Perception of species-specific vocalizations in rats: Role of the cholinergic septo-hippocampal pathway and aging

International Journal of Developmental Neuroscience

Volumn 16, Issue 7-8, 1998, Pages 715-727

  Hörtnagl, Heide ^a,b   Groll Knapp, Elisabeth ^b   Khanakah, Gelas ^b   Sperk, Günther ^c   Bubna Littitz, Hermann ^d  

^a HUMBOLDT UNIVERSITY   (Germany)

^b UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF INNSBRUCK   (Austria)

^d UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

Aging; Alzheimer's disease; Cholinergic septo hippocampal pathway; Event related potentials; Vocalization

Indexed keywords

CHOLINE ACETYLTRANSFERASE;

AGING; ANIMAL EXPERIMENT; ARTICLE; CHOLINERGIC ACTIVITY; CHOLINERGIC SYSTEM; CONTROLLED STUDY; ENZYME ACTIVITY; EVENT RELATED POTENTIAL; EVOKED CORTICAL RESPONSE; HEARING; HIPPOCAMPUS; NONHUMAN; PRIORITY JOURNAL; RAT; THETA RHYTHM; VOCALIZATION;

ACETYLCHOLINE; ACOUSTIC STIMULATION; AGING; ANIMALS; AUDITORY PATHWAYS; AUDITORY PERCEPTION; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, AUDITORY; HIPPOCAMPUS; MALE; NEUROTRANSMITTER AGENTS; RATS; RATS, SPRAGUE-DAWLEY; SEPTUM PELLUCIDUM; SPECIES SPECIFICITY; VOCALIZATION, ANIMAL;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS;

EID: 0345130023     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0736-5748(98)00083-5     Document Type: Article

References (86)

1. Aarsland, D., Larsen, J. P., Reinvang, I. and Aasland, A. M., Effects of cholinergic blockade on language in healthy young women. Implications for the cholinergic hypothesis in dementia of the Alzheimer type. Brain, 1994, 117, 1377-1384.
2. Bartus, R. T., Dean, R. L., Beer, B. and Lippa, S., Cholinergic hypothesis of geriatric memory dysfunction. A critical review. Science, 1982, 217, 408-417.
3. Baxter, M. G., Holland, P. C. and Gallagher, M., Disruption of decrements in conditioned stimulus processing by selective removal of hippocampal cholinergic input. J. Neurosci., 1997, 17, 5230-5236.
4. Berntson, G. G., Boysen, S. T. and Torello, M. W., Vocal perception: brain event-related potentials in a chimpanzee. Develop. Psychobiol., 1993, 26, 305-319.
5. Besson, M., Kutas, M. and Van Petten, C., An event-related potential (ERP) analysis of semantic congruity and repetition effects in sentences. J. Cogn. Neurosci., 1992, 4, 132-149.
6. Bhargava, V. K., Salamy, A. and McLean, C. M., Effects of cholinergic drugs on auditory evoked responses (CER) of rat cortex. Neuropharmacology, 1978, 17, 1009-1013.
7. Blokland, A., Acetylcholine: a neurotransmitter for learning and memory? Brain Res. Rev., 1996, 21, 285-300.
8. Brazhnik, E. S., Vinogradova, O. S., Stafekhina, V. S. and Kitchigina, V. F., Acetylcloline, theta-rhythm and activity of hippocampal neurons in the rabbit - I: spontaneous activity. Neuroscience, 1993, 53, 961-970.
9. Buchwald, J. S., Rubinstein, E. H., Schwafel, J. and Strandburg, R. J., Midlatency auditory evoked responses: differential effects of a cholinergic agonist and antagonist. Electroenceph. Clin. Neurophysiol., 1991, 80, 303-309.
10. Burgess, A. P. and Gruzelier, J. H., Short duration synchronization of human theta rhythm during recognition memory. NeuroReport, 1997, 8, 1039-1042.
11. Buzsáki, G., Grastyán, E., Tveritskaya, I. N. and Czopf, J., Hippocampal evoked potentials and EEG changes during classical conditioning in the rat. Electroenceph. Clin. Neurophysiol., 1979, 47, 64-74.
12. Buzsáki, G., Bickford, R. G., Armstrong, D. M., Ponomareff, G., Chen, K. S., Ruiz, R., Thal, L. J. and Gage, F. H., Electric activity in the neocortex of freely moving young and aged rats. Neuroscience, 1988, 26, 735-744.
13. Carpenter, G. A. and Grossberg, St., Normal and amnesic learning, recognition and memory by a neural model of cortico-hippocampal interactions. Trends Neurosci., 1993, 16, 131-137.
14. Caspers, H., Die Beeinflussung der corticalen Gleichspannung durch sensible und sensorische Reize beim wachen, frei beweglichen Tier. Pflügers Arch., 1960, 272, 53-54.
15. Chrobak, J. J., Hanin, I., Schmechel, D. E. and Walsh, T. J., AF64A-induced working memory impairment: behavioural, neurochemical and histological correlates. Brain Res., 1988, 463, 107-117.
16. Collerton, D., Cholinergic function and intellectual decline in Alzheimer's disease. Review. Neuroscience, 1986, 19, 1-28.
17. David, E., Finkenzeller, P., Kallert, S. and Keidel, W. D., Akustischen Reizen zugeordnete Gleichspannungsänderungen am intakten Schädel des Menschen. Pflügers Arch., 1969, 309, 362-367.
18. Decker, M. W., The effect of aging on hippocampal and cortical projections of the forebrain cholinergic system. Brain Res. Rev., 1987, 12, 423-438.
19. Deutsch, J. A., The cholinergic synapse and the site of memory. Science, 1971, 174, 788-794.
20. Eichenbaum, H., Otto, T. and Cohen, N. J., Two functional components of the hippocampal memory system. Behav. Brain Sci., 1994, 17, 449-518.
21. El Tamer, A., Wulfert, E. and Hanin, I., Age-dependent effect of AF64A on cholinergic activity in the septo-hippocampal pathway of the rat brain: decreased responsiveness in aged rats. Neurosci. Lett., 1996, 203, 123-126.
22. Farwell, L. A. and Donchin, E., The truth will out: Interrogative Polygraphy ("Lie Detection") with event-related brain potentials. Psychophysiology, 1991, 28, 531-547.
23. Felice, L. J., Felice, J. D. and Kissinger, P. T., Determination of catecholamines in rat brain parts by reversed phase ionpair liquid chromatography. J. Neurochem., 1978, 31, 1461-1465.
24. Ferguson, J. H., Jasper, H. M. and Laminar, D. C., Studies of acetylcholine activated epileptiform discharge in cerebral cortex. Electroenceph. Clin. Neurophysiol., 1971, 30, 377-390.
25. Fibiger, H. C., Cholinergic mechanisms in learning, memory and dementia: a review of recent evidence. Trends Neurosci., 1991, 14, 220-223.
26. Fischer, W., Wictorin, K., Björklund, A., Williams, L. R., Varon, S. and Gage, F. H., Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature, 1987, 329, 65-68.
27. Fisher, A., Mantione, C. R., Abraham, D. and Hanin, I., Long-term cholinergic hypofunction induced in mice by ethylcholine aziridinium ion (AF64A) in vivo. J. Pharmaco. Exp. Ther., 1982, 222, 140-145.
28. Fonnum F., Radiochemical microassay for the determination of choline acetyltransferase and acetylcholinesterase activities. Biochem. J., 1969, 115, 465-472.
29. Friedman, D., Cognitive event-related potential components during continuous recognition memory for pictures. Psychophysiology, 1990, 27, 136-148.
30. Goodin, D. S., Clinical utility of long latency "cognitive" event-related potentials (P3): the pros. Electroenceph. Clin. Neurophysiol., 1990, 76, 2-5.
31. Groll-Knapp, E., Haider, M., Kienzl, K., Handler, A. and Trimmel, M., Changes in discrimination learning and brain activity (ERPs) due to combined exposure to NO and CO in rats. Toxicology, 1988, 49, 441-447.
32. Groll-Knapp, E., Haider, M., Trimmel, M. and Hörtnagl, H., Changes in brain functions due to noise and its combination with brain affecting substances. In Noise as a Public Health Problem, ed. M. Vallet. Actes Inrets 34, Vol. 3. INRETS, Arcueil Cedex-France, 1993, pp. 527-534.
33. Gumnit, R. G., DC potential changes from the auditory cortex of cat. J. Neurophysiol., 1960, 23, 667-675.
34. Haider, M., Groll-Knapp, E. and Trimmel, M., Cortical dc shifts related to sustained sensory stimulation and motor activity. In From Neuron to Action, ed. L. Deecke and J. C. Eccles. Springer, New York, 1990, pp. 59-64.
35. Halgren, E., Squires, N. K., Wilson, C. L., Rohrbaugh, J. W., Babb, T. L. and Crandall, P. H., Endogenous potentials generated in the human hippocampal formation and amygdala by infrequent events. Science, 1980, 210, 803-805.
36. Hanin, I., Fisher, A., Hörtnagl, H., Leventer, S. M., Potter, P. E. and Walsh, T. L., Ethylcholine aziridinium (AF64A, ECMA) and other potential cholinergic neuronspecific neurotoxins. In Psychopharmacology: The Third Generation of Progress, ed. H. Y. Melzer. Raven Press, New York, 1987, pp. 341-349.
37. Harrison, J. B., Buchwald, J. S., Kaga, K., Woolf, N. J. and Butcher, L. L., 'Cat P300' disappears after septal lesions. Electroenceph. Clin. Neurophysiol., 1988, 69, 55-64.
38. Hillyard, S. A. and Kutas, M., Electrophysiology of cognitive processing. In Annual Review of Psychology, ed. M. R. Rosenzweig and L. W. Porter, Vol. 34. Palo Alto, California, 1983, pp. 33-61.
39. Hörtnagl, H., Potter, P. E. and Hanin, I., Effect of cholinergic deficit induced by ethylcholine aziridinium (AF64A) on noradrenergic and dopaminergic parameters in rat brain. Brain Res., 1987, 421, 75-84.
40. Hörtnagl, H., Berger, M. L., Sperk, G. and Pifl, C., Regional heterogeneity in the distribution of neurotransmitter markers in the rat hippocampus. Neuroscience, 1991, 45, 261-272.
41. Hörtnagl, H., Hansen, L., Kindel, G., Schneider, B., El Tamer, A. and Hanin, I., Sex differences and estrous cycle-variations in the AF64A-induced cholinergic deficit in the rat hippocampus. Brain Res. Bull., 1993, 31, 129-134.
42. Inglis, F. M. and Fibiger, H. C., Increases in hippocampal and frontal cortical acetylcholine release associated with presentation of sensory stimuli. Neuroscience, 1995, 66, 81-86.
43. Johnson, R., On the neural generators of the P300 component of the event-related potential. Psychophysiology, 1993, 30, 90-97.
44. Johnston, V. S., Miller, D. R. and Burleson, M. H., Multiple P3s to emotional stimuli and their theoretical significance. Psychophysiology, 1986, 23, 684-694.
45. Kesner, R. P., Crutcher, K. A. and Measom, M. O., Medial septal and nucleus basalis magnocellularis lesions produce order memory deficits in rats which mimic symptomatology of Alzheimer's disease. Neurobiol. Aging, 1986, 7, 287-295.
46. Kesner, R. P., Reevaluation of the contribution of the basal forebrain cholinergic system to memory. Neurobiol. Aging, 1988, 9, 609-616.
47. König, J. F. R. and Klippel, R. A., The Rat Brain. A Stereotaxic Atlas of the Forebrain and Lower Parts of the Brain Stem. R. E. Krieger. Huntington, New York, 1970.
48. Leventer, S. M., Wulfert, E. and Hanin, I., Time course of ethylcholine mustard aziridinium ion (AF64A)-induced cholinotoxicity in vivo. Neuropharmacology, 1987, 26, 361-365.
49. Marksteiner, J. and Sperk, G., Concomitant increase of somatostatin, neuropeptide Y and glutamate decarboxylase in frontal cortex of rats with decreased seizure threshold. Neuroscience, 1988, 26, 379-385.
50. McCallum, W. C., Human slow potential research: a review. In Slow Potential Changes in the Human Brain, ed. W. C. McCallum and S. H. Curry. Plenum Press, New York, 1993, pp. 1-12.
51. McCarthy, G. and Wood, C. C., Intercranial recordings and endogeneous ERPs in humans. In The London Symposium, ed. R. J. Ellingson, N. M. F. Murray and A. M. Halliday. Electroenceph. Clin. Neurophysiol., 1987, Suppl. 39, 331-337.
52. Mini, A., Palomba, D., Angrilli, A. and Bravi, S., Emotional information processing and visual evoked brain potentials. Percept. Mot. Skills, 1996, 83, 143-152.
53. Murai, S., Saito, H., Masuda, Y., Odashima, J. and Itoh, T., AF64A disrupts retrieval processes in long-term memory of mice. NeuroReport, 1995, 6, 349-352.
54. Naumann, E., Kaiser, W., Bartussek, D. and Fehm-Wolfsdorf, G., Vasopressin, memory and the late positive complex of the event-related potential. In Psychophysiological Brain Research, ed. C. H. M. Brunia, A. W. K. Gaillard and A. Kok. University Press, Tilburg, 1990, pp. 101-105.
55. Nonmaur, P., Collet, A., Puma, C., Frankel-Kohn, L. and Sharif, A., Relations between acetylcholine release and electrophysiological characteristics of theta rhythm: a microdialysis study in the urethane-anesthetized rat hippocampus. Brain Res. Bull., 1997, 42, 141-147.
56. Okada, Y. C., Kaufman, L. and Williamson, S. J., The Hippocampal formation as a source of the slow endogenous potentials. Electroenceph. Clin. Neurophysiol., 1983, 55, 417-426.
57. O'Keefe, J. and Nadel, L., The Hippocampus as a Cognitive Map. Clarendon Press, Oxford, 1978.
58. Paller, K. A., McCarthy, G. and Wood, C. C., ERPs predictive of subsequent recall and recognition performance. Biol. Psychology, 1988, 26, 269-276.
59. Palomba, D., Angrilli, A. and Mini, A., Visual evoked potentials, heart rate responses and memory to emotional pictorial stimuli. Int. J. Psychophysiol., 1997, 27, 55-67.
60. Petsche, H., Stumpf, C. and Gogolak, G., The significance of the rabbit's septum as a relay station between the midbrain and the hippocampus - I: the control of hippocampus arousal activity by the septum cells. Electroenceph. Clin. Neurophysiol., 1962, 14, 202-211.
61. Pfefferbaum, A., Ford, J. M. and Kraemer, H. C., Clinical utility of long latency "cognitive" event-related potentials (P3): the cons. Electroenceph. Clin. Neurophysiol., 1990, 76, 6-12.
62. Pfleger, W., Schellberg, D., Besthorn, Ch. and Gasser, Th., Emotion and brain: effects of non-verbal affective stimulation on male righthanders. In Psychophysiological Brain Research, ed. C. H. M. Brunia, A. W. K. Gaillard and A. Kok. University Press, Tilburg, 1990, pp. 65-69.
63. Picton, T. W., Woods, D. L. and Proulx, G. B., Human auditory sustained potentials - II: stimulus relationships. Electroenceph. Clin. Neurophysiol., 1978, 45, 198-210.
64. Picton, T. W. and Hillyard, S. A., Endogenous event-related potentials. In Handbook of Electroencephalography and Clinical Neurophysiology: Human Event-Related Potentials, ed. T. W. Picton. Elsevier, Amsterdam, 1988, pp. 361-426.
65. Pineda, J. A., Swick, D. and Foote, S. L., Noradrenergic and cholinergic influences on the genesis of P3-like potentials. In Event-Related Brain Research, ed. C. H. M. Brunia, G. Mulder and M. N. Verbaten. Electroenceph. Clin. Neurophysiol., 1991, Suppl. 42, 165-172.
66. Pittel, Z., Fisher, A. and Heldman, E., Reversible and irreversible inhibition of high-affinity choline transport caused by ethylcholine aziridinium ion. J. Neurochem., 1987, 49, 468-474.
67. Polak, R. L., Molenaar, P. C. and Van Gelder, M., Acetylcholine metabolism and choline uptake in cortical slices. J. Neurochem., 1977, 29, 477-485.
68. Polich, J., P300 in clinical applications: meaning, method and measurements. In Electroencephalography: Basic Principles, Clinical Applications, and Related Fields, ed. E. Niedermeyer and F. Lopes de Silva. William & Wilkins, Baltimore, 1993, pp. 1005-1018.
69. Price, D. L., New perspectives on Alzheimer's disease. Ann. Rev. Neurol., 1986, 9, 489-512.
70. Riekkinen, P. jr, Riekkinen, M., Sirviö, J., Miettinen, R. and Riekkinen, P., Loss of cholinergic neurons in the nucleus basalis induces neocortical electroencephalographic and passive avoidance deficits. Neuroscience, 1992, 47, 823-831.
71. Roberts, E. and Simonson, D. G., Some properties of L-glutamic acid decarboxylase in mouse brain. Biochem. Pharmacol, 1963, 12, 113-134.
72. Ruchkin, D. S. and Sutton, S., Positive slow wave and P300: association and disassociation. In Tutorials in ERP Research: Endogenous Components, ed. A. W. K. Gaillard and W. Ritter. North-Holland Publishing Comp, Amsterdam, 1983, pp. 233-250.
73. Ruchkin, D. S., Sutton, S. and Mahaffey, D., Functional differences between members of the P300 complex: P3E and P3b. Psychophysiology, 1987, 24, 87-103.
74. Rudell, A. P., Cracco, R. Q., Hassan, N. F. and Eberle, L. P., Recognition potential: sensitivity to visual field stimulated. Electroenceph. Clin. Neurophysiol., 1993, 87, 221-234.
75. Sarter, M. and Bruno, J. P., Age-related changes in rodent cortical acetylcholine and cognition: main effects of age vs age as an intervening variable. Brain Res. Rev., 1998, 27, 143-156.
76. Schmid, R., Hong, J. S., Meek, J. and Costa, E., The effect of kainic acid on the hippocampal content of putative neurotransmitter amino acids. Brain Res., 1980, 200, 355-362.
77. Sperk, G., Simultaneous determination of serotonin, 5-hydroxyindoleacetic acid, 3,4 dihydroxyphenylacetic acid and homovanillic acid by high performance liquid chromatography with electrochemical detection. J. Neurochem., 1982, 38, 840-843.
78. Sperk, G. and Widmann, R., Somatostatin precursor in the rat striatum: changes after local injection of kainic acid. J. Neurochem., 1985, 45, 1441-1447.
79. Squires, N. K., Halgren, E., Wilson, Ch. and Crandall, P., Human endogenous limbic potentials: cross-modality and depth/surface comparisons in epileptic subjects. In Tutorials in ERP Research: Endogenous Components, ed. A. W. K. Gaillard and W. Ritter. North-Holland Publishing Comp, Amsterdam, 1983, pp. 217-232.
80. Trimmel, M., DC potentials of the brain. In Clinical and Experimental Neuropsychophysiology, ed. D. Papakostopuolos and I. Martin. Croom Helm, Kent, 1985, pp. 312-338.
81. Tucek, S., Regulation of acetylcholine synthesis in the brain. J. Neurochem., 1985, 44, 11-24.
82. Vinogradova, O. S., Brazhnik, E. S., Kitchigina, V. F. and Stafekhina, V. S., Acetylcholine, theta-rhythm and activity of hippocampal neurons in the rabbit - IV: sensory stimulation. Neuroscience, 1993, 53, 993-1007.
83. Walsh, T. J., Tilson, H. A., DeHaven, D. L., Mailman, R. B., Fisher, A. and Hanin, I., AF64A, a cholinergic neurotoxin selectively depletes acetylcholine in hippocampus and cortex and produces long term passive avoidance and radial arm maze deficits in the rat. Brain Res., 1984, 321, 91-102.
84. Wang, Y. P., Nakashima, K., Shiraishi, Y., Kawai, Y., Ohama, E. and Takahashi, K., P300-like potential disappears in rabbits with lesions in the nucleus basalis of Meynert. Exp. Brain Res., 1997, 114, 288-292.
85. Winkler, J., Suhr, S. T., Gage, F. H., Thal, L. J. and Fisher, L. J., Essential role of neocortical acetylcholine in spatial memory. Nature, 1995, 375, 484-487.
86. Zawia, N., Arendash, G. W. and Wecker, L., Basal forebrain cholinergic neurons in aged rat brain are more susceptible to ibotenate-induced degeneration than neurons in young adult brain. Brain Res., 1992, 589, 333-337.