Why do lesions in the rodent anterior thalamic nuclei cause such severe spatial deficits?

Neuroscience and Biobehavioral Reviews

Volumn 54, Issue , 2015, Pages 131-144

  Aggleton, John P ^a   Nelson, Andrew J D ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Alternation; Amnesia; Direction; Fornix; Learning; Mammillary bodies; Memory; Navigation; Space; Thalamus

Indexed keywords

AMNESIA; ANIMAL BEHAVIOR; ANTERODORSAL NUCLEUS; ANTEROMEDIAL NUCLEUS; ANTEROVENTRAL NUCLEUS; BRAIN DYSFUNCTION; BRAIN FORNIX; BRAIN INJURY; BRAIN MAPPING; GENE EXPRESSION; HIPPOCAMPUS; IMMEDIATE EARLY GENE; MAMMILLARY BODY; MEMORY CONSOLIDATION; MORRIS WATER MAZE TEST; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; REUNIENS NUCLEUS; REVIEW; SPATIAL LEARNING; SPATIAL MEMORY; T-MAZE TEST; TASK PERFORMANCE; THALAMUS ANTERIOR NUCLEUS; THALAMUS NUCLEUS; WORKING MEMORY; ANIMAL; BRAIN CORTEX; HUMAN; MAZE TEST; METABOLISM; MOUSE; NERVE CELL NETWORK; NERVE TRACT; PATHOLOGY; PHYSIOLOGY; RAT;

PROTEIN C FOS;

ANIMALS; ANTERIOR THALAMIC NUCLEI; CEREBRAL CORTEX; HIPPOCAMPUS; HUMANS; MAZE LEARNING; MICE; NERVE NET; NEURAL PATHWAYS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; SPATIAL LEARNING; SPATIAL MEMORY;

EID: 84930622426     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2014.08.013     Document Type: Review

References (157)

1. Aggleton J.P., Sahgal A. The contribution of the anterior thalamic nuclei to anterograde amnesia. Neuropsychologia 1993, 31:1001-1019.
2. Aggleton J.P., Hunt P.R., Rawlins J.N. The effects of hippocampal lesions upon spatial and non-spatial tests of working memory. Behav. Brain Res. 1986, 19:133-146.
3. Aggleton J.P., Hunt P.R., Shaw C. The effects of mammillary body and combined amygdalar-fornix lesions on tests of delayed non-matching-to-sample in the rat. Behav. Brain Res. 1990, 15:145-157.
4. Aggleton J.P., Keith A.B., Sahgal A. Both fornix and anterior thalamic, but not mammillary, lesions disrupt delayed nonmatching-to-position memory in rats. Behav. Brain Res. 1991, 44:151-161.
5. Aggleton J.P., Neave N., Nagle S., Hunt P.R. A comparison of the effects of anterior thalamic, mamillary body and fornix lesions on reinforced spatial alternation. Behav. Brain Res. 1995, 68:91-101.
6. Aggleton J.P., Neave N., Nagle S., Sahgal A. A comparison of the effects of medial prefrontal, cingulate cortex, and cingulum bundle lesions on tests of spatial memory: evidence of a double dissociation between frontal and cingulum bundle contributions. J. Neurosci. 1995, 15:7270-7281.
7. Aggleton J.P., Hunt P.R., Nagle S., Neave N. The effects of selective lesions within the anterior thalamic nuclei on spatial memory in the rat. Behav. Brain Res. 1996, 81:189-198.
8. Aggleton J.P., Poirier G.L., Aggleton H.S., Vann S.D., Pearce J.M. Lesions of the fornix and anterior thalamic nuclei dissociate different aspects of hippocampal-dependent spatial learning: implications for the neural basis of scene learning. Behav. Neurosci. 2009, 123:504-519.
9. Aggleton J.P., O'Mara S.M., Vann S.D., Wright N.F., Tsanov M., Erichsen J.T. Hippocampal-anterior thalamic pathways for memory: uncovering a network of direct and indirect actions. Eur. J. Neurosci. 2010, 31:2292-2307.
10. Aggleton J.P., Brown M.W., Albasser M.M. Contrasting brain activity patterns for item recognition memory and associative recognition memory: insights from immediate-early gene functional imaging. Neuropsychologia 2012, 50:3141-3155.
11. Aggleton J.P. Understanding anterograde amnesia: disconnections and hidden lesions. Q. J. Exp. Psychol. 2008, 61:1441-1471.
12. Aggleton J.P. Understanding retrosplenial amnesia: insights from animal studies. Neuropsychologia 2010, 48:2328-2338.
13. Albo Z., Viana Di Prisco G., Vertes R.P. Anterior thalamic unit discharge profiles and coherence with hippocampal theta rhythm. Thal. Relat. Syst. 2003, 2:133-144.
14. Alexinsky T. Differential effect of thalamic and cortical lesions on memory systems in the rat. Behav. Brain Res. 2001, 122:175-191.
15. Amin E., Wright N., Poirier G.L., Thomas K.L., Erichsen J.T., Aggleton J.P. Selective lamina dysregulation in granular retrosplenial cortex (area 29) after anterior thalamic lesion: an in situ hybridization and trans-neuronal tracing study in rats. Neuroscience 2010, 169:1255-1267.
16. Baird A.L., Futter J.E., Muir J.L., Aggleton J.P. On the transience of egocentric working memory: evidence from testing the contribution of limbic brain regions. Behav. Neurosci. 2004, 118:785-797.
17. Bannerman D.M., Good M.A., Butcher S.P., Ramsay M., Morris R.G.M. Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature 1995, 378:182-186.
18. Bannerman D.M., Yee B.K., Good M.A., Heupel M.J., Iversen S.D., Rawlins J.N.P. Double dissociation of function within the hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behav. Neurosci. 1999, 113:1170-1188.
19. Beracochea D.J., Jaffard R. Impairment of spontaneous alternation behavior in sequential test procedures following mammillary body lesions in mice: evidence for time-dependent interference-related memory deficits. Behav. Neurosci. 1987, 101:187-197.
20. Beracochea D.J., Jaffard R. Effects of anterior thalamic lesions on spatial memory in mice. NeuroReport 1994, 5:917-920.
21. Beracochea D.J., Jaffard R., Jarrard L.E. Effects of anterior or dorsomedial thalamic ibotenic lesions on learning and memory in rats. Behav. Neural Biol. 1989, 51:364-376.
22. Bonaccorsi J., Cintoli S., Mastrogiacomo R., Baldanzi S., Braschi C., Pizzorusso T., Cenni M.C., Berardi N. System consolidation of spatial memories in mice: effects of enriched environment. Neural Plast. 2013, 10.1155/2013/956312.
23. Brito G.N., Thomas G.J., Davis B.J., Gingold S.I. Prelimbic cortex, mediodorsal thalamus, septum, and delayed alternation in rats. Exp. Brain Res. 1982, 46:52-58.
24. Bussey T.J., Duck J., Muir J.L., Aggleton J.P. Distinct pattern of behavioural impairments resulting from fornix transection or neurotoxic lesions of the perirhinal and postrhinal cortices in the rat. Behav. Brain Res. 2000, 111:187-202.
25. Byatt G., Dalrymple-Alford J.C. Both anteromedial and anteroventral thalamic lesions impair radial-maze learning in rats. Behav. Neurosci. 1996, 110:1335-1348.
26. Cain D.P., Boon F., Corcoran M.E. Thalamic and hippocampal mechanisms in spatial navigation: a dissociation between brain mechanisms for learning how versus learning where to navigate. Behav. Brain Res. 2006, 170:241-256.
27. Calton J.L., Stackman R.W., Goodridge J.P., Archery W.B., Dudchenko P.A., Taube J.S. Hippocampal place cell instability after lesions of the head direction cell network. J. Neurosci. 2003, 23:9719-9731.
28. Cassel J.-C., de Vasconcelos A.P., Loureiro M., Cholvin T., Dalrymple-Alford J.C., Vertes R.P. The reuniens and rhomboid nuclei: neuroanatomy, electrophysiological characteristics and behavioral implications. Prog. Neurobiol. 2013, 111:34-52.
29. Célérier A., Ognard R., Decorte L., Beracochea D. Deficits of spatial and non-spatial memory and of auditory fear conditioning following anterior thalamic lesions in mice: comparison with chronic alcohol consumption. Eur. J. Neurosci. 2000, 12:2575-2584.
30. Cho J., Sharp P.E. Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. Behav. Neurosci. 2001, 115:3-25.
31. Cross L., Aggleton J.P., Brown M.W., Warburton E.C. The medial dorsal thalamic nucleus and the medial prefrontal cortex of the rat function together to support associative but not item recognition. Learn. Mem. 2013, 20:41-50.
32. Davoodi F.G., Motamedi F., Naghdi N., Akbari E. Effect of reversible inactivation of the reuniens nucleus on spatial learning and memory in rats using Morris water maze task. Behav. Brain Res. 2009, 198:130-135.
33. Dember W.N., Fowler H. Spontaneous alternation behaviour. Psych. Bull. 1958, 55:412-428.
34. Dember W.N. Response by the rat to environmental change. J. Comp. Phys. Psychol. 1956, 49:93-95.
35. Deng W., Aimone J.B., Gage F.H. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nat. Rev. Neurosci. 2010, 11:339-350.
36. Dias R., Aggleton J.P. Effects of selective excitotoxic prefrontal lesions on acquisition of nonmatching- and matching-to-place in the T-maze: differential involvement of the prelimbic-infralimbic and anterior cingulate cortices in providing behavioural flexibility. Eur. J. Neurosci. 2000, 12:4457-4466.
37. Dolleman-van der Weel M.J., Morris R.G.M., Witter M.P. Neurotoxic lesions of the thalamic nucleus reuniens or mediodorsal nucleus in rats affect non-mnemonic aspects of watermaze training. Brain Struct. Funct. 2009, 213:329-342.
38. Domesick V.B. The fasculus cinguli in the rat. Brain Res. 1970, 20:19-32.
39. Douglas R.J. Cues for spontaneous alternation. J. Comp. Phys. Psychol. 1966, 62:171-183.
40. Dragunow M., Faull R. The use of c-fos as a metabolic marker in neuronal pathway tracing. J. Neurosci. Methods 1989, 29:261-265.
41. Dudchenko P.A., Wood E.R., Eichenbaum H. Neurotoxic hippocampal lesions have no effect on odor span and little effect on odor recognition memory but produce significant impairments on spatial span, recognition, and alternation. J. Neurosci. 2000, 20:2964-2977.
42. Dudchenko P.A. How do animals actually solve the T maze?. Behav. Neurosci. 2001, 115:850-860.
43. Dumont J.R., Aggleton J.P. Dissociation of recognition and recency memory judgments after anterior thalamic nuclei lesions in rats. Behav. Neurosci. 2013, 127:415-431.
44. Dumont J.R., Amin E., Poirier G.L., Albasser M.M., Aggleton J.P. Anterior thalamic nuclei lesions in rats disrupt markers of neural plasticity in distal limbic brain regions. Neuroscience 2012, 224:81-101.
45. Dumont J.R., Amin E., Aggleton J.P. Selective importance of the rat anterior thalamic nuclei for configural learning involving distal spatial cues. Eur. J. Neurosci. 2014, 39:241-256.
46. Dumont J.R., Wright N.F., Pearce J.M., Aggleton J.P. The impact of anterior thalamic lesions on active and passive spatial learning in stimulus controlled environments: geometric cues and pattern arrangement. Behav. Neurosci. 2014, 128:161-177.
47. Dupire A., Kant P., Mons N., Marchand A.R., Coutureau E., Dalrymple-Alford J., Wolff M. A role for anterior thalamic nuclei in affective cognition: interaction with environmental conditions. Hippocampus 2013, 23:392-404.
48. Encinas J.M., Hamani C., Lozano A.M., Enikolopov G. Neurogenic hippocampal targets of deep brain stimulation. J. Comp. Neurol. 2011, 519:6-20.
49. Frohardt R.J., Bassett J.P., Taube J.S. Path integration and lesions within the head direction cell circuit: comparison between the roles of the anterodorsal thalamus and dorsal tegmental nucleus. Behav. Neurosci. 2006, 120:135-149.
50. Futter J.E., Aggleton J.P. How rats perform spatial working memory tasks: limitations in the use of egocentric and idiothetic working memory. Q. J. Exp. Psychol. 2006, 59:77-99.
51. Garden D.L., Massey P.V., Caruana D.A., Johnson B., Warburton E.C., Aggleton J.P., Bashir Z.I. Anterior thalamic lesions stop synaptic plasticity in retrosplenial cortex slices: expanding the pathology of diencephalic amnesia. Brain 2009, 132:1847-1857.
52. Goodridge J.P., Taube J.S. Interaction between postsubiculum and anterior thalamus in the generation of head direction cell activity. J. Neurosci. 1997, 17:9315-9330.
53. Granon S., Poucet B. Involvement of the rat prefrontal cortex in cognitive functions: a central role for the prelimbic area. Psychobiology 2000, 28:229-237.
54. Greene E., Naranjo J.N. Thalamic role in spatial memory. Behav. Brain Res. 1986, 19:123-131.
55. Guzowski J.F., McGaugh J.L. Antisense oligooxynucleotide-mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:2693-2698.
56. Guzowski J.F., Setlow B., Wagner E.K., McGaugh J.L. Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J. Neurosci. 2001, 21:5089-5098.
57. Guzowski J.F. Insights into immediate-early gene function in hippocampal memory consolidation using antisense oligonucleotide and fluorescent imaging approaches. Hippocampus 2002, 12:86-104.
58. Hallock H.L., Wang A., Shaw C.L., Griffin A.L. Transient inactivation of the thalamic nucleus reuniens and rhomboid nucleus produces deficits of a working-memory dependent tactile-visual conditional discrimination task. Behav. Neurosci. 2013, 127:860-866.
59. Hamani C., Stone S.S., Garten A., Lozano A.M., Winocur G. Memory rescue and enhanced neurogenesis following electrical stimulation of the anterior thalamus in rats treated with corticosterone. Exp. Neurol. 2011, 232:100-104.
60. Hamilton D.A., Akers K.G., Weisnd M.P., Sutherland R.S. How do room and apparatus cues control navigation in the Morris water task? Evidence for distinct contributions to a movement vector. J. Exp. Psychol.: Anim. Behav. Proc. 2007, 33:100-114.
61. He J., Yamada K., Nabeshima T. A role of Fos expression in the CA3 region of the hippocampus in spatial memory formation in rats. Neuropsychopharmacology 2002, 26:259-268.
62. Hembrook J.R., Mair R.G. Lesions of reuniens and rhomboid thalamic nuclei impair radial maze win-shift performance. Hippocampus 2011, 21:815-826.
63. Herdegen T., Leah J.F. Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res. Brain Res. Rev. 1998, 28:370-490.
64. Hindley E.L., Nelson A.J.D., Aggleton J.P., Vann S.D. The rat retrosplenial cortex is required when visual cues are used flexibly to determine location. Behav. Brain Res. 2014, 263:98-107.
65. Horne M.R., Gilroy K.E., Cuell S.F., Pearce J.M. Latent spatial learning in an environment with a distinctive shape. J. Exp. Psychol.: Anim. Behav. Proc. 2012, 38:139-147.
66. Hunt P.R., Aggleton J.P. Medial dorsal thalamic lesions and working memory in the rat. Behav. Neural. Biol. 1991, 55:227-246.
67. Hunt P.R., Aggleton J.P. Neurotoxic lesions of the dorsomedial thalamus impair the acquisition but not the performance of delayed matching to place by rats: a deficit in shifting response rules. J. Neurosci. 1998, 18:10045-10052.
68. Jankowski M.M., Ronnqvist K.C., Vann S.D., Wright N.F., Erichsen J.T., Aggleton J.P., O'Mara S.M. The anterior thalamus provides a subcortical circuit supporting memory and spatial navigation. Front. Syst. Neurosci. 2013, 7:10. (3389/fnsys.2013.00045 file).
69. Jankowski M.M., Islam M.N., Wright N.F., Vann S.D., Erichsen J.T., Aggleton J.P., O'Mara S.M. Nucleus reuniens of the thalamus contains head direction cells. ELife 2014, 1-10. 10.7554/elLife.03075.
70. Jenkins T.A., Dias R., Amin E., Brown M.W., Aggleton J.P. Fos imaging reveals that lesions of the anterior thalamic nuclei produce widespread limbic hypoactivity in rats. J. Neurosci. 2002, 22:5230-5238.
71. Jenkins T.A., Dias R., Amin E., Aggleton J.P. Changes in Fos expression in the rat brain after unilateral lesions of the anterior thalamic nuclei. Eur. J. Neurosci. 2002, 16:1425-1432.
72. Jenkins T.A., Amin E., Pearce J.M., Brown M.W., Aggleton J.P. Novel spatial arrangements of familiar stimuli promote activity in the rat hippocampal formation but not the parahippocampal cortices; a c-fos expression study. Neuroscience 2004, 124:43-52.
73. Jenkins T.A., Vann S.D., Amin E., Aggleton J.P. Anterior thalamic lesions stop immediate early gene activation in selective laminae of the retrosplenial cortex: evidence of covert pathology in rats?. Eur. J. Neurosci. 2004, 19:3291-3304.
74. Kivy P., Earl R.W., Walker E.L. Stimulus context and satiation. J. Comp. Phys. Psychol. 1956, 49:90-92.
75. Kubik S., Miyashita T., Guzowski J.F. Using immediate-early genes to map hippocampal subregional functions. Learn. Mem. 2007, 14:758-770.
76. Kuramoto S., Yasuhara T., Agari T., Kondo A., Matsui T., Miyoshi Y., Shingo T., Date I. Injection of muscimol, a GABAa agonist into the anterior thalamic nucleus, suppresses hippocampal neurogenesis in amygdala-kindled rats. Neurol. Res. 2009, 31:407-413.
77. Lalonde R. The neurobiological basis of spontaneous alternation. Neurosci. Biobehav. Rev. 2002, 26:91-104.
78. Leger M., Quiedeville A., Paizanis E., Natkunarajah S., Freret T., Boulouard M., Schumann-Bard P. Environmental enrichment enhances episodic-like memory in association with a modified neuronal activation profile in adult mice. PLoS One 2012, 10.1371/journal.pone.0048043.
79. Loukavenko E.A., Ottley M.C., Moran J.P., Wolff M., Dalrymple-Alford J.C. Towards therapy to relieve memory impairment after anterior thalamic lesions: improved spatial working memory after immediate and delayed postoperative enrichment. Eur. J. Neurosci. 2007, 26:3267-3276.
80. Loureiro M., Cholvin T., Lopez J., Merienne N., Latreche A., Cosquer B., Geiger K., Kelche C., Cassel J.-C., de Vasconcelos A.P. The ventral midline thalamus (reuniens and rhomboid nuclei) contributes to the persistence of spatial memory in rats. J. Neurosci. 2012, 32:9947-9959.
81. M'Harzi M., Collery M., Delacour J. First evidence of a possible role of the reticular thalamic nucleus in working memory in rats. Neurosci. Res. Comm. 1991, 8:167-174.
82. Mair R.G., Burk J.A., Porter M.C. Impairment of radial maze delayed nonmatching after lesions of anterior thalamus and parahippocampal cortex. Behav. Neurosci. 2003, 117:596-605.
83. McGregor A., Hayward A.J., Pearce J.M., Good M.A. Hippocampal lesions disrupt navigation based on the shape of the environment. Behav. Neurosci. 2004, 118:1011-1021.
84. Mendez-Lopez M., Arias J.L., Bontempi B., Wolff M. Reduced cytochrome oxidase activity in the retrosplenial cortex after lesions to the anterior thalamic nuclei. Behav. Brain Res. 2013, 250:264-273.
85. Mitchell A.S., Dalrymple-Alford J.C. Dissociable memory effects after medial thalamus lesions in the rat. Eur. J. Neurosci. 2005, 22:973-985.
86. Mitchell A.S., Dalrymple-Alford J.C. Lateral and anterior thalamic lesions impair independent memory systems. Learn. Mem. 2006, 13:388-396.
87. Mizumori S.J., Cooper B.G., Leutgeb S., Pratt W.E. A neural systems analysis of adaptive navigation. Mol. Neurobiol. 2000, 21:57-82.
88. Mizuno M., Yamada K., Maekawa K., Saito M., Seishima M., Nabeshima T. CREB phosphorylation as a molecular marker of memory processing in the hippocampus for spatial learning. Behav. Brain Res. 2002, 133:135-141.
89. Moreau P.-H., Tsenkina Y., Lecourtier L., Lopez J., Cosquer B., Wolff M., Dalrymple-Alford J., Cassel J.-C. Lesions of the anterior thalamic nuclei and intralaminar thalamic nuclei: place and visual discrimination learning in the water maze. Brain Struct. Funct. 2013, 218:657-667.
90. Moser E.I., Kropff E., Moser M.-B. Place cells, grid cells, and the brain's spatial representation system. Ann. Rev. Neurosci. 2008, 31:69-89.
91. Mufson E.J., Pandya D.N. Some observations on the course and composition of the cingulum bundle in the rhesus monkey. J. Comp. Neurol. 1984, 225:31-43.
92. Nagahara A.H., Handa R.J. Fetal alcohol exposure alters the induction of immediate early gene mRNA in the rat prefrontal cortex after an alternation task. Alcohol. Clin. Exp. Res. 1995, 19:1389-1397.
93. Neave N., Lloyd S., Sahgal A., Aggleton J.P. Lack of effect of lesions in the anterior cingulate cortex and retrosplenial cortex on certain tests of spatial memory in the rat. Behav. Brain Res. 1994, 65:89-101.
94. Neave N., Nagle S., Aggleton J.P. Evidence for the involvement of the mamillary bodies and cingulum bundle in allocentric spatial processing by rats. Eur. J. Neurosci. 1997, 9:941-955.
95. Nelson A., Hindley E., Haddon J., Aggleton J.P., Vann S.D. A novel role for the rat retrosplenial cortex in cognitive control. Learn. Mem. 2014, 21:90-97.
96. Olton D.S., Becker J.T., Handelmann G.E. Hippocampus, space and memory. Behav. Brain Sci. 1979, 2:313-365.
97. Packard M.G., McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol. Learn. Mem. 1996, 65:65-72.
98. Pearce J.M., Roberts A.D.L., Good M. Hippocampal lesions disrupt navigation based on cognitive maps but not heading vectors. Nature 1998, 396:75-77.
99. Poirier G.L., Aggleton J.P. Post-surgical interval and lesion location within limbic thalamus determine extent of retrosplenial cortex immediate-early gene hypoactivity. Neuroscience 2009, 162:452-469.
100. Poirier G.L., Shires K.L., Sugden D., Amin E., Thomas K.L., Carter D.A., Aggleton J.P. Anterior thalamic lesions produce chronic and profuse transcriptional de-regulation in retrosplenial cortex: a model of retrosplenial hypoactivity and covert pathology. Thalamus Relat. Syst. 2008, 4:59-77.
101. Pothuizen H.H., Aggleton J.P., Vann S.D. Do rats with retrosplenial cortex lesions lack direction. Eur. J. Neurosci. 2008, 28:2486-2498.
102. Pothuizen H.H., Davies M., Albasser M.M., Aggleton J.P., Vann S.D. Granular and dysgranular retrosplenial cortices provide qualitatively different contributions to spatial working memory: evidence from immediate-early gene imaging in rats. Eur. J. Neurosci. 2009, 30:877-888.
103. Prasad J.A., Chudasama Y. Viral tracing identifies parallel disynapatic pathways to the hippocampus. J. Neurosci. 2013, 33:8494-8503.
104. Ragozzino M.E., Detrick S., Kesner R.P. Involvement of the prelimbic-infralimbic areas of the rodent prefrontal cortex in behavioral flexibility for places and response learning. J. Neurosci. 1999, 19:4585-4594.
105. Rampon C., Jiang C.H., Dong H., Tang Y.P., Lockhart D.J., Schultz P.G., Tsien J.Z., Hu Y. Effects of environmental enrichment on gene expression in the brain. Proc. Natl. Acad. Sci. 2000, 97:12880-12884.
106. Rutishauser U., Ross I.B., Mamelak A.N., Schuman E.M. Human memory strength is predicted by theta-frequency phase-locking of single neurons. Proc. Natl. Acad. Sci. 2010, 468:903-907.
107. Sánchez-Santed F., de Bruin J.P., Heinsbroek R.P., Verwer R.W. Spatial delayed alternation of rats in a T-maze: effects of neurotoxic lesions of the medial prefrontal cortex and of T-maze rotations. Behav. Brain Res. 1997, 84:73-79.
108. Sharp P.E., Koester K. Lesions of the mammillary body region severely disrupt the cortical head direction, but not place cell signal. Hippocampus 2008, 18:766-784.
109. Shaw C., Aggleton J.P. The effects of fornix and medial prefrontal lesions on delayed non-matching-to-sample by rats. Behav. Brain Res. 1993, 54:91-102.
110. Silva A.J., Kogan J.H., Frankland P.W., Kida S. CREB and memory. Ann. Rev. Neurosci. 1998, 21:127-148.
111. Still A., Macmillan A. Odor trail and spontaneous alternation. Psychon. Sci. 1969, 16:160-161.
112. Sutherland R.J., Rodriguez A.J. The role of the fornix/fimbria and some related subcortical structures in place learning and memory. Behav. Brain Res. 1989, 32:265-277.
113. Swanson L.W., Cowan W.M. An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J. Comp. Neurol. 1977, 172:49-84.
114. Sziklas V., Petrides M. The effects of lesions to the anterior thalamic nuclei on object-place associations in rats. Eur. J. Neurosci. 1999, 11:559-566.
115. Taube J.S. Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J. Neurosci. 1995, 15:70-86.
116. Taube J.S. The head direction signal: origins and sensory-motor integration. Ann. Rev. Neurosci. 2007, 30:181-207.
117. Tischmeyer W., Grimm R. Activation of immediate early genes and memory formation. Cell Mol. Life Sci. 1999, 55:564-574.
118. Toda H., Hamani C., Fawcett A.P., Hutchison W.D., Lozano A.M. The regulation of adult hippocampal neurogenesis by deep brain stimulation. J. Neurosurg. 2008, 108:132-138.
119. Tsanov M., Chah E., Vann S.D., Reilly R., Erichsen J.T., Aggleton J.P., O'Mara S.M. Theta-modulated head-direction cells in the rat anterior thalamus. J. Neurosci. 2011, 31:9489-9502.
120. Tsanov M., Wright N., Vann S.D., Erichsen J., Aggleton J.P., O'Mara S.M. Differential regulation of synaptic plasticity of the hippocampal and the hypothalamic inputs to the anterior thalamus. Hippocampus 2011, 21:1-8.
121. Tsanov M., Wright N., Vann S.D., Erichsen J.T., Aggleton J.P., O'Mara S.M. Hippocampal inputs mediate theta-related plasticity in anterior thalamus. Neuroscience 2011, 187:52-62.
122. Van Groen T., Wyss J. Connections of the retrosplenial dysgranular cortex in the rat. J. Comp. Neurol. 1992, 315:200-216.
123. Van Groen T., Wyss J. Projections from the laterdorsal nucleus of the thalamus to the limbic and visual cortices in the rat. J. Comp. Neurol. 1992, 324:427-448.
124. Van Groen T., Wyss J. Connections of the retrosplenial granular b cortex in the rat. J. Comp. Neurol. 2003, 463:249-263.
125. Van Groen T., Vogt B.A., Wyss J.M. Interconnections between the thalamus and retrosplenial cortex in the rodent brain. Neurobiology of Cingulate Cortex and Limbic Thalamus: A Comprehensive Handbook 1993, 123-150. Birkhäuser, Boston. B.A. Vogt, M. Gabriel (Eds.).
126. Van Groen T., Kadish I., Wyss J. Role of the anterodorsal and anteroventral nuclei of the thalamus in spatial memory in the rat. Behav. Brain Res. 2002, 132:19-28.
127. Van Groen T., Kadish I., Wyss J. The role of the laterodorsal nucleus of the thalamus in spatial learning and memory in the rat. Behav. Brain Res. 2002, 136:329-337.
128. Vann S.D., Aggleton J.P. Extensive cytotoxic lesions of the rat retrosplenial cortex reveal consistent deficits on tasks that tax allocentric spatial memory. Behav. Neurosci 2002, 116:85-94.
129. Vann S.D., Aggleton J.P. Evidence of a spatial encoding deficit with lesions of the mammillary bodies or mammillothalamic tract. J. Neurosci. 2003, 23:3506-3514.
130. Vann S.D., Albasser M.M. Hippocampal, retrosplenial and prefrontal hypoactivity in a model of diencephalic amnesia: evidence towards an interdependent subcortical-cortical memory network. Hippocampus 2009, 19:1090-1102.
131. Vann S.D., Brown M., Aggleton J.P. Fos expression in the rostral thalamic nuclei and associated cortical regions in response to different spatial memory tasks. Neuroscience 2000, 101:983-991.
132. Vann S.D., Brown M.W., Erichsen J.T., Aggleton J.P. Fos imaging reveals differential patterns of hippocampal and parahippocampal subfield activity in response to different spatial memory tasks. J. Neurosci. 2000, 20:2711-2718.
133. Vann S.D., Wilton L.A.K., Muir J.L., Aggleton J.P. Testing the importance of the caudal retrosplenial cortex for spatial memory in rats. Behav. Brain Res. 2003, 140:107-118.
134. Vann S.D., Aggleton J.P., Maguire E.A. What does the retrosplenial cortex do?. Nat. Rev. Neurosci. 2009, 10:792-802.
135. Vann S.D., O'Mara S., Erichsen J.T., Aggleton J.P. Selective disconnection of the hippocampal formation projections to the mammillary bodies produces only mild deficits on spatial memory tasks: implications for fornix function. Hippocampus 2011, 21:945-957.
136. Vann S.D. Transient spatial deficit associated with bilateral lesions of the lateral mammillary nuclei. Eur. J. Neurosci. 2005, 21:820-824.
137. Vann S.D. Gudden's ventral tegmental nucleus is vital for memory: re-evaluating diencephalic inputs for amnesia. Brain 2009, 132:2372-2384.
138. Vann S.D. Re-evaluating the role of the mammillary bodies in memory. Neuropsychologia 2010, 48:2316-2327.
139. Vann S.D. A role for the head-direction system in geometric learning. Behav. Brain Res. 2011, 224:201-206.
140. Vann S.D. Dismantling the Papez circuit for memory in rats. Elife 2013, 10.7554/eLife.00736.
141. Vertes R.P., Albo Z., Viana Di Prisco G. Theta-rhythmically firing neurons in the anterior thalamus: implications for mnemonic functions of Papez's circuit. Neuroscience 2001, 104:619-625.
142. Vertes R.P., Hoover W.B., Viana Di Prisco G. Theta rhythm of the hippocampus: subcortical control and functional significance. Behav. Cogn. Neurosci. Rev. 2004, 3:173-200.
143. Vertes R.P., Hoover W.B., Do Valle A.C., Sherman A., Rodriguez J.J. Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat. J. Comp. Neurol. 2006, 499:768-796.
144. Warburton E.C., Aggleton J.P. Differential deficits in the Morris water maze following cytotoxic lesions of the anterior thalamus and fornix transection. Behav. Brain Res. 1999, 98:27-38.
145. Warburton E.C., Baird A.L., Aggleton J.P. Assessing the magnitude of the allocentric spatial deficit associated with complete loss of the anterior thalamic nuclei in rats. Behav. Brain Res. 1997, 87:223-232.
146. Warburton E.C., Aggleton J.P., Muir J.L. Comparing the effects of selective cingulate cortex and cingulum bundle lesions on a spatial navigation task. Eur. J. Neurosci. 1998, 10:622-634.
147. Warburton E.C., Morgan A., Baird A.L., Muir J.L., Aggleton J.P. Does pretraining spare the spatial deficit associated with anterior thalamic damage in rats?. Behav. Neurosci. 1999, 113:956-967.
148. Warburton E.C., Baird A.L., Morgan A., Muir J.L., Aggleton J.P. Disconnecting hippocampal projections to the anterior thalamus produces deficits on tests of spatial memory in rats. Eur. J. Neurosci. 2000, 12:1714-1726.
149. Warburton E.C., Morgan A., Baird A., Muir J.L., Aggleton J.P. The conjoint importance of the hippocampus and anterior thalamic nuclei for allocentric spatial learning: evidence from a disconnection study in the rat. J. Neurosci. 2001, 21:7323-7330.
150. Whishaw I.Q., Cassel J.-C., Jarrard L.E. Rats with fimbria-fornix lesions display a place response in a swimming pool: a dissociation between getting there and knowing where. J. Neurosci. 1995, 15:5779-5788.
151. Wilton L.A.K., Baird A.L., Muir J.L., Aggleton J.P. Excitotoxic lesions of the rostral thalamic reticular nucleus do not affect the performance of spatial learning and memory tasks in the rat. Behav. Brain Res. 2001, 120:177-187.
152. Wilton L.A., Baird A.L., Muir J.L., Honey R.C., Aggleton J.P. Loss of the thalamic nuclei for "head direction" impairs performance on spatial memory tasks in rats. Behav. Neurosci. 2001, 115:689-861.
153. Wolff M., Gibb S.J., Dalrymple-Alford J.C. Beyond spatial memory: the anterior thalamus and memory for the temporal order of a sequence of odour cues. J. Neurosci. 2006, 26:2907-2913.
154. Wolff M., Gibb S.J., Cassel J.-C., Dalrymple-Alford J.C. Anterior but not intralaminar thalamic nuclei support allocentric spatial memory. Neurobiol. Learn. Mem. 2008, 90:71-80.
155. Wolff M., Loukavenko E.A., Will B.E., Dalrymple-Alford J.C. The extended hippocampal-diencephalic memory system: enriched housing promotes recovery of the flexible use of spatial representations after anterior thalamic lesions. Hippocampus 2008, 18:996-1007.
156. Wood E.R., Dudchenko P.A., Robitsek R.J., Eichenbaum H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 2000, 27:623-633.
157. Wright N.F., Vann S.D., Erichsen J.T., O'Mara S., Aggleton J.P. Segregation of parallel inputs to the anteromedial and anteroventral thalamic nuclei of the rat. J. Comp. Neurol. 2013, 521:2966-2986.