Distinct, parallel pathways link the medial mammillary bodies to the anterior thalamus in macaque monkeys

European Journal of Neuroscience

Volumn 26, Issue 6, 2007, Pages 1575-1586

  Vann, Seralynne D ^a   Saunders, Richard C ^b   Aggleton, John P ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Amnesia; Anterior thalamic nuclei; Hippocampus; Mammillary bodies; Mammillothalamic tract; Memory

Indexed keywords

ARTICLE; BRAIN REGION; CONTROLLED STUDY; MACACA; MAMMILLARY BODY; MEMORY; MONKEY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; THALAMUS;

ANIMALS; ANTERIOR THALAMIC NUCLEI; FLUORESCENT DYES; HORSERADISH PEROXIDASE; IMMUNOHISTOCHEMISTRY; MACACA FASCICULARIS; MACACA MULATTA; MAMILLARY BODIES; MEDIODORSAL THALAMIC NUCLEUS; NEURAL PATHWAYS;

EID: 34548673970     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05773.x     Document Type: Article

References (52)

1. Aggleton, J.P. Brown, M.W. (1999) Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav. Brain Sci., 22, 425 489.
2. Aggleton, J.P., Desimone, R. Mishkin, M. (1986) The origin, course, and termination of the hippocampo-thalamic projections in the macaque. J. Comp. Neurol., 243, 409 421.
3. Aggleton, J.P. Mishkin, M. (1983) Memory impairments following restricted medial thalamic lesions in monkeys. Exp. Brain Res., 52, 199 209.
4. Aggleton, J.P. Mishkin, M. (1985) Mamillary body lesions and visual recognition in monkeys. Exp. Brain Res., 58, 190 197.
5. Aggleton, J.P., Vann, S.D. Saunders, R.C. (2005) Projections from the hippocampal region to the mammillary bodies in macaque monkeys. Eur. J. Neurosci., 22, 2519 2530.
6. Albo, Z., Di Prisco, G.V. Vertes, R.P. (2003) Anterior thalamic unit discharge profiles and coherence with hippocampal theta rhythm. Thalamus Related Systems, 2, 133 144.
7. Barbas, H., Haswell Henion, T.H. Dermon, C.R. (1991) Diverse thalamic projections to the prefrontal cortex in the rhesus monkey. J. Comp. Neurol., 313, 65 94.
8. Bentivoglio, M., Kultas-Ilinsky, K. Ilinsky, I. (1993) Limbic thalamus: structure, intrinsic organisation, and connections. In Vogt, B.A. Gabriel, M. (Eds), Neurobiology of the Cingulate Cortex and Limbic Thalamus. Birkhauser, Boston, pp. 71 122.
9. Carmichael, S.T. Price, J.L. (1985) Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J. Comp. Neurol., 363, 615 641.
10. Crosby, E.C. Showers, M.J.C. (1969) Comparative anatomy of the preoptic and hypothalamic areas. In Haymaker, W., Anderson, E. Nauta, W.J.H. (Eds), The Hypothalamus. Charles C Thomas, Illinois, USA, pp. 61 134.
11. Crouch, R.L. (1934) The nuclear configuration of the hypothalamus and the subthalamus of macacus rhesus. J. Comp. Neurol., 59, 431 485.
12. Cruce, J.A.F. (1975) An autoradiographic study of the projections of the mammillothalamic tract in the rat. Brain Res., 85, 211 219.
13. Delay, J. Brion, S. (1969) Le Syndrome de Korsakoff. Masson, Paris.
14. Dusoir, H., Kapur, N., Brynes, D.P., McKinstry, S. Hoare, R.D. (1990) The role of diencephalic pathology in human memory disorder. Brain, 113, 1695 1706.
15. Fry, W.J., Krumins, R., Fry, F.J., Thomas, G. Borbely, S. Ades, H. (1963) Origins and distributions of some efferent pathways from the mammillary nuclei of the cat. J. Comp. Neurol., 120, 195 257.
16. Gaffan, D. (1992) The role of the hippocampus-fornix-mammillary system in episodic memory. In Squire, L.R. Butters, N. (Eds), Neuropsychology of Memory. 2nd Edn. Guilford Press, New York, pp. 336 346.
17. Gentilini, M., De Renzi, E. Crispi, G. (1987) Bilateral paramedial thalamic infarcts: report of eight cases. J. Neurol. Neurosurg. Psychiat., 50, 900 909.
18. Gold, J.J. Squire, L.R. (2006) The anatomy of memory: neurohistological analysis of three new cases. Learn. Mem., 13, 1 12.
19. Hardy, H. Heimer, L. (1977) A safer and more sensitive substitute for diaminobenzidene in the light microscopic demonstration of retrograde and anterograde transport of HRP. Neurosci. Lett., 5, 235 240.
20. Hasselmo, M., Cannon, R.C. Koene, R. (2002) A simulation of parahippocampal and hippocampal structures guiding spatial navigation of a virtual rat in a virtual environment: a functions framework for theta theory. In Witter, M. Wouterlood, F. (Eds), The Parahippocampal Region: Organization and Role in Cognition Functions. Oxford University Press, Oxford, UK, pp. 139 157.
21. Hildebrandt, H., Muller, S., Bussman-Mork, B., Goebel, S. Eilers, N. (2001) Are some memory deficits unique to lesions of the mammillary bodies? J. Clin. Exp. Neuropsych., 23, 490 501.
22. Hopkins, D.A. (2005) Neuroanatomy of head direction cell circuits. In Wiener, S.I. Taube, J.S. (Eds), Head Direction Cells and the Neural Mechanisms of Spatial Orientation. MIT Press, Cambridge, Massachusetts, pp. 17 44.
23. Keizer, K., Kuypers, H.G.J.M., Huisman, A.M. Dann, O. (1983) Diamidino yellow dihydrochloride (DY.2HCL); a new fluorescent retrograde neuronal tracer which migrates only very slowly out of the cell. Exp. Brain Res., 51, 179 191.
24. Kievet, J. Kuypers, H.G.J.M. (1977) Organization of the thalamo-cortical connexions to the frontal lobe in the rhesus monkey. Exp. Brain Res., 29, 299 322.
25. Kirk, I.J. (1998) Frequency modulation of hippocampal theta by the supramammillary nucleus, and other hypothalamo-hippocampal interactions: mechanisms and functional implications. Neurosci. Biobehav. Rev., 22, 291 302.
26. Kocsis, K. Vertes, R.P. (1994) Characterization of neurons of the supramammillary nucleus and mammillary body that discharge rhythmically with the hippocampal theta rhythm in the rat. J. Neurosci., 14, 7040 7052.
27. Kuypers, H.G.J.M., Bentivoglio, M., Catsman-Berrevoets, C.E. Bharos, A.T. (1980) Double retrograde neuronal labeling through divergent axon collaterals using two fluorescent tracers with the same excitation wavelength which label different features of the cell. Exp. Brain Res., 40, 383 392.
28. Loftus, M., Knight, R.T. Amaral, D.G. (2000) An analysis of atrophy in the medial mammillary nucleus following hippocampal and fornix lesions in humans and nonhuman primates. Exp. Neurol., 163, 180 190.
29. Markowitsch, H.J. (1982) Thalamic mediodorsal nucleus and memory: a critical evaluation of studies in animals and man. Neurosci. Biobehav. Rev., 6, 351 380.
30. Mesulam, M. (1978) Tetramethyl benzidene for horseradish peroxidase neurohistochemistry: a noncarcinogenic blue reaction-product with superior sensitivity for visualizing neural afferents and efferents. J. Histochem. Cytochem., 26, 106 117.
31. Nauta, W.J.H. Haymaker, W. (1969) Hypothalamic nuclei and fibre connections. In Haymaker, W., Anderson, E. Nauta, W.J.H. (Eds), The Hypothalamus. Charles C Thomas, Illinois, USA, pp. 136 203.
32. Olszewski, I. (1952) The Thalamus of the Macaca Mulatta. S. Karger, Basel.
33. Parker, A. Gaffan, D. (1997) Mammillary body lesions in monkeys impair object-in-place memory: functional unity of the fornix-mamillary system. J. Cogn. Neurosci., 9, 512 521.
34. Powell, T.P.S., Guillery, R.W. Cowan, W.M. (1957) A quantitative study of the fornix-mamillo-thalamic system. J. Anat., 91, 419 437.
35. Rose, J. (1939) The cell structure of the mamillary body in the mammals and in man. J. Anat., 74, 91 115.
36. Rosene, D., Roy, N.J. Davis, B.J. (1986) A cryoprotection method that facilitates cutting frozen sections of whole monkey brains for histological and histochemical processing without freezing artifact. J. Histochem. Cytochem., 34, 1301 1315.
37. Saunders, R.C., Mishkin, M. Aggleton, J.P. (2005) Projections from the entorhinal cortex, perirhinal cortex, presubiculum, and parasubiculum to the medial thalamus in macaque monkeys: identifying different pathways using disconnection techniques. Exp. Brain Res., 167, 1 16.
38. Tanaka, Y., Miyazawa, Y., Akaoka, F. Yamada, T. (1997) Amnesia following damage to the mammillary bodies. Neurology, 48, 160 165.
39. Taube, J.S. (1998) Head direction cells and the neurophysiological basis for a sense of direction. Prog. Neurobiol., 55, 225 256.
40. Van der Werf, Y., Scheltens, P., Lindeboom, J., Witter, M.P., Uylings, H.B.M. Jolles, J. (2003) Deficits of memory, executive functioning and attention following infarction in the thalamus; a study of 22 cases with localised lesions. Neuropsychologia, 41, 1330 1344.
41. Van der Werf, Y., Witter, M.P., Uylings, H.B.M. Jolles, J. (2000) Neuropsychology of infarctions in the thalamus: a review. Neuropsychologia, 38, 613 627.
42. Van Groen, T. Wyss, J.M. (1992) Projections from the laterodorsal nucleus of the thalamus to the limbic and visual cortices. J. Comp. Neurol., 324, 427 448.
43. Vann, S.D. Aggleton, J.P. (2003) Evidence of a spatial encoding deficit in rats with lesions of the mammillary bodies or mammillothalamic tract. J. Neurosci., 23, 3506 3514.
44. Vann, S.D. Aggleton, J.P. (2004) The mammillary bodies - two memory systems in one? Nat. Rev. Neurosci., 5, 35 44.
45. Veazey, R.B., Amaral, D.G. Cowan, W.M. (1982a) The morphology and connections of the posterior hypothalamus in the cynomolgus monkey (Macaca fascicularis). I. Cytoarchitectonic organization. J. Comp. Neurol., 207, 114 134.
46. Veazey, R.B., Amaral, D.G. Cowan, W.M. (1982b) The morphology and connections of the posterior hypothalamus in the cynomolgus monkey (Macaca fascicularis). II. Efferent connections. J. Comp. Neurol., 207, 135 156.
47. Vertes, R.P., Albo, Z. Di Prisco, G.V. (2001) Theta-rhythmically firing neurons in the anterior thalamus: implications for mnemonic functions of Papez's circuit. Neuroscience, 104, 619 625.
48. Vertes, R.P., Hoover, W.B. Di Prisco, G.V. (2004) Theta rhythm of the hippocampus: subcortical control and functional significance. Behav. Cogn. Neurosci. Rev., 3, 173 200.
49. Victor, M., Adams, R.D. Collins, G.H. (1971) The Wernicke-Korsakoff Syndrome. Davis, Philadelphia.
50. Von Cramon, D.Y., Hebel, N. Schuri, U. (1985) A contribution to the anatomical basis of thalamic amnesia. Brain, 108, 993 1008.
51. Xiao, D. Barbas, H. (2002a) Pathways for emotions and memory. I. Input and output zones linking the anterior thalamic nuclei with prefrontal cortices in the rhesus monkey. Thalamus Related Systems, 2, 21 32.
52. Xiao, D. Barbas, H. (2002b) Pathways for emotions and memory. II. Afferent input to the anterior thalamic nuclei from prefrontal, temporal, hypothalamic areas and the basal ganglia in the rhesus monkey. Thalamus Related Systems, 2, 33 48.