Behavioural state differentially engages septohippocampal cholinergic and GABAergic neurons in R6/1 Huntington's disease mice

Neurobiology of Learning and Memory

Volumn 97, Issue 2, 2012, Pages 261-270

  Ransome, Mark I ^a   Hannan, Anthony J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

C Fos; Cholinergic; Cognition; GABAergic; Hippocampus; Huntington's disease; Septohippocampal system

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AROUSAL; ARTICLE; BEHAVIORAL SCIENCE; CELL ACTIVATION; CELL COUNT; CELL FUNCTION; CELL POPULATION; CHOLINERGIC ACTIVITY; CHOLINERGIC NERVE; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; FOREBRAIN; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; HIPPOCAMPUS; HUNTINGTON CHOREA; LOCOMOTION; MOUSE; NONHUMAN; SEPTOHIPPOCAMPUS;

ANIMALS; BEHAVIOR, ANIMAL; CHOLINERGIC NEURONS; COGNITION; DISEASE MODELS, ANIMAL; ENVIRONMENT; EXPLORATORY BEHAVIOR; GABAERGIC NEURONS; HIPPOCAMPUS; HUNTINGTON DISEASE; MAZE LEARNING; MEMORY; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY;

EID: 84856769213     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2012.01.004     Document Type: Article

References (79)

1. Ali A.E., Wilson Y.M., Murphy M. A single exposure to an enriched environment stimulates the activation of discrete neuronal populations in the brain of the fos-tau-lacZ mouse. Neurobiology of Learning and Memory 2009, 92:381-390.
2. Aziz N.A., Anguelova G.V., Marinus J., Lammers G.J., Roos R.A. Sleep and circadian rhythm alterations correlate with depression and cognitive impairment in Huntington's disease. Parkinsonism and Related Disorders 2010, 16:345-350.
3. Ballarini F., Moncada D., Martinez M.C., Alen N., Viola H. Behavioral tagging is a general mechanism of long-term memory formation. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:14599-14604.
4. Berchtold N.C., Kesslak J.P., Cotman C.W. Hippocampal brain-derived neurotrophic factor gene regulation by exercise and the medial septum. Journal of Neuroscience Research 2002, 68:511-521.
5. Bland B.H., Oddie S.D. Theta band oscillation and synchrony in the hippocampal formation and associated structures: The case for its role in sensorimotor integration. Behavioural Brain Research 2001, 127:119-136.
6. Bolivar V.J., Manley K., Messer A. Early exploratory behavior abnormalities in R6/1 Huntington's disease transgenic mice. Brain Research 2004, 1005:29-35.
7. Buzsaki G. Theta rhythm of navigation: Link between path integration and landmark navigation, episodic and semantic memory. Hippocampus. 2005, 15:827-840.
8. Castaneda M.T., Sanabria E.R., Hernandez S., Ayala A., Reyna T.A., Wu J.Y., et al. Glutamic acid decarboxylase isoforms are differentially distributed in the septal region of the rat. Neuroscience Research 2005, 52:107-119.
9. Cepeda C., Starling A.J., Wu N., Nguyen O.K., Uzgil B., Soda T., et al. Increased GABAergic function in mouse models of Huntington's disease: Reversal by BDNF. Journal of Neuroscience Research 2004, 78:855-867.
10. Colom L.V. Septal networks: Relevance to theta rhythm, epilepsy and Alzheimer's disease. Journal of Neurochemistry 2006, 96:609-623.
11. Colom L.V., Castaneda M.T., Reyna T., Hernandez S., Garrido-Sanabria E. Characterization of medial septal glutamatergic neurons and their projection to the hippocampus. Synapse 2005, 58:151-164.
12. Cooper-Kuhn C.M., Winkler J., Kuhn H.G. Decreased neurogenesis after cholinergic forebrain lesion in the adult rat. Journal of Neuroscience Research 2004, 77:155-165.
13. Cotman C.W., Berchtold N.C. Exercise: A behavioral intervention to enhance brain health and plasticity. Trends in Neurosciences 2002, 25:295-301.
14. Davies P., Maloney A.J. Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 1976, 2:1403.
15. Del Tongo C., Carretta D., Fulgenzi G., Catini C., Minciacchi D. Parvalbumin-positive GABAergic interneurons are increased in the dorsal hippocampus of the dystrophic mdx mouse. Acta Neuropathologica 2009, 118:803-812.
16. Dellu F., Contarino A., Simon H., Koob G.F., Gold L.H. Genetic differences in response to novelty and spatial memory using a two-trial recognition task in mice. Neurobiology of Learning and Memory 2000, 73:31-48.
17. Freund T.F., Antal M. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 1988, 336:170-173.
18. Gil J.M., Rego A.C. The R6 lines of transgenic mice: A model for screening new therapies for Huntington's disease. Brain Research Reviews 2009, 59:410-431.
19. Giovannini M.G., Rakovska A., Benton R.S., Pazzagli M., Biachi L., Pepeu G. Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats. Neuroscience 2001, 106:43-53.
20. Gorelova N., Reiner P.B. Histamine depolarizes cholinergic septal neurons. Journal of Neurophysiology 1996, 75:707-714.
21. HDCRG, Huntington's Disease Collaborative Research Group. (1993). A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntington's Disease Collaborative Research Group. Cell, 72, pp. 971-983.
22. Herdegen T., Leah J.D. Inducible and constitutive transcription factors in the mammalian nervous system: Control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Research. Brain Research Reviews 1998, 28:370-490.
23. Herrera D.G., Robertson H.A. Activation of c-fos in the brain. Progress in Neurobiology 1996, 50:83-107.
24. Huerta P.T., Lisman J.E. Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature 1993, 364:723-725.
25. Jinno S., Kosaka T. Cellular architecture of the mouse hippocampus: A quantitative aspect of chemically defined GABAergic neurons with stereology. Neuroscience Research 2006, 56:229-245.
26. Kahneman D. Attention and effort 1973, Prentice-Hall Inc, New Jersey.
27. Kimura H., McGeer P.L., Peng F., McGeer E.G. Choline acetyltransferase-containing neurons in rodent brain demonstrated by immunohistochemistry. Science 1980, 208:1057-1059.
28. Kohler C.A., da Silva W.C., Benetti F., Bonini J.S. Histaminergic mechanisms for modulation of memory systems. Neural Plasticity 2011, 2011:328602.
29. Kovacs K.J. Measurement of immediate-early gene activation- c-fos and beyond. Journal of Neuroendocrinology 2008, 20:665-672.
30. Kunig G., Leenders K.L., Sanchez-Pernaute R., Antonini A., Vontobel P., Verhagen A., et al. Benzodiazepine receptor binding in Huntington's disease: [11C] Flumazenil uptake measured using positron emission tomography. Annals of Neurology 2000, 47:644-648.
31. Lange K.W., Javoy-Agid F., Agid Y., Jenner P., Marsden C.D. Brain muscarinic cholinergic receptors in Huntington's disease. Journal of Neurology 1992, 239:103-104.
32. Lecourtier L., de Vasconcelos A.P., Cosquer B., Cassel J.C. Combined lesions of GABAergic and cholinergic septal neurons increase locomotor activity and potentiate the locomotor response to amphetamine. Behavioural Brain Research 2010, 213:175-182.
33. Lecourtier L., de Vasconcelos A.P., Cosquer B., Cassel J.C. Septohippocampal pathways contribute to system consolidation of a spatial memory: Sequential implication of gabaergic and cholinergic neurons. Hippocampus 2010.
34. Li J.Y., Popovic N., Brundin P. The use of the R6 transgenic mouse models of Huntington's disease in attempts to develop novel therapeutic strategies. NeuroRx 2005, 2:447-464.
35. Lyness S.A., Zarow C., Chui H.C. Neuron loss in key cholinergic and aminergic nuclei in Alzheimer disease: A meta-analysis. Neurobiology of Aging 2003, 24:1-23.
36. Ma S., Olucha-Bordonau F.E., Hossain M.A., Lin F., Kuei C., Liu C., et al. Modulation of hippocampal theta oscillations and spatial memory by relaxin-3 neurons of the nucleus incertus. Learning and Memory 2009, 16:730-742.
37. Maccaferri G., Lacaille J.C. Interneuron Diversity series: Hippocampal interneuron classifications--making things as simple as possible, not simpler. Trends Neurosci. 2003, 26:564-571.
38. Mangiarini L., Sathasivam K., Seller M., Cozens B., Harper A., Hetherington C., et al. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 1996, 87:493-506.
39. Manseau F., Danik M., Williams S. A functional glutamatergic neurone network in the medial septum and diagonal band area. Journal of Physiology 2005, 566:865-884.
40. Manyam N.V., Hare T.A., Katz L., Glaeser B.S. Huntington's disease. Cerebrospinal fluid GABA levels in at-risk individuals. Archives of Neurology 1978, 35:728-730.
41. McKenna J.T., Cordeira J.W., Jeffrey B.A., Ward C.P., Winston S., McCarley R.W., et al. c-Fos protein expression is increased in cholinergic neurons of the rodent basal forebrain during spontaneous and induced wakefulness. Brain Research Bulletin 2009, 80:382-388.
42. Mohapel P., Leanza G., Kokaia M., Lindvall O. Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiology of Aging 2005, 26:939-946.
43. Moncada D., Viola H. Induction of long-term memory by exposure to novelty requires protein synthesis: Evidence for a behavioral tagging. Journal of Neuroscience 2007, 27:7476-7481.
44. Niewiadomska G., Baksalerska-Pazera M., Riedel G. The septo-hippocampal system, learning and recovery of function. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2009, 33:791-805.
45. Nithianantharajah J., Barkus C., Murphy M., Hannan A.J. Gene-environment interactions modulating cognitive function and molecular correlates of synaptic plasticity in Huntington's disease transgenic mice. Neurobiology of Disease 2008, 29:490-504.
46. Oddie S.D., Bland B.H. Hippocampal formation theta activity and movement selection. Neuroscience and Biobehavioral Reviews 1998, 22:221-231.
47. O'Keefe J., Recce M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 1993, 3:317-330.
48. Painold A., Anderer P., Holl A.K., Letmaier M., Saletu-Zyhlarz G.M., Saletu B., et al. Comparative EEG mapping studies in Huntington's disease patients and controls. Journal of Neural Transmission 2010, 117:1307-1318.
49. Panula P., Revuelta A.V., Cheney D.L., Wu J.Y., Costa E. An immunohistochemical study on the location of GABAergic neurons in rat septum. Journal of Comparative Neurology 1984, 222:69-80.
50. Paxinos G., Franklin K.B.J. The mouse brain in stereotaxic coordinates 2001, Academic Press, San Diego. (2nd ed.).
51. Perry T.L., Hansen S., Kloster M. Huntington's chorea. Deficiency of gamma-aminobutyric acid in brain. New England Journal of Medicine 1973, 288:337-342.
52. Pop-Jordanov J., Pop-Jordanova N. Neurophysical substrates of arousal and attention. Cognitive Processing 2009, 10(Suppl 1):S71-S79.
53. Ransome M.I., Turnley A.M. Analysis of neuronal subpopulations in mice over-expressing suppressor of cytokine signaling-2. Neuroscience 2005, 132:673-687.
54. Ransome M.I., Turnley A.M. Systemically delivered Erythropoietin transiently enhances adult hippocampal neurogenesis. Journal of Neurochemistry 2007, 102:1953-1965.
55. Ransome M.I., Turnley A.M. Growth hormone signaling and hippocampal neurogenesis: Insights from genetic models. Hippocampus 2008, 18:1034-1050.
56. Sarter M., Bruno J.P. Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: Differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents. Neuroscience 2000, 95:933-952.
57. Sarter M., Bruno J.P. The neglected constituent of the basal forebrain corticopetal projection system: GABAergic projections. European Journal of Neuroscience 2002, 15:1867-1873.
58. Semba K. The cholinergic basal forebrain: A critical role in cortical arousal. The basal forebrain anatomy to function 1991, 197-218. Plenum Press, New York, (Vols. 1-2). P.W. Kalivas, I. Hanin (Eds.).
59. Sipione S., Cattaneo E. Modeling Huntington's disease in cells, flies, and mice. Molecular Neurobiology 2001, 23:21-51.
60. Smith C.M., Ryan P.J., Hosken I.T., Ma S., Gundlach A.L. Relaxin-3 systems in the brain-The first 10 years. Journal of Chemical Neuroanatomy 2011.
61. Smith R., Chung H., Rundquist S., Maat-Schieman M.L., Englund E., Liu R.A., et al. Cholinergic neuronal defect without cell loss in Huntington's disease. Human Molecular Genetics 2006, 15:3119-3131.
62. Sotty F., Danik M., Manseau F., Laplante F., Quirion R., Williams S. Distinct electrophysiological properties of glutamatergic, cholinergic and GABAergic rat septohippocampal neurons: Novel implications for hippocampal rhythmicity. Journal of Physiology 2003, 551:927-943.
63. Spokes E.G. GABA in Huntington's chorea, Parkinsonism and schizophrenia. Advances in Experimental Medicine and Biology 1979, 123:461-473.
64. Stewart M., Fox S.E. Do septal neurons pace the hippocampal theta rhythm?. Trends in Neurosciences 1990, 13:163-168.
65. Streletz L.J., Reyes P.F., Zalewska M., Katz L., Fariello R.G. Computer analysis of EEG activity in dementia of the Alzheimer's type and Huntington's disease. Neurobiology of Aging 1990, 11:15-20.
66. Van der Borght K., Mulder J., Keijser J.N., Eggen B.J., Luiten P.G., Van der Zee E.A., et al. Input from the medial septum regulates adult hippocampal neurogenesis. Brain Research Bulletin 2005, 67:117-125.
67. van der Hiele K., Jurgens C.K., Vein A.A., Reijntjes R.H., Witjes-Ane M.N., Roos R.A., et al. Memory activation reveals abnormal EEG in preclinical Huntington's disease. Movement Disorders 2007, 22:690-695.
68. Vanderwolf C.H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalography and Clinical Neurophysiology 1969, 26:407-418.
69. Vertes R.P. Hippocampal theta rhythm: A tag for short-term memory. Hippocampus 2005, 15:923-935.
70. Vertes R.P., Kocsis B. Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 1997, 81:893-926.
71. Vinogradova O.S. Expression, control, and probable functional significance of the neuronal theta-rhythm. Progress in Neurobiology 1995, 45:523-583.
72. Walker F.O. Huntington's disease. Lancet 2007, 369:218-228.
73. Walker F.O., Young A.B., Penney J.B., Dovorini-Zis K., Shoulson I. Benzodiazepine and GABA receptors in early Huntington's disease. Neurology 1984, 34:1237-1240.
74. Wang S.H., Redondo R.L., Morris R.G. Relevance of synaptic tagging and capture to the persistence of long-term potentiation and everyday spatial memory. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:19537-19542.
75. Winson J. Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 1978, 201:160-163.
76. Wu M., Shanabrough M., Leranth C., Alreja M. Cholinergic excitation of septohippocampal GABA but not cholinergic neurons: Implications for learning and memory. Journal of Neuroscience 2000, 20:3900-3908.
77. Yoder R.M., Pang K.C. Involvement of GABAergic and cholinergic medial septal neurons in hippocampal theta rhythm. Hippocampus 2005, 15:381-392.
78. Zafonte R., Hammond F., Dennison A., Chew E. Pharmacotherapy to enhance arousal: What is known and what is not. Progress in Brain Research 2009, 177:293-316.
79. Zar J.H. Biostatistical analysis 1999, Prentice-Hall, New Jersey. 4th ed.