognition memory for objects, place, and temporal order: a disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex Journal of Neuroscience 27 2007 2948 2957 (Pubitemid 46438982)
4. A.M. Barr, S.B. Powell, A. Markou, and M.A. Geyer Iloperidone reduces sensorimotor gating deficits in pharmacological models, but not a developmental model, of disrupted prepulse inhibition in rats Neuropharmacology 51 2006 457 465 (Pubitemid 44215953)
5. A. Bellon, G. Le Pen, J. Matricon, T.M. Jay, and M.O. Krebs Potential application as screening and drug designing tools of cytoarchitectural deficiencies present in three animal models of schizophrenia Expert Opinion on Drug Discovery 4 2009 257 278
6. M. Bianchi, K.C.F. Fone, A.J. Shah, A.R. Atkins, L.A. Dawson, C.A. Heidbreder, J.J. Hagan, and C.A. Marsden Chronic fluoxetine differentially modulates the hippocampal microtubular and serotonergic system in grouped and isolation reared rats European Neuropsychopharmacology 19 2009 778 790
7. M. Bianchi, K.F.C. Fone, N. Azmi, C.A. Heidbreder, J.J. Hagan, and C.A. Marsden Isolation rearing induces recognition memory deficits accompanied by cytoskeletal alterations in rat hippocampus European Journal of Neuroscience 24 2006 2894 2902 (Pubitemid 44813840)
8. M.J. Bickerdike, I.K. Wright, and C.A. Marsden Social isolation attenuates rat forebrain 5-HT release induced by KCI stimulation and exposure to a novel environment Behavioural Pharmacology 4 1993 231 236 (Pubitemid 23181742)
9. J.M. Birrell, and V.J. Brown Medial frontal cortex mediates perceptual attentional set shifting in the rat Journal of Neuroscience 20 2000 4320 4324 (Pubitemid 30365702)
10. A. Bjornebekk, A.A. Mathe, and S. Brene Isolated flinders sensitive line rats have decreased dopamine D2 receptor mRNA Neuroreport 18 2007 1039 1043 (Pubitemid 46905180)
11. V.P. Bozikas, M.H. Kosmidis, G. Kiosseoglou, and A. Karavatos Neuropsychological profile of cognitively impaired patients with schizophrenia Comprehensive Psychiatry 47 2006 136 143 (Pubitemid 43259419)
12. M.W. Brown, and J.P. Aggleton Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nature Reviews Neuroscience 2 2001 51 61 (Pubitemid 33673349)
13. K.E. Burnham, M.G. Baxter, J.R. Bainton, E. Southam, L.A. Dawson, D.M. Bannerman, and T. Sharp Activation of 5-HT6 receptors facilitates attentional set shifting Psychopharmacology 208 2010 13 21
14. A.W. Cassidy, S.K. Mulvany, M.N. Pangalos, K.J. Murphy, and C.M. Regan Developmental emergence of reelin deficits in the prefrontal cortex of Wistar rats reared in social isolation Neuroscience 166 2010 377 385
15. A.W. Cassidy, S.K. Mulvany, M.N. Pangalos, K.J. Murphy, and C.M. Regan Reduced reelin protein synthesis in ventral hippocampus of isolation reared Wistar rats accompanies impaired avoidance conditioning Behavioural Brain Research 213 2010 130 134
16. Y. Chudasama, and T.W. Robbins Psychopharmacological approaches to modulating attention in the five-choice serial reaction time task: implications for schizophrenia Psychopharmacology 174 2004 86 98 (Pubitemid 38925094)
17. J. Cilia, C. Reavill, J.J. Hagan, and D.N.C. Jones Long-term evaluation of isolation-rearing induced prepulse inhibition deficits in rats Psychopharmacology 156 2001 327 337 (Pubitemid 32702222)
18. T.A. Comery, R. Shah, and W.T. Greenough Differential rearing alters spine density on medium-sized spiny neurons in the rat corpus striatum - evidence for association of morphological plasticity with early response gene-expression Neurobiology of Learning and Memory 63 1995 217 219
19. J.W. Dalley, D.E. Theobald, E.A.C. Pereira, P. Li, and T.W. Robbins Specific abnormalities in serotonin release in the prefrontal cortex of isolation-reared rats measured during behavioural performance of a task assessing visuospatial attention and impulsivity Psychopharmacology 164 2002 329 340 (Pubitemid 35341000)
20. K.M. Day-Wilson, D.N.C. Jones, E. Southam, J. Cilia, and S. Totterdell Medial prefrontal cortex volume loss in rats with isolation rearing-induced deficits in prepulse inhibition of acoustic startle Neuroscience 141 2006 1113 1121 (Pubitemid 44128668)
21. G. De Foubert, M.J. O'Neill, and T.S.C. Zetterstrom Acute onset by 5-HT6-receptor activation on rat brain brain-derived neurotrophic factor and activity-regulated cytoskeletal-associated protein mRNA expression Neuroscience 147 2007 778 785 (Pubitemid 46990655)
22. E. Djouma, K. Card, D.J. Lodge, and A.J. Lawrence The CRF1 receptor antagonist, antalarmin, reverses isolation-induced up-regulation of dopamine D-2 receptors in the amygdala and nucleus accumbens of Fawn-Hooded rats European Journal of Neuroscience 23 2006 3319 3327
23. S.L. Eastwood, P.W. Burnet, and P.J. Harrison Decreased hippocampal expression of the susceptibility gene PPP3CC and other calcineurin subunits in schizophrenia Biological Psychiatry 57 2005 702 710 (Pubitemid 40487913)
24. D.F. Einon, and M.J. Morgan A critical period for social isolation in the rat Developmental Psychobiology 10 1977 123 132 (Pubitemid 8101093)
25. R. Elliott, P.J. McKenna, T.W. Robbins, and B.J. Sahakian Neuropsychological evidence for frontostriatal dysfunction in schizophrenia Psychological Medicine 25 1995 619 630
26. A. Ennaceur, and J. Delacour A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data Behavioural Brain Research 31 1988 47 59
27. A.G. Foley, W.D. Hirst, H.C. Gallagher, C. Barry, J.J. Hagan, N. Upton, F.S. Walsh, A.J. Hunter, and C.M. Regan The selective 5-HT6 receptor antagonists SB-271046 and SB-399885 potentiate NCAM PSA immunolabeling not neurogenesis, in the hippocampal of dentate granule cells, but formation of mature Wistar rats Neuropharmacology 54 2008 1166 1174
28. K.C. Fone, K. Shalders, Z.D. Fox, R. Arthur, and C.A. Marsden Increased 5-HT2C receptor responsiveness occurs on rearing rats in social isolation Psychopharmacology (Berlin) 123 1996 346 352
29. K.C.F. Fone An update on the role of the 5-hydroxytryptamine(6) receptor in cognitive function Neuropharmacology 55 2008 1015 1022
30. K.C.F. Fone, and M.V. Porkess Behavioural and neurochemical effects of post-weaning social isolation in rodents - relevance to developmental neuropsychiatric disorders Neuroscience & Biobehavioral Reviews 32 2008 1087 1102
31. A.J. Fulford, and C.A. Marsden Social isolation in the rat enhances alpha(2)-autoreceptor function in the hippocampus in vivo Neuroscience 77 1997 57 64 (Pubitemid 27060306)
32. A.J. Fulford, and C.A. Marsden Conditioned release of 5-hydroxytryptamine in vivo in the nucleus accumbens following isolation-rearing in the rat Neuroscience 83 1998 481 487 (Pubitemid 28062638)
33. A.J. Fulford, and C.A. Marsden Effect of isolation-rearing on conditioned dopamine release in vivo in the nucleus accumbens of the rat Journal of Neurochemistry 70 1998 384 390 (Pubitemid 28020866)
34. C. Gerard, S. ElMestikawy, C. Lebrand, J. Adrien, M. Ruat, E. Traiffort, M. Hamon, and M.P. Martres Quantitative RT-PCR distribution of serotonin 5-HT6 receptor mRNA in the central nervous system of control or 5,7- dihydroxytryptamine-treated rats Synapse 23 1996 164 173 (Pubitemid 26230563)
35. M.A. Geyer, L.S. Wilkinson, T. Humby, and T.W. Robbins Isolation rearing of rats produces a deficit in prepulse inhibition of acoustic startle similar to that in schizophrenia Biological Psychiatry 34 1993 361 372 (Pubitemid 23295752)
36. F.S. Hall, T. Humby, L.S. Wilkinson, and T.W. Robbins The effects of isolation-rearing on sucrose consumption in rats Physiology & Behavior 62 1997 291 297 (Pubitemid 27326897)
37. F.S. Hall, L.S. Wilkinson, T. Humby, W. Inglis, D.A. Kendall, C.A. Marsden, and T.W. Robbins Isolation rearing in rats: pre- and postsynaptic changes in striatal dopaminergic systems Pharmacology Biochemistry and Behavior 59 1998 859 872 (Pubitemid 28237897)
38. R.S. Hammond, L.E. Tull, and R.W. Stackman On the delay-dependent involvement of the hippocampus in object recognition memory Neurobiology of Learning and Memory 82 2004 26 34 (Pubitemid 38737427)
39. M.K. Harte, S.B. Powell, N.R. Swerdlow, M.A. Geyer, and G.P. Reynolds Deficits in parvalbumin and calbindin immunoreactive cells in the hippocampus of isolation reared rats Journal of Neural Transmission 114 2007 893 898 (Pubitemid 47013594)
40. C.A. Heidbreder, R. Foxton, J. Cilia, Z.A. Hughes, A.J. Shah, A. Atkins, A.J. Hunter, J.J. Hagan, and D.N. Jones Increased responsiveness of dopamine to atypical, but not typical antipsychotics in the medial prefrontal cortex of rats reared in isolation Psychopharmacology (Berlin) 156 2001 338 351 (Pubitemid 32702223)
41. C.A. Heidbreder, I.C. Weiss, A.M. Domeney, C. Pryce, J. Homberg, G. Hedou, J. Feldon, M.C. Moran, and P. Nelson Behavioral, neurochemical and endocrinological characterization of the early social isolation syndrome Neuroscience 100 2000 749 768
42. C. Heim, and C.B. Nemeroff The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies Biological Psychiatry 49 2001 1023 1039 (Pubitemid 32595461)
43. K.G.C. Hellemans, L.C. Benge, and M.C. Olmstead Adolescent enrichment partially reverses the social isolation syndrome Developmental Brain Research 150 2004 103 115 (Pubitemid 38639815)
44. S.R. Howes, J.W. Dalley, C.H. Morrison, T.W. Robbins, and B.J. Everitt Leftward shift in the acquisition of cocaine self-administration in isolation-reared rats: relationship to extracellular levels of dopamine, serotonin and glutamate in the nucleus accumbens and amygdala-striatal FOS expression Psychopharmacology (Berlin) 151 2000 55 63 (Pubitemid 30639840)
45. D. Ibi, K. Takuma, H. Koike, H. Mizoguchi, K. Tsuritani, Y. Kuwahara, H. Kamei, T. Nagai, Y. Yoneda, T. Nabeshima, and K. Yamada Social isolation rearing-induced impairment of the hippocampal neurogenesis is associated with deficits in spatial memory and emotion-related behaviors in juvenile mice Journal of Neurochemistry 105 2008 921 932 (Pubitemid 351562741)
46. S. Jessberger, R.E. Clark, N.J. Broadbent, G.D. Clemenson Jr., A. Consiglio, D.C. Lie, L.R. Squire, and F.H. Gage Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats Learning & Memory 16 2009 147 154
47. C. Jones, A.M. Brown, D.P. Auer, and K.C.F. Fone The mGluR2/3 agonist LY379268 reverses post-weaning social isolation induced recognition memory deficits in the rat Psychopharmacology (Berlin) 214 2011 269 283
48. Jones, C.A., Watson, D.J.G., Fone, K.C.F. Animal models of schizophrenia. British Journal of Pharmacology, in press.
49. G.H. Jones, T.D. Hernandez, D.A. Kendall, C.A. Marsden, and T.W. Robbins Dopaminergic and serotonergic function following isolation rearing in rats: study of behavioural responses and postmortem and in vivo neurochemistry Pharmacology Biochemistry and Behavior 43 1992 17 35
50. G.H. Jones, C.A. Marsden, and T.W. Robbins Behavioural rigidity and rule-learning deficits following isolation-rearing in the rat: neurochemical correlates Behavioural Brain Research 43 1991 35 50
51. C.S. Karam, J.S. Ballon, N.M. Bivens, Z. Freyberg, R.R. Girgis, J.E. Lizardi-Ortiz, S. Markx, J.A. Lieberman, and J.A. Javitch Signaling pathways in schizophrenia: emerging targets and therapeutic strategies Trends in Pharmacological Sciences 31 2010 381 390
52. I. Kendall, H.A. Slotten, X. Codony, J. Burgueno, P.J. Pauwels, J.M. Vela, and K.C. Fone E-6801, a 5-HT(6) receptor agonist, improves recognition memory by combined modulation of cholinergic and glutamatergic neurotransmission in the rat Psychopharmacology (Berlin) 213 2011 413 420
53. M. King, C. Spicer, A. Sleight, C. Marsden, and K. Fone 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 202 2009 111 123
54. M.V. King, K.C.F. Fone, S. Shacham, and K.S. Gannon The novel 5-HT6 receptor antagonist, PRX-07037, enhances memory and reduces food intake in a neurodevelopmental model of schizophrenia Journal of Psychopharmacology 21 2007 A57
55. 6 receptor antagonist, reduces weight gain and enhances memory in a neurodevelopmental model of schizophrenia Society for Neuroscience Abstracts 2007 499.25
56. M.V. King, N. Kurian, M. Smith, D. Ray, K.C.F. Fone, D.A. Kendall, C.A. Marsden, and T.V. Sharp Reversal of vesicular glutamate transporter 1 (VGLUT1) lentiviral short hairpin RNA (SHRNA) vector-induced cognitive deficits by a 5-HT6 receptor antagonist Journal of Psychopharmacology 24 2010 A68
57. M.V. King, C.A. Marsden, and K.C.F. Fone A role for the 5-HT1A, 5-HT4 and 5-HT6 receptors in learning and memory Trends in Pharmacological Sciences 29 2008 482 492
58. M.V. King, N. Papadopolou, N. Kurian, K.C.F. Fone, D.A. Kendall, C.A. Marsden, and T.V. Sharp Lentiviral delivery of a short hairpin RNA (shRNA) vector targeting vesicular glutamate transporter 1 (VGLUT1) into mouse hippocampus impairs cognition Journal of Psychopharmacology 23S 2009 A19
59. M.V. King, A.J. Sleight, M.L. Woolley, I.A. Topham, C.A. Marsden, and K.C.F. Fone 5-HT6 receptor antagonists reverse delay-dependent deficits in novel object discrimination by enhancing consolidation - an effect sensitive to NMDA receptor antagonism Neuropharmacology 47 2004 195 204 (Pubitemid 38824643)
60. L.P. Lacroix, L.A. Dawson, J.J. Hagan, and C.A. Heidbreder 5-HT6 receptor antagonist SB-271046 enhances extracellular levels of monoamines in the rat medial prefrontal cortex Synapse 51 2004 158 164 (Pubitemid 38018798)
61. M.D. Lapiz, Y. Mateo, T. Parker, and C. Marsden Effects of noradrenaline depletion in the brain on response on novelty in isolation-reared rats Psychopharmacology (Berlin) 152 2000 312 320
62. A. Leng, A. Ouagazzal, J. Feldon, and G.A. Higgins Effect of the 5-HT6 receptor antagonists Ro 04-6790 and Ro 65-7199 on latent inhibition and prepulse inhibition in the rat: comparison to clozapine Pharmacology Biochemistry and Behavior 75 2003 281 288 (Pubitemid 36859812)
63. N.X. Li, J.L. Ping, R.B. Wu, C. Wang, X.H. Wu, and L. Li Auditory fear conditioning modulates prepulse inhibition in socially reared rats and isolation-reared rats Behavioral Neuroscience 122 2008 107 118 (Pubitemid 351389709)
64. F. Loiseau, A. Dekeyne, and M.J. Millan Pro-cognitive effects of 5-HT6 receptor antagonists in the social recognition procedure in rats: implication of the frontal cortex Psychopharmacology 196 2008 93 104
65. B. Marcos, M. Cabero, M. Solas, B. Aisa, and M.J. Ramirez Signalling pathways associated with 5-HT6 receptors: relevance for cognitive effects International Journal of Neuropsychopharmacology 13 2010 775 784
66. M.M. McClure, M.J. Romero, C.R. Bowie, A. Reichenberg, P.D. Harvey, and L.J. Siever Visual-spatial learning and memory in schizotypal personality disorder: continued evidence for the importance of working memory in the schizophrenia spectrum Archives of Clinical Neuropsychology 22 2007 109 116 (Pubitemid 46209596)
67. S.L. McLean, B. Grayson, M. Harris, C. Protheroe, S. Bate, M.L. Woolley, and J.C. Neill Isolation rearing impairs novel object recognition and attentional set shifting performance in female rats Journal of Psychopharmacology 24 2010 57 63
68. J. Meffre, M. Seveno, M.J. Milian, C.M. La Cour, A. Dekeyne, J. Bockaert, and P. Marin Proteomic and functional analysis suggests that 5-HT6 receptors compromise cognition by recruiting mTOR Schizophrenia Research 117 2010 373 374
69. M.J. Millan, and M. Brocco Cognitive impairment in schizophrenia: a review of developmental and genetic models, and pro-cognitive profile of the optimised D-3 > D-2 antagonist, S33138 Therapie 63 2008 187 229
70. E.S. Mitchell, B.J. Hoplight, S.P. Lear, and J.F. Neumaier BGC20-761, a novel tryptamine analog, enhances memory consolidation and reverses scopolamine-induced memory deficit in social and visuospatial memory tasks through a 5-HT6 receptor-mediated mechanism Neuropharmacology 50 2006 412 420 (Pubitemid 43209037)
71. E.S. Mitchell, and J.F. Neumaier 5-HT6 receptor antagonist reversal of emotional learning and prepulse inhibition deficits induced by apomorphine or scopolamine Pharmacology Biochemistry and Behavior 88 2008 291 298 (Pubitemid 350116256)
72. C. Morgan, and H. Fisher Environment and schizophrenia: environmental factors in schizophrenia: childhood trauma - a critical review Schizophrenia Bulletin 33 2007 3 10 (Pubitemid 46026253)
73. M.J. Morgan Effects of post-weaning environment on learning in rat Animal Behaviour 21 1973 429 442
74. S. Muchimapura, A.J. Fulford, R. Mason, and C.A. Marsden Isolation rearing in the rat disrupts the hippocampal response to stress Neuroscience 112 2002 697 705 (Pubitemid 34634163)
75. S. Muchimapura, R. Mason, and C.A. Marsden Effect of isolation rearing on pre- and post-synaptic serotonergic function in the rat dorsal hippocampus Synapse 47 2003 209 217 (Pubitemid 36056834)
76. K.J. Murphy, J.P.F. ter Horst, A.W. Cassidy, I.E.J. DeSouza, M. Morgunova, C. Li, L.M. Connole, N.C. O'Sullivan, J.S. Loscher, A.T. Brady, N. Rombach, J. Connellan, P.A. McGettigan, D. Scully, R. Fedriani, B. Lukasz, M.P. Moran, O.M. McCabe, C.M. Wantuch, Z.A. Hughes, S.K. Mulvany, D.G. Higgins, M.N. Pangalos, K.L. Marquis, W.T. O'Connor, R.H. Ring, D. von Schack, and C.M. Regan Temporal dysregulation of cortical gene expression in the isolation reared Wistar rat Journal of Neurochemistry 113 2010 601 614
77. J.C. Myskiw, J.I. Rossato, L.R.M. Bevilaqua, J.H. Medina, I. Izquierdo, and M. Cammarota On the participation of mTOR in recognition memory Neurobiology of Learning and Memory 89 2008 338 351 (Pubitemid 351318273)
78. J.C. Neill, S. Barnes, S. Cook, B. Grayson, N.F. Idris, S.L. McLean, S. Snigdha, L. Rajagopal, and M.K. Harte Animal models of cognitive dysfunction and negative symptoms of schizophrenia: focus on NMDA receptor antagonism Pharmacology & Therapeutics 128 2010 419 432
79. P.G. Nestor, M. Kubicki, N. Kuroki, R.J. Gurrera, M. Nimikiewicz, M.E. Shenton, and R.W. McCarley Episodic memory and neuroimaging of hippocampus and fornix in chronic schizophrenia Psychiatry Research - Neuroimaging 155 2007 21 28 (Pubitemid 46578289)
80. G.D. Phillips, S.R. Howes, R.B. Whitelaw, L.S. Wilkinson, T.W. Robbins, and B.J. Everitt Isolation rearing enhances the locomotor response to cocaine and a novel environment, but impairs the intravenous self-administration of cocaine Psychopharmacology 115 1994 407 418 (Pubitemid 24217102)
81. P.M. Plotsky, and M.J. Meaney Early, postnatal experience alters hypothalamic corticotrophin-releasing factor (CRF) messenger-RNA, median-eminence CRF content and stress-induced release in adult-rats Molecular Brain Research 18 1993 195 200
82. M.A. Preece, J.W. Dalley, D.E.H. Theobald, T.W. Robbins, and G.P. Reynolds Region specific changes in forebrain 5-hydroxytryptamine(1A) and 5-hydroxytryptamine(2A) receptors in isolation-reared rats: an in vitro autoradiography study Neuroscience 123 2004 725 732 (Pubitemid 38045409)
83. S. Qin, N. Kurian, M.V. King, C. Hofland, T.V. Sharp, E. Dremencov, T.I.F.H. Cremers, and B.H.C. Westerink In vivo shRNA knockdown of VGluT1 via lentivirus-mediated delivery system reduces Glu release in hippocampus FENS Abstracts 5 2010 079.35
84. C. Riemer, E. Borroni, B. Levet-Trafit, J.R. Martin, S. Poli, R.H.P. Porter, and M. Bos 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 Journal of Medicinal Chemistry 46 2003 1273 1276 (Pubitemid 36428233)
85. R. Schreiber, J. Vivian, L. Hedley, K. Szczepanski, R.L. Secchi, M. Zuzow, S. van Laarhoven, J.L. Moreau, J.R. Martin, A. Sik, and A. Blokland Effects of the novel 5-HT6 receptor antagonist RO4368554 in rat models for cognition and sensorimotor gating European Neuropsychopharmacology 17 2007 277 288 (Pubitemid 46135932)
86. N.C. Schrijver, P.N. Pallier, V.J. Brown, and H. Wurbel Double dissociation of social and environmental stimulation on spatial learning and reversal learning in rats Behavioural Brain Research 152 2004 307 314 (Pubitemid 38757901)
87. N.C.A. Schrijver, and H. Wurbel Early social deprivation disrupts attentional, but not affective, shifts in rats Behavioral Neuroscience 115 2001 437 442 (Pubitemid 32378172)
88. M.I. Schubert, M.V. Porkess, N. Dashdorj, K.C.F. Fone, and D.P. Auer Effects of social isolation rearing on the limbic brain: a combined behavioral and magnetic resonance imaging volumetry study in rats Neuroscience 159 2009 21 30
89. A.B. Silva-Gomez, D. Rojas, I. Juarez, and G. Flores Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats Brain Research 983 2003 128 136 (Pubitemid 36957950)
90. H.A. Slotten, M. Kalinichev, J.J. Hagan, C.A. Marsden, and K.C.F. Fone Long-lasting changes in behavioural and neuroendocrine indices in the rat following neonatal maternal separation: gender-dependent effects Brain Research 1097 2006 123 132 (Pubitemid 44043110)
91. C.S. Stanford, and C.A. Marsden Regional specialisation in the central noradrenergic response to unconditioned and conditioned environmental stimuli T. Steckler, Handbook of Stress and the Brain 2005 487 501
92. C.W. Stevenson, C.A. Marsden, and R. Mason Early life stress causes FG-7142-induced corticolimbic dysfunction in adulthood Brain Research 1193 2008 43 50
93. N.R. Swerdlow, D.L. Braff, and M.A. Geyer Animal models of deficient sensorimotor gating: what we know, what we think we know and what we hope to know soon Behavioural Pharmacology 11 2000 185 204 (Pubitemid 30449750)
94. V. Valentini, R. Frau, F. Bordi, F. Borsini, and G. Di Chiara A microdialysis study of ST1936, a novel 5-HT6 receptor agonist Neuropharmacology 60 2011 602 608
95. J. van Os, G. Kenis, and B.P.F. Rutten The environment and schizophrenia Nature 468 2010 203 212
96. G.B. Varty, D.L. Braff, and M.A. Geyer Is there a critical developmental 'window' for isolation rearing-induced changes in prepulse inhibition of the acoustic startle response? Behavioural Brain Research 100 1999 177 183 (Pubitemid 29130252)
97. G.B. Varty, and M.A. Geyer Effects of isolation rearing on startle reactivity, habituation, and prepulse inhibition in male Lewis, Sprague-Dawley, and Fischer F344 rats Behavioral Neuroscience 112 1998 1450 1457 (Pubitemid 29052632)
98. G.B. Varty, and G.A. Higgins Examination of drug-induced and isolation-induced disruptions of prepulse inhibition as models to screen antipychotic drugs Psychopharmacology 112 1995 15 26
99. G.B. Varty, C.A. Marsden, and G.A. Higgins Reduced synaptophysin immunoreactivity in the dentate gyrus of prepulse inhibition-impaired isolation-reared rats Brain Research 824 1999 197 203 (Pubitemid 29225524)
100. I.C. Weiss, L. Di Iorio, J. Feldon, and A.M. Domeney Strain differences in the isolation-induced effects on prepulse inhibition of the acoustic startle response and on locomotor activity Behavioral Neuroscience 114 2000 364 373 (Pubitemid 30488996)
101. I.C. Weiss, J. Feldon, and A.M. Domeney Isolation rearing-induced disruption of prepulse inhibition: further evidence for fragility of the response Behavioural Pharmacology 10 1999 139 149 (Pubitemid 29150034)
102. N. Wongwitdecha, and C.A. Marsden Effect of social isolation on the reinforcing properties of morphine in the conditioned place preference test Pharmacology Biochemistry and Behavior 53 1996 531 534 (Pubitemid 26088538)
103. M.L. Woolley, C.A. Marsden, and K.C. Fone 5-HT6 receptors Current Drug Targets - CNS & Neurological Disorders 3 2004 59 79
104. I.K. Wright, H. Ismail, N. Upton, and C.A. Marsden Effect of isolation rearing on 5-HT agonist-induced responses in the rat Psychopharmacology 105 1991 259 263
105. I.K. Wright, N. Upton, and C.A. Marsden Effect of established and putative anxiolytics on extracellular 5-HT and 5-HIAA in the ventral hippcampus of rats during behaviour on the elevated X-maze Psychopharmacology 109 1992 338 346
106. H.M. Yun, J.H. Baik, I. Kang, C. Jin, and H. Rhim Physical interaction of Jab1 with human serotonin 6 G-protein-coupled receptor and their possible roles in cell survival Journal of Biological Chemistry 285 2010 10016 10029
107. H.M. Yun, S. Kim, H.J. Kim, E. Kostenis, J.I. Kim, J.Y. Seong, J.H. Baik, and H. Rhim The novel cellular mechanism of human 5-HT6 receptor through an interaction with Fyn Journal of Biological Chemistry 282 2007 5496 5505 (Pubitemid 47093777)