Organization of food protection behavior is differentially influenced by 192 IgG-saporin lesions of either the medial septum or the nucleus basalis magnocellularis

Brain Research

Volumn 1241, Issue , 2008, Pages 122-135

  Martin, Megan M ^a   Winter, Shawn S ^a   Cheatwood, Joseph L ^b,c   Carter, Lynniece A ^a   Jones, Jeana L ^a   Weathered, Scott L ^a   Wagner, Steven J ^a   Wallace, Douglas G ^a  

^a NORTHERN ILLINOIS UNIVERSITY   (United States)

^b LOYOLA UNIVERSITY CHICAGO   (United States)

^c HINES VA HOSPITAL   (United States)

Author keywords

Attentional processing; Bracing; Cortex; Dodging; Hippocampus; Interval timing; Parvalbumin; Rattus norvegicus

Indexed keywords

IMMUNOGLOBULIN G; SAPORIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATTENTION; BRAIN DAMAGE; CONTROLLED STUDY; FEMALE; FOOD INTAKE; HIPPOCAMPUS; INFORMATION PROCESSING; NONHUMAN; OLIVARY NUCLEUS; PRIORITY JOURNAL; RAT;

ACETYLCHOLINE; ANIMALS; ANTIBODIES, MONOCLONAL; ATTENTION; BASAL NUCLEUS OF MEYNERT; BEHAVIOR, ANIMAL; CHOLINERGIC FIBERS; COGNITION; CUES; DENERVATION; FEEDING BEHAVIOR; FEMALE; FORNIX, BRAIN; HIPPOCAMPUS; IMMUNOTOXINS; NEURAL PATHWAYS; PARVALBUMINS; RATS; RATS, LONG-EVANS; RATS, SPRAGUE-DAWLEY; RIBOSOME INACTIVATING PROTEINS, TYPE 1; SEPTAL NUCLEI; SOCIAL BEHAVIOR;

RATTUS; RATTUS NORVEGICUS;

EID: 55549117103     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.09.018     Document Type: Article

References (67)

1. Alreja M., Wu M., Liu W., Atkins J.B., Leranth C., and Shanabrough M. Muscarinic tone sustains impulse flow in the septohippocampal GABA but not cholinergic pathway: implications for learning and memory. J. Neurosci. 20 21 (2000) 8103-8110
2. Amaral D.G., and Kurz J. An analysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation of the rat. J. Comp. Neurol. 240 1 (1985) 37-59
3. Ammassari-Teule M., Amoroso D., Forloni G.L., Rossi-Arnaud C., and Consolo S. Mechanical deafferentation of basal forebrain-cortical pathways and neurotoxic lesions of the nucleus basalis magnocellularis: comparative effect on spatial learning and cortical acetylcholine release in vivo. Behav. Brain Res. 54 2 (1993) 145-152
4. Barlow J.S. Inertial navigation as a basis for animal navigation. J. Theor. Biol. 6 (1964) 76-117
5. Baxter M.G., and Gallagher M. Intact spatial learning in both young and aged rats following selective removal of hippocampal cholinergic input. Behav. Neurosci. 110 3 (1996) 460-467
6. Baxter M.G., Bucci D.J., Gorman L.K., Wiley R.G., and Gallagher M. Selective immunotoxic lesions of basal forebrain cholinergic cells: effects on learning and memory in rats. Behav. Neurosci. 109 4 (1995) 714-722
7. Berger-Sweeney J., Heckers S., Mesulam M.M., Wiley R.G., Lappi D.A., and Sharma M. Differential effects on spatial navigation of immunotoxin-induced cholinergic lesions of the medial septal area and nucleus basalis magnocellularis. J. Neurosci. 14 7 (1994) 4507-4519
8. Bizon J.L., Han J.S., Hudon C., and Gallagher M. Effects of hippocampal cholinergic deafferentation on learning strategy selection in a visible platform version of the water maze. Hippocampus 13 6 (2003) 676-684
9. Buhusi C.V., and Meck W.H. Differential effects of methamphetamine and haloperidol on the control of an internal clock. Behav. Neurosci. 116 (2002) 291-297
10. Buhusi C.V., and Meck W.H. What makes us tick? Functional and neural mechanisms of interval timing. Nat. Rev. Neurosci. 6 10 (2005) 755-765
11. Burk J.A., and Sarter M. Dissociation between the attentional functions mediated via basal forebrain cholinergic and GABAergic neurons. Neuroscience. 105 4 (2001) 899-909
12. Cahill J.F., and Baxter M.G. Cholinergic and noncholinergic septal neurons modulate strategy selection in spatial learning. Eur. J. Neurosci. 14 11 (2001) 1856-1864
13. Connor D.J., Langlais P.J., and Thal L.J. Behavioral impairments after lesions of the nucleus basalis by ibotenic acid and quisqualic acid. Brain Res. 555 1 (1991) 84-90
14. Dunnett S.B., Everitt B.J., and Robbins T.W. The basal forebrain-cortical cholinergic system: interpreting the functional consequences of excitotoxic lesions. Trends Neurosci. 14 11 (1991) 494-501
15. Dwyer T.A., Servatius R.J., and Pang K.C. Noncholinergic lesions of the medial septum impair sequential learning of different spatial locations. J. Neurosci. 27 2 (2007) 299-303
16. Etienne A.S. The orientation of the golden hamster to its nestsite after the elimination of various sensory cues. Experientia 36 (1980) 1048-1050
17. Etienne A.S., and Jeffery K.J. Path integration in mammals. Hippocampus 14 2 (2004) 180-192
18. Everitt B.J., and Robbins T.W. Central cholinergic systems and cognition. Annu. Rev. Psychol. 48 (1997) 649-684
19. Frielingsdorf H., Thal L.J., and Pizzo D.P. The septohippocampal cholinergic system and spatial working memory in the Morris water maze. Behav. Brain Res. 168 1 (2006) 37-46
20. Gallistel C.R. The Organization of Learning (1990), MIT, Cambridge
21. Gibbon J., Church R.M., and Meck W.H. Scalar timing in memory. Ann. N. Y. Acad. Sci. 423 (1984) 52-77
22. Gibbs R.B., and Johnson D.A. Cholinergic lesions produce task-selective effects on delayed matching to position and configural association learning related to response pattern and strategy. Neurobiol. Learn. Mem. 88 1 (2007) 19-32
23. Hagan J.J., Salamone J.D., Simpson J., Iversen S.D., and Morris R.G.M. Place navigation in rats is impaired by lesions of medial septum and diagonal band but not nucleus basalis magnocellularis. Behav. Brain Res. 27 (1988) 9-20
24. Hepler D.J., Olton D.S., Wenk G.L., and Coyle J.T. Lesions in nucleus basalis magnocellularis and medial septal area of rats produce qualitatively similar memory impairments. J. Neurosci. 5 4 (1985) 866-873
25. Jonasson Z., Cahill J.F., Tobey R.E., and Baxter M.G. Sexually dimorphic effects of hippocampal cholinergic deafferentation in rats. Eur. J. Neurosci. 20 11 (2004) 3041-3053
26. Karnovsky M.J., and Roots A. A "direct-coloring" thiocholine method for cholinesterases. J. Histochem. Cytochem. 12 (1964) 219-221
27. Kelsey J.E., and Landry B.A. Medial septal lesions disrupt spatial mapping ability in rats. Behav. Neurosci. 102 2 (1988) 289-293
28. Lehmann O., Grottick A.J., Cassel J.C., and Higgins G.A. A double dissociation between serial reaction time and radial maze performance in rats subjected to 192 IgG-saporin lesions of the nucleus basalis and/or the septal region. Eur. J. Neurosci. 18 3 (2003) 651-666
29. Maaswinkel H., Jarrard L.E., and Whishaw I.Q. Hippocampectomized rats are impaired in homing by path integration. Hippocampus 9 5 (1999) 553-561
30. Maricq A.V., and Church R.M. The differential effects of haloperidol and methamphetamine on time estimation in the rat. Psychopharmacology (Berlin) 79 (1983) 10-15
31. Martin M.M., and Wallace D.G. Selective hippocampal cholinergic deafferentation impairs self-movement cue use during a food hoarding task. Behav. Brain Res. 183 1 (2007) 78-86
32. Martin M.M., Horn K.L., Kusman K.J., and Wallace D.G. Medial septum lesions disrupt exploratory trip organization: evidence for septohippocampal involvement in dead reckoning. Physiol. Behav. 90 2-3 (2007) 412-424
33. Matell M.S., and Meck W.H. Neuropsychological mechanisms of interval timing behavior. BioEssays. 22 (2000) 94-103
34. Matell M.S., Berridge K.C., and Aldridge J.W. Dopamine D1 activation shortens the duration of phases in stereotypes grooming sequences. Behav. Processes 71 (2006) 241-249
35. McGaughy J., Kaiser T., and Sarter M. Behavioral vigilance following infusions of 192 IgG-saporin into the basal forebrain: selectivity of the behavioral impairment and relation to cortical AChE-positive fiber density. Behav. Neurosci. 110 2 (1996) 247-265
36. McGaughy J., Dalley J.W., Morrison C.H., Everitt B.J., and Robbins T.W. Selective behavioral and neurochemical effects of cholinergic lesions produced by intrabasalis infusions of 192 IgG-saporin on attentional performance in a five-choice serial reaction time task. J. Neurosci. 22 5 (2002) 1905-1913
37. McMahan R.W., Sobel T.J., and Baxter M.G. Selective immunolesions of hippocampal cholinergic input fail to impair spatial working memory. Hippocampus 7 2 (1997) 130-136
38. Meck W.H. Selective adjustment of the speed of internal clock and memory processes. J. Exp. Psychol. Anim. Behav. Processes 9 (1983) 171-201
39. Meck W.H., Church R.M., Wenk G.L., and Olton D.S. Nucleus basalis magnocellularis and medial septal area lesions differentially impair temporal memory. J. Neurosci. 7 11 (1987) 3505-3511
40. M'Harzi M., and Jarrard L.E. Effects of medial and lateral septal lesions on acquisition of a place and cue radial maze task. Behav. Brain Res. 49 2 (1992) 159-165
41. Mitchell S.J., Rawlins J.N., Steward O., and Olton D.S. Medial septal area lesions disrupt theta rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats. J. Neurosci. 2 3 (1982) 292-302
42. Mittelstaedt M.L., and Mittelstaedt H. Homing by path integration in a mammal. Naturwissenschaften 67 (1980) 566-567
43. Miyamoto M., Kato J., Narumi S., and Nagaoka A. Characteristics of memory impairment following lesioning of the basal forebrain and medial septal nucleus in rats. Brain Res. 419 1-2 (1987) 19-31
44. Mizumori S.J., Perez G.M., Alvarado M.C., Barnes C.A., and McNaughton B.L. Reversible inactivation of the medial septum differentially affects two forms of learning in rats. Brain Res. 528 1 (1990) 12-20
45. Oddie S.D., Kirk I.J., Whishaw I.Q., and Bland B.H. Hippocampal formation is involved in movement selection: evidence from medial septal cholinergic modulation and concurrent slow-wave (theta rhythm) recording. Behav. Brain Res. 88 2 (1997) 169-180
46. Oddie S.D., Kirk I.J., Gorny B.P., Whishaw I.Q., and Bland B.H. Impaired dodging in food-conflict following fimbria-fornix transection in rats: a novel hippocampal formation deficit. Brain Res. Bull. 57 5 (2002) 565-573
47. Olton D.S., Wenk G.L., Church R.M., and Meck W.H. Attention and the frontal cortex as examined by simultaneous temporal processing. Neuropsychologia 26 2 (1988) 307-318
48. Parron C., and Save E. Evidence for entorhinal and parietal cortices involvement in path integration in the rat. Exp. Brain. Res. 159 3 (2004) 349-359
49. Pinel J.P., Jones C.H., and Whishaw I.Q. Behavior from the ground up: rat behavior from the ventral perspective. Psychobiology 20 (1992) 185-188
50. Risold P.Y. The septal region. In: Paxinos G. (Ed). Rat Nervous System. 3rd ed. (2004), Elsevier AP, San Diego, CA 602-703
51. Robbins T.W., Everitt B.J., Marston H.M., Wilkinson J., Jones G.H., and Page K.J. Comparative effects of ibotenic acid- and quisqualic acid-induced lesions of the substantia innominata on attentional function in the rat: further implications for the role of the cholinergic neurons of the nucleus basalis in cognitive processes. Behav. Brain Res. 35 3 (1989) 221-240
52. Roberts S. Isolation of an internal clock. J. Exp. Psychol. Anim. Behav. Processes 7 (1981) 242-268
53. Santucci A.C., and Haroutunian V. Nucleus basalis lesions impair memory in rats trained on nonspatial and spatial discrimination tasks. Physiol. Behav. 45 5 (1989) 1025-1031
54. Smith H.R., and Pang K.C. Orexin-saporin lesions of the medial septum impair spatial memory. Neuroscience 132 2 (2005) 261-271
55. Tóth K., Freund T.F., and Miles R. Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum. J. Physiol. 500 Pt 2 (1997) 463-474
56. Wallace D.G., and Whishaw I.Q. NMDA lesions of Ammon's horn and the dentate gyrus disrupt the direct and temporally paced homing displayed by rats exploring a novel environment: evidence for a role of the hippocampus in dead reckoning. Eur. J. Neurosci. 18 3 (2003) 513-523
57. Wallace D.G., Wallace P.S., Field E., and Whishaw I.Q. Pharmacological manipulations of food protection behavior in rats: evidence for dopaminergic contributions to time perception during a natural behavior. Brain Res. 1112 1 (2006) 213-221
58. Wallace D.G., Martin M.M., and Winter S.S. Fractionating dead reckoning: role of the compass, odometer, logbook, and home base establishment in spatial orientation. Naturwissenschaften (2008) [Electronic publication ahead of print]
59. Whishaw I.Q. Food wrenching and dodging: use of action patterns for the analysis of sensorimotor and social behavior in the rat. J. Neurosci. Methods 24 (1988) 169-178
60. Whishaw I.Q., and Tomie J.A. Food wresting and dodging: strategies used by rats (Rattus norvegicus) for obtaining and protecting food from conspecifics. J. Comp. Physiol. Psychol. 92 (1987) 474-500
61. Whishaw I.Q., and Tomie J.A. Food wrenching and dodging: a neuroethological test of cortical and dopaminergic contributions to sensorimotor behavior in the rat. Behav. Neurosci. 102 1 (1988) 110-123
62. Whishaw I.Q., and Gorny B.P. Food wrenching and dodging: eating time estimates influence dodge probability and amplitude. Aggress. Behav. 20 (1994) 35-47
63. Whishaw I.Q., Maaswinkel H., Gonzalez C.L., and Kolb B. Deficits in allothetic and idiothetic spatial behavior in rats with posterior cingulate cortex lesions. Behav. Brain Res. 118 1 (2001) 67-76
64. Woolf N.J. Cholinergic systems in mammalian brain and spinal cord. Prog. Neurobiol. 37 6 (1991) 475-524
65. Wrenn C.C., Lappi D.A., and Wiley R.G. Threshold relationship between lesion extent of the cholinergic basal forebrain in the rat and working memory impairment in the radial maze. Brain Res. 847 2 (1999) 284-298
66. Wu M., Shanabrough M., Leranth C., and Alreja M. Cholinergic excitation of septohippocampal GABA but not cholinergic neurons: implications for learning and memory. J. Neurosci. 20 10 (2000) 3900-3908
67. Wu M., Newton S.S., Atkins J.B., Xu C., Duman R.S., and Alreja M. Acetylcholinesterase inhibitors activate septohippocampal GABAergic neurons via muscarinic but not nicotinic receptors. J. Pharmacol. Exp. Ther. 307 2 (2003) 535-543