Spatial learning of the water maze: Progression of brain circuits mapped with cytochrome oxidase histochemistry

Neurobiology of Learning and Memory

Volumn 93, Issue 3, 2010, Pages 362-371

  Conejo, N M ^a   Gonzalez Pardo H ^a   Gonzalez Lima, F ^b   Arias, J L ^a  

^a UNIVERSITY OF OVIEDO   (Spain)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Limbic system; Neural networks; Rat; Spatial learning

Indexed keywords

CYTOCHROME C OXIDASE;

ADULT ANIMAL; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN MAPPING; CONTROLLED STUDY; ENZYME ACTIVITY; HISTOCHEMISTRY; LEARNING; MALE; MAZE TEST; NONHUMAN; PREFRONTAL CORTEX; RAT; SPATIAL LEARNING; TASK PERFORMANCE; THALAMUS VENTRAL NUCLEUS;

ANIMALS; ANTERIOR THALAMIC NUCLEI; ELECTRON TRANSPORT COMPLEX IV; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MAZE LEARNING; NERVE NET; PARIETAL LOBE; RATS; RATS, WISTAR; SPACE PERCEPTION; WATER;

EID: 77950691905     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2009.12.002     Document Type: Article

References (58)

1. Aggleton J.P., Brown M.W. Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behavioral and Brain Science. 1999, 22:425-444.
2. Agin V., Chicher R., Chichery M.P. Effects of learning on cytochrome oxidase activity in cuttlefish brain. Neuroreport 2001, 12:113-116.
3. Bontempi B., Jaffard R., Destrade C. Differential temporal evolution of post-training changes in regional brain glucose metabolism induced by repeated spatial discrimination training in mice. visualization of the memory consolidation process?. European Journal of Neuroscience 1996, 8:2348-2360.
4. Bontempi B., Laurent-Demir C., Destrade C., Jaffard R. Time-dependent reorganization of brain circuitry underlying long-term memory storage. Nature 1999, 400:671-675.
5. Bruchey A.K., Gonzalez-Lima F. Enhanced metabolic capacity of the frontal cerebral cortex after Pavlovian conditioning. Neuroscience 2008, 152:299-307.
6. Cada A., de la Torre J.C., Gonzalez-Lima F. Chronic cerebrovascular ischemia in aged rats: Effects on brain metabolic capacity and behavior. Neurobiologyof Aging 2000, 21:225-233.
7. Conejo N.M., González-Pardo H., Vallejo G., Arias J.L. Involvement of the mammillary bodies in spatial working memory revealed by cytochrome oxidase activity. Brain Research 2004, 1011:107-114.
8. Conejo N.M., Gonzalez-Pardo H., Vallejo G., Arias J.L. Changes in brain oxidative metabolism induced by water maze training. Neuroscience 2007, 145:403-412.
9. Déglise P., Dacher M., Dion E., Gauthier M., Armengaud C. Regional brain variations of cytochrome oxidase staining during olfactory learning in the honeybee (Apis mellifera). Behavioral Neuroscience 2003, 117:540-547.
10. Delatour B., Gisquet-Verrier P. Functional role of rat prelimbic-infralimbic cortices in spatial memory: Evidence for their involvement in attention and behavioural flexibility. Behavioral Brain Research 2000, 109:113-128.
11. D'Hooge R., De Deyn P.P. Applications of the Morris water maze in the study of learning and memory. Brain Research Brain Research Reviews 2001, 36:60-90.
12. Frankland P.W., Bontempi B. The organization of recent and remote memories. Nature Reviews Neuroscience 2005, 6:119-130.
13. Gonzalez-Lima F., Cada A. Cytochrome oxidase activity in the auditory system of the mouse: A qualitative and quantitative histochemical study. Neuroscience 1994, 63:559-578.
14. Gonzalez-Lima F., Jones D. Quantitative mapping of cytochrome oxidase activity in the central auditory system of the gerbil: A study with calibrated activity standards and metal-intensified histochemistry. Brain Research 1994, 660:34-49.
15. Guye M., Bartolomei F., Ranjeva J.P. Imaging structural and functional connectivity: Towards a unified definition of human brain organization?. Current Opinion in Neurology 2008, 21:393-403.
16. 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.
17. Kesner R.P., Lee I., Gilbert P. A behavioral assessment of hippocampal function based on a subregional analysis. Review Neuroscience 2004, 15:333-351.
18. Leutgeb J.K., Leutgeb S., Moser M.B., Moser E.I. Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 2007, 315:961-966.
19. López L., Lorente L., Arias J., González-Pardo H., Cimadevilla J., Arias J.L. Changes of cytochrome oxidase activity in rat suprachiasmatic nucleus. Brain Research 1997, 769:367-371.
20. Maviel T., Durkin T.P., Menzaghi F., Bontempi B. Sites of neocortical reorganization critical for remote spatial memory. Science 2004, 305:96-99.
21. McClelland J.L., Goddard N.H. Considerations arising from a complementary learning systems perspective on hippocampus and neocortex. Hippocampus 1996, 6:654-665.
22. McGaugh J.L. Memory-A century of consolidation. Science 2000, 287:248-251.
23. McIntosh A.R. Mapping cognition to the brain through neural interactions. Memory 1999, 7:523-548.
24. McIntosh A.R. Contexts and catalysts: A resolution of the localization and integration of function in the brain. Neuroinformatics 2004, 4:175-182.
25. McIntosh A.R., Gonzalez-Lima F. Network interactions among limbic cortices, basal forebrain, and cerebellum differentiate a tone conditioned as a Pavlovian excitor or inhibitor: Fluorodeoxyglucose mapping and covariance structural modeling. Journal of Neurophysiology 1994, 72:1717-1733.
26. Mcintosh A.R., Gonzalez-Lima F. Structural equation modelling and its application to network analysis of functional brain imaging. Human Brain Mapping 1994, 2:2-22.
27. Morris R.G., Inglis J., Ainge J.A., Lverman H.J., Tulloch J., Dudai Y., et al. Memory reconsolidation: Sensitivity of spatial memory to inhibition of protein synthesis in dorsal hippocampus during encoding and retrieval. Neuron 2006, 50:479-489.
28. Moser E.I., Kropff E., Moser M.B. Place cells, grid cells, and the brain's spatial representation system. Annual Review in Neuroscience 2008, 31:69-89.
29. Nadel L., Moscovitch M. Hippocampal contributions to cortical plasticity. Neuropharmacology 1998, 37:431-439.
30. Nitz D. Parietal cortex, navigation, and the construction of arbitrary reference frames for spatial information. Neurobioloy of Learning and Memory 2009, 91:179-185.
31. Poirier G.L., Amin E., Aggleton J.P. Qualitatively different hippocampal subfield engagement emerges with mastery of a spatial memory task by rats. The Journal of Neuroscience 2008, 28:1034-1045.
32. Poremba A., Jones D., Gonzalez-Lima F. Metabolic effects of blocking tone conditioning on the rat auditory system. Neurobiology of Learning and Memory 1997, 68:154-171.
33. Poremba A., Jones D., Gonzalez-Lima F. Classical conditioning modifies cytochrome oxidase activity in the auditory system. European Journal of Neuroscience 1998, 10:3035-3043.
34. Puga F., Barrett D.W., Bastida C.C., Gonzalez-Lima F. Functional networks underlying latent inhibition learning in the mouse brain. Neuroimage 2007, 38:171-183.
35. Rauchs G., Orban P., Balteau E., Schmidt C., Degueldre C., Luxen A., et al. Partially segregated neural networks for spatial and contextual memory in virtual navigation. Hippocampus 2008, 18:503-518.
36. Redish A.D., Touretzky D.S. Cognitive maps beyond the hippocampus. Hippocampus 1997, 7:15-35.
37. Rolls E.T. An attractor network in the hippocampus: Theory and neurophysiology. Learning & Memory 2007, 14:714-731.
38. Rolls E.T., Kesner R.P. A computational theory of hippocampal function, and empirical tests of the theory. Progress in Neurobiology 2006, 79:1-48.
39. Ros J., Pellerin L., Magara F., Dauguet J., Schenk F., Magistretti P.J. Metabolic activation pattern of distinct hippocampal subregions during spatial learning and memory retrieval. Journal of Cerebral Blood Flow and Metabolism 2006, 6:468-477.
40. Rosenbaum R.S., Ziegler M., Winocur G., Grady C.L., Moscovitch M. "I have often walked down this street before": fMRI studies on the hippocampus and other structures during mental navigation of an old environment. Hippocampus 2004, 14:826-835.
41. Sakata J.T., Coomber P., Gonzalez-Lima F., Crews D. Functional connectivity among limbic brain areas: Differential effects of incubation temperature and gonadal sex in the leopard gecko, Eublepharis macularius. Brain Behavior and Evolution 2000, 55:139-151.
42. Save E., Poucet B. Role of the parietal cortex in long-term representation of spatial information in the rat. Neurobiology of Learning and Memory 2009, 91:172-178.
43. Shao J., Dongsheng T. The Jacknife and bootstrap 1995, Springer-Verlag, New York.
44. 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.
45. Sheehan T., Andrew Chambers R., Russell D.S. Regulation of affect by the lateral septum: Implications for neuropsychiatry. Brain Research Reviews 2004, 46:71-117.
46. Spiers H.J., Maguire E.A. Thoughts, behaviour, and brain dynamics during navigation in the real world. Neuroimage 2006, 31:1826-1840.
47. Stephan K.E., Marshall J.C., Friston K.J., Rowe J.B., Ritzl A., Zilles K., et al. Lateralized cognitive processes and lateralized task control in the human brain. Science 2003, 301:384-386.
48. Taube J.S. Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. Journal of Neuroscience 1995, 15:70-86.
49. Uecker A., Gonzalez-Lima F., Cada A., Reiman E.M. Behavior and brain uptake of fluorodeoxyglucose in mature and aged C57BL/6 mice. Neurobiology of Aging 2000, 21:705-718.
50. van Groen T., Kadish I., Wyss J.M. Role of the anterodorsal and anteroventral nuclei of the thalamus in spatial memory in the rat. Behavioral Brain Research 2002, 132:19-28.
51. Vann S.D., Aggleton J.P. Testing the importance of the retrosplenial guidance system: Effects of different sized retrosplenial cortex lesions on heading direction and spatial working memory. Behavioral Brain Research 2004, 155:97-108.
52. Vann S.D., Brown M.W., Aggleton J.P. Fos expression in the rostral thalamic nuclei and associated cortical regions in response to different spatial memory tests. Neuroscience 2000, 101:983-991.
53. Villarreal J.S., Gonzalez-Lima F., Berndt J., Barea-Rodriguez E.J. Water maze training in aged rats: Effects on brain metabolic capacity and behavior. Brain Research 2002, 939:43-51.
54. Wang G.W., Cai J.X. Disconnection of the hippocampal-prefrontal cortical circuits impairs spatial working memory performance in rats. Behavioral Brain Research 2006, 175:329-336.
55. Wang G.W., Cai J.X. Reversible disconnection of the hippocampal-prelimbic cortical circuit impairs spatial learning but not passive avoidance learning in rats. Neurobiology of Learning and Memory 2008, 90:365-373.
56. Warburton E.C., Baird A., Morgan 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. Journal of Neuroscience 2001, 21:7323-7330.
57. Wong-Riley M.T. Cytochrome oxidase: An endogenous metabolic marker for neuronal activity. Trends in Neuroscience 1989, 12:94-101.
58. Zimmer H.D. Visual and spatial working memory: From boxes to networks. Neuroscience & Biobehavioral Reviews 2008, 32:1373-1395.