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Lesions of the anterior thalamic nuclei and intralaminar thalamic nuclei: place and visual discrimination learning in the water maze

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Abstract

Medial thalamic damage produces memory deficits in humans (e.g., Korsakoff’s syndrome) and experimental animals. Both the anterior thalamic nuclei (ATN) and rostral intralaminar plus adjacent lateral thalamic nuclei (ILN/LT) have been implicated. Based on the differences in their main connections with other neural structures, we tested the prediction that ATN lesions would selectively impair acquisition of spatial location discrimination, reflecting a hippocampal system deficit, whereas ILN/LT lesions would impair acquisition of visual pattern discrimination, reflecting a striatal system deficit. Half the rats were first trained in a spatial task in a water maze before switching to a visual task in the same maze, while the remainder were tested with the reverse order of tasks. Compared with sham-operated controls, (1) rats with ATN lesions showed impaired place learning, but normal visual discrimination learning, (2) rats with ILN/LT lesions showed no deficit on either task. Rats with ATN lesions were also hyperactive when their home cage was placed in a novel room and remained more active than ILN/LT or SHAM rats for the subsequent 21 h, especially during the nocturnal phase. These findings confirmed the influence of ATN lesions on spatial learning, but failed to support the view that ILN/LT lesions disrupt striatal-dependent memory.

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References

  • Aggleton JP (2008) Understanding anterograde amnesia: disconnections and hidden lesions. Q J Exp Psychol 61:1441–1471

    Article  Google Scholar 

  • Aggleton JP, Brown MW (1999) Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav Brain Sci 22(3):425–444

    PubMed  CAS  Google Scholar 

  • Aggleton JP, Dumont JR, Warburton EC (2011) Unraveling the contributions of the diencephalon to recognition memory: a review. Learn Mem 18(6):384–400

    Article  PubMed  Google Scholar 

  • Aggleton JP, Poirier GL, Aggleton HS, Vann SD, Pearce JM (2009) 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 123(3):504–519

    Article  PubMed  Google Scholar 

  • Anzalone S, Vetreno RP, Ramos RL, Savage LM (2010) Cortical cholinergic abnormalities contribute to the amnesic state induced by pyrithiamine-induced thiamine deficiency in the rat. Eur J Neurosci 32(5):847–858

    Article  PubMed  Google Scholar 

  • Bailey KR, Mair RG (2004) Dissociable effects of frontal cortical lesions on measures of visuospatial attention and spatial working memory in the rat. Cereb Cortex 14(9):974–985

    Article  PubMed  CAS  Google Scholar 

  • Bailey KR, Mair RG (2005) Lesions of specific and nonspecific thalamic nuclei affect prefrontal cortex-dependent aspects of spatial working memory. Behav Neurosci 119(2):410–419

    Article  PubMed  Google Scholar 

  • Bailey KR, Mair RG (2006) The role of striatum in initiation and execution of learned action sequences in rats. J Neurosci 26(3):1016–1025

    Article  PubMed  CAS  Google Scholar 

  • Bailey KR, Mair RG (2007) Effects of frontal cortex lesions on action sequence learning in the rat. Eur J Neurosci 25(9):2905–2915

    Article  PubMed  Google Scholar 

  • Berendse HW, Groenewegen HJ (1991) Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat. Neuroscience 42(1):73–102

    Article  PubMed  CAS  Google Scholar 

  • Byatt G, Dalrymple-Alford JC (1996) Both anteromedial and anteroventral thalamic lesions impair radial-maze learning in rats. Behav Neurosci 110(6):1335–1348

    Article  PubMed  CAS  Google Scholar 

  • Cassel JC, Cassel S, Galani R, Kelche C, Will B, Jarrard L (1998) Fimbria-fornix vs selective hippocampal lesions in rats: effects on locomotor activity and spatial learning and memory. Neurobiol Learn Mem 69(1):22–45

    Article  PubMed  CAS  Google Scholar 

  • Cook D, Kesner RP (1988) Caudate nucleus and memory for egocentric localization. Behav Neural Biol 49(3):332–343

    Article  PubMed  CAS  Google Scholar 

  • DeCoteau WE, Kesner RP (2000) A double dissociation between the rat hippocampus and medial caudoputamen in processing two forms of knowledge. Behav Neurosci 114(6):1096–1108

    Article  PubMed  CAS  Google Scholar 

  • Galani R, Duconseille E, Bildstein O, Cassel JC (2001) Effects of room and cage familiarity on locomotor activity measures in rats. Physiol Behav 74(1–2):1–4

    Article  PubMed  CAS  Google Scholar 

  • Galani R, Jarrard LE, Will BE, Kelche C (1997) Effects of postoperative housing conditions on functional recovery in rats with lesions of the hippocampus, subiculum, or entorhinal cortex. Neurobiol Learn Mem 67(1):43–56

    Article  PubMed  CAS  Google Scholar 

  • Gibb SJ, Wolff M, Dalrymple-Alford JC (2006) Odour-place paired-associate learning and limbic thalamus: comparison of anterior, lateral and medial thalamic lesions. Behav Brain Res 172(1):155–168

    Article  PubMed  Google Scholar 

  • Gold JJ, Squire LR (2006) The anatomy of amnesia: neurohistological analysis of three new cases. Learn Mem 13(6):699–710

    Article  PubMed  Google Scholar 

  • Harding A, Halliday G, Caine D, Kril J (2000) Degeneration of anterior thalamic nuclei differentiates alcoholics with amnesia. Brain 123:141–154

    Article  PubMed  Google Scholar 

  • Harrison LM, Mair RG (1996) A comparison of the effects of frontal cortical and thalamic lesions on measures of spatial learning and memory in the rat. Behav Brain Res 75(1–2):195–206

    Article  PubMed  CAS  Google Scholar 

  • Hembrook JR, Mair RG (2011) Lesions of reuniens and rhomboid thalamic nuclei impair radial maze win-shift performance. Hippocampus 21(8):815–826

    PubMed  Google Scholar 

  • Jodar M, Martos P, Fernández S, Canovas D, Rovira A (2011) Neuropsychological profile of bilateral paramedian infarctions: three cases. Neurocase 17(4):345–352

    Article  PubMed  CAS  Google Scholar 

  • Kato S, Kuramochi M, Kobayashi K, Fukabori R, Okada K, Uchigashima M, Watanabe M, Tsutsui Y, Kobayashi K (2011) Selective neural pathway targeting reveals key roles of thalamostriatal projection in the control of visual discrimination. J Neurosci 31(47):17169–17179

    Article  PubMed  CAS  Google Scholar 

  • Kesner RP (2000) Behavioral analysis of the contribution of the hippocampus and parietal cortex to the processing of information: interactions and dissociations. Hippocampus 10(4):483–490

    Article  PubMed  CAS  Google Scholar 

  • Kesner RP, Bolland BL, Dakis M (1993) Memory for spatial locations, motor responses, and objects: triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex. Exp Brain Res 93(3):462–470

    Article  PubMed  CAS  Google Scholar 

  • Koger SM, Mair RG (1994) Comparison of the effects of frontal cortical and thalamic lesions on measures of olfactory learning and memory in the rat. Behav Neurosci 108(6):1088–1100

    Article  PubMed  CAS  Google Scholar 

  • Kopelman MD (2002) Disorders of memory. Brain 125:2152–2190

    Article  PubMed  Google Scholar 

  • Lehmann O, Bertrand F, Jeltsch H, Morer M, Lazarus C, Will B, Cassel JC (2002) 5,7-DHT-induced hippocampal 5-HTdepletion attenuates behavioural deficits produced by 192 IgG-saporin lesions of septal cholinergic neurons in the rat. Eur J Neurosci 15:1991–2006

    Article  PubMed  Google Scholar 

  • Lopez J, Wolff M, Lecourtier L, Cosquer B, Bontempi B, Dalrymple-Alford J, Cassel JC (2009) The intralaminar thalamic nuclei contribute to remote spatial memory. J Neurosci 29(10):3302–3306

    Article  PubMed  CAS  Google Scholar 

  • Loureiro M, Lecourtier L, Engeln M, Lopez J, Cosquer B, Geiger K, Kelche C, Cassel JC, Pereira de Vasconcelos A (2011) The ventral hippocampus is necessary for expressing a spatial memory. Brain Struct Funct (Epub ahead of print)

  • Mair RG, Anderson CD, Langlais PJ, McEntee WJ (1988) Behavioral impairments, brain lesions and monoaminergic activity in the rat following recovery from a bout of thiamine deficiency. Behav Brain Res 27(3):223–239

    Article  PubMed  CAS  Google Scholar 

  • Mair RG, Burk JA, Porter MC (1998) Lesions of the frontal cortex, hippocampus, and intralaminar thalamic nuclei have distinct effects on remembering in rats. Behav Neurosci 112(4):772–792

    Article  PubMed  CAS  Google Scholar 

  • Mair RG, Burk JA, Porter MC (2003) Impairment of radial maze delayed nonmatching after lesions of anterior thalamus and parahippocampal cortex. Behav Neurosci 117(3):596–605

    Article  PubMed  Google Scholar 

  • Mair RG, Koch JK, Newman JB, Howard JR, Burk JA (2002) A double dissociation within striatum between serial reaction time and radial maze delayed nonmatching performance in rats. J Neurosci 22(15):6756–6765

    PubMed  CAS  Google Scholar 

  • Mair RG, Onos KD, Hembrook JR (2011) Cognitive activation by central thalamic stimulation: the Yerkes–Dodson law revisited. Dose Response 9(3):313–331

    Article  PubMed  CAS  Google Scholar 

  • McDonald RJ, White NM (1993) A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behav Neurosci 107(1):3–22

    Article  PubMed  CAS  Google Scholar 

  • McDonald RJ, White NM (1994) Parallel information processing in the water maze evidence for independent memory systems involving dorsal striatum and hippocampus. Behav Neural Biol 61(3):260–270

    Article  PubMed  CAS  Google Scholar 

  • Mena-Segovia J, Cintra L, Prospero-Garcia O, Giordano M (2002) Changes in sleep-waking cycle after striatal excitotoxic lesions. Behav Brain Res 136(2):475–481

    Article  PubMed  Google Scholar 

  • Mitchell AS, Dalrymple-Alford JC (2005) Dissociable memory effects after medial thalamus lesions in the rat. Eur J Neurosci 22(4):973–985

    Article  PubMed  Google Scholar 

  • Mitchell AS, Dalrymple-Alford JC (2006) Lateral and anterior thalamic lesions impair independent memory systems. Learn Mem 13(3):388–396

    Article  PubMed  Google Scholar 

  • Mitchell JA, Hall G (1988) Caudate-putamen lesions in the rat may impair or potentiate maze learning depending upon availability of stimulus cues and relevance of response cues. Q J Exp Psychol 40B(3):243–258

    Google Scholar 

  • Moran JP, Dalrymple-Alford JC (2003) Perirhinal cortex and anterior thalamic lesions: comparative effects on learning and memory. Behav Neurosci 117(6):1326–1341

    Article  PubMed  Google Scholar 

  • Oscar-Berman M, Zola-Morgan SM (1980) Comparative neuropsychology and Korsakoff’s syndrome. I. Spatial and visual reversal learning. Neuropsychologia 18(4–5):499–512

    Article  PubMed  CAS  Google Scholar 

  • Packard MG, McGaugh JL (1992) Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: further evidence for multiple memory systems. Behav Neurosci 106(3):439–446

    Article  PubMed  CAS  Google Scholar 

  • Packard MG, Teather LA (1998) Amygdala modulation of multiple memory systems: hippocampus and caudate-putamen. Neurobiol Learn Mem 69(2):163–203

    Article  PubMed  CAS  Google Scholar 

  • Parent MB, Baxter MG (2004) Septohippocampal acetylcholine: involved in but not necessary for learning and memory? Learn Mem 11:87–94

    Article  Google Scholar 

  • Paxinos G, Watson P (1998) The rat brain in stereotaxis coordinates. Academic Press, New York

    Google Scholar 

  • Savage LM, Castillo R, Langlais PJ (1998) Effects of lesions of thalamic intralaminar and midline nuclei and internal medullary lamina on spatial memory and object discrimination. Behav Neurosci 112(6):1339–1352

    Article  PubMed  CAS  Google Scholar 

  • Savage LM, Roland J, Klintsova A (2007) Selective septohippocampal—but not forebrain amygdalar—cholinergic dysfunction in diencephalic amnesia. Brain Res 1139:210–219

    Article  PubMed  CAS  Google Scholar 

  • Sziklas V, Petrides M (1999) The effects of lesions to the anterior thalamic nuclei on object-place associations in rats. Eur J Neurosci 11(2):559–566

    Article  PubMed  CAS  Google Scholar 

  • Sziklas V, Petrides M (2007) Contribution of the anterior thalamic nuclei to conditional learning in rats. Hippocampus 17:456–461

    Article  PubMed  CAS  Google Scholar 

  • van der Werf YD, Jolles J, Witter MP, Uylings HB (2003) Contributions of thalamic nuclei to declarative memory functioning. Cortex 39(4–5):1047–1062

    PubMed  Google Scholar 

  • van der Werf YD, Witter MP, Groenewegen HJ (2002) The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Rev 39:107–140

    Article  PubMed  Google Scholar 

  • van der Werf YD, Witter MP, Uylings HB, Jolles J (2000) Neuropsychology of infarctions in the thalamus: a review. Neuropsychologia 38(5):613–627

    Article  PubMed  Google Scholar 

  • Vann SD, Albasser MM (2009) Hippocampal, retrosplenial, and prefrontal hypoactivity in a model of diencephalic amnesia: evidence towards an interdependent subcortical–cortical memory network. Hippocampus 19:1090–1102

    Article  PubMed  Google Scholar 

  • Warburton EC, Baird AL, Morgan A, Muir JL, Aggleton JP (2001) The conjoint importance of the hippocampus and anterior thalamic nuclei for allocentric spatial learning: evidence from a disconnection study in the rat. J Neurosci 21:7323–7330

    PubMed  CAS  Google Scholar 

  • White NM, McDonald RJ (2002) Multiple parallel memory systems in the brain of the rat. Neurobiol Learn Mem 77:125–184

    Article  PubMed  Google Scholar 

  • Wilkinson LS, Mittleman G, Torres E, Humby T, Hall FS, Robbins TW (1993) Enhancement of amphetamine-induced locomotor activity and dopamine release in nucleus accumbens following excitotoxic lesions of the hippocampus. Behav Brain Res 55:143–150

    Article  PubMed  CAS  Google Scholar 

  • Winer BJ (1971) Statistical principles in experimental design, 2nd edn. McGraw-Hill, New York

    Google Scholar 

  • Wolff M, Gibb SJ, Dalrymple-Alford JC (2006) Beyond spatial memory: the anterior thalamus and memory for the temporal order of a sequence of odor cues. J Neurosci 26(11):2907–2913

    Article  PubMed  CAS  Google Scholar 

  • Wolff M, Gibb SJ, Cassel JC, Dalrymple-Alford JC (2008a) Anterior but not intralaminar thalamic nuclei support allocentric spatial memory. Neurobiol Learn Mem 90(1):71–80

    Article  PubMed  Google Scholar 

  • Wolff M, Loukavenko EA, Will BE, Dalrymple-Alford JC (2008b) The extended hippocampal–diencephalic memory system: enriched housing promotes recovery of the flexible use of spatial representations after anterior thalamic lesions. Hippocampus 18:996–1007

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors are grateful to O. Bildstein, G. Edomwony and O. Egesi for their help in animal care. They also acknowledge research funds from the University of Strasbourg and the CNRS. J.C.D-A. has been supported during his stay in Strasbourg as an invited professor by University of Strasbourg. M.W. was supported by a Lavoisier post-doctoral fellowship from the French Government (when he was at Christchurch) and a 1-year fellowship by the Fondation pour la Recherche Médicale. A 3-year PhD fellowship was awarded to J.L. from the French Ministère de l’Enseignement Supérieur et de la Recherche. Finally, L.L. contributed to the current work while being a post-doctoral fellow supported by the French A.N.R. (ANR-06-NEURO-027-04).

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Correspondence to Jean-Christophe Cassel.

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P.-H. Moreau and Y. Tsenkina contributed equally to the work.

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Moreau, PH., Tsenkina, Y., Lecourtier, L. et al. Lesions of the anterior thalamic nuclei and intralaminar thalamic nuclei: place and visual discrimination learning in the water maze. Brain Struct Funct 218, 657–667 (2013). https://doi.org/10.1007/s00429-012-0419-0

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  • DOI: https://doi.org/10.1007/s00429-012-0419-0

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