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Nucleus basalis lesions attenuate aquisition, but not retention, of Pavlovian heart rate conditioning and have no effect on eyeblink conditioning

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Summary

Rabbits with lesions of the anterior nucleus basalis of Meynert (nBM) were compared with animals with sham lesions or unoperated control animals on a classical conditioning task in which heart rate (HR) and eyeblink (EB) conditioned responses (CRs) were as sessed. The nBM lesions impaired the magnitude of the decelerative HR CR, but had no effect on the EB CR. A second experiment, in which animals were lesioned af ter acquisition was complete, showed that anterior nBM lesions had no effect on retention of either the HR or EB CR. These data suggest that the anterior nBM may participate in the early stages of information processing in which stimuli are evaluated for their significance based on their association with a reinforcer. However, the ante rior nBM is apparently not involved in the selection of a somatomotor response to deal effectively with such changing stimulus contingencies.

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References

  1. Albiniak BA, Powell DA (1980) Peripheral autonomie mechanisms and Pavlovian conditioning in the rabbit (Oryctolagus cuniculus). J Comp Physiol Psychol 94: 1101–1113

  2. Altman HJ, Crosland RD, Jenden DJ, Berman RF (1985) Further characterizations of the nature of the behavioral and neurochemical effects of lesions to the nucleus basalis of Meynert in the rat. Neurobiol Aging 6: 125–130

  3. Bartus RT (1980) Cholinergic drug effects on memory and cognition in animals. In: Poon LW (ed) Aging in the 1980's: psychological issues. American Psychological Association, Washington, DC, pp 163–180

  4. Beninger RJ, Wirsching BA, Jhamandas K, Boegman RJ (1989) Animal studies of brain acetylcholine and memory. Arch Gerontol Geriatr, 1: 71–90

  5. Bigl V, Woolf NJ, Butcher LL (1982) Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital, and cingulate cortices: a combined fluorescent tracer and acetylcholinesterase analysis. Brain Res Bull, 8: 727–763

  6. Buchanan SL, Powell DA (1982a) Cingulate cortex: its role in Pavlovian conditioning. J Comp Physiol Psychol, 96: 755–774

  7. Buchanan SL, Powell DA (1982b) Cingulate damage attenuates conditioned bradycardia. Neurosci Lett, 29: 261–268

  8. Bull G, Oderfeld-Nowak C (1971) Standardization of a radiochemical assay of choline acetyltransferase and a study of the activation of the enzyme in rabbit brain. J Neurochem 18: 935–941

  9. Davies P (1985) A critical review of the role of the cholinergic system in human memory and cognition. Ann NY Acad Sci 444: 212–217

  10. Davis KL, Yamamura HI (1978) Cholinergic underactivity in human memory disorders. Life Sci 23: 1729–1734

  11. Dawson ME, Schell AM (1987) Human autonomie and skeletal classical conditioning: the role of conscious cognitive factors. In: Davey G (ed) Cognitive processes and Pavlovian conditioning in humans. John Wiley and Sons, New York, pp 27–55

  12. Deutsch JA (1971) The cholinergic synapse and the site of memory. Science 174: 788–794

  13. Dohanich GP, McEwen BS (1986) Cholinergic limbic projections and behavioral role of basal forebrain nuclei in the rat. Brain Res Bull 16: 477–482

  14. Downs D, Cardozo C, Schneiderman N, Yehle AL, Van Dercar DH, Zwilling G (1972) Central effects of atropine upon aversive classical conditioning in rabbits. Psychopharmologia 23: 319–333

  15. Drachman DA, Leavitt J (1974) Human memory and the cholinergic system. Arch Neurol 30: 113–121

  16. El-Defrawy SR, Coloma F, Jhamandas K, Boegman RJ, Beninger RJ, Wirsching BA (1985) Functional and neurochemical cortical cholinergic impairment following neurotoxic lesions of the nucleus basalis magnocellularis in the rat. Neurobiol aging 6: 325–330

  17. Everitt BJ, Robbins TW, Evenden JL, Marston HM, Jones GH, Sirkia TE (1987) The effects of excitotoxic lesions of the substantia innominata, ventral and dorsal globus pallidus on the acquisition and retention of a conditional visual discrimination: implications for cholinergic hypotheses of learning and memory. Neuroscience 22: 441–469

  18. Furedy JJ (1971) Explicitly-unpaired and truly-random CS-controls in human classical differential autonomic conditioning. Psychophysiology 8: 497–503

  19. Gentile CG, Jarrell TW, Teich AH, McCabe P, Schneiderman N (1986) The role of amygdaloid central nucleus in the retention of differential Pavlovian conditioning of bradycardia in rabbits. Behav Brain Res 20: 263–273

  20. Gibbs CM, Powell DA (1988) Neuronal correlates of classically conditioned bradycardia in the rabbit: studies of the medial prefrontal cortex. Brain Res 442: 86–96

  21. Girgis M, Shih-Chang W (1981) Stereotaxic atlas of the rabbit brain. St. Louis Warren H. Green, Inc

  22. Gormezano I, Kehoe EJ, Marshall BS (1983) Twenty years of classical conditioning research with the rabbit. Prog Psychobiol Physiol Psychol 10: 197–275

  23. Hernandez LL, Buchanan SL, Powell DA (1987) Somatomotor thresholds in the New Zealand albino rabbit. Psychol Rep 61: 265–266

  24. Kao K-T, Powell DA (1988) Lesions of the substantia nigra retard Pavlovian eyeblink but not heart rate conditioning in the rabbit. Behav Neurosci 102: 515–525

  25. Kapp BS, Frysinger RC, Gallagher M, Haselton JR (1979) Amygdala central nucleus lesions: effect on heart rate conditioning in the rabbit. Physiol Behav 23: 1109–1117

  26. Kazis E, Milligan WL, Powell DA (1973) Autonomic-somatic relationships: blockade of heart rate and corneoretinal potential. J Comp Physiol Psych 84: 98–110

  27. Kesner RP, Adelstein T, Crutcher KA (1987) Rats with nucleus basalis magnocellularis lesions mimic mnemonic symptomatology observed in patients with dementia of the Alzheimer's type. Behav Neurosci 101: 451–456

  28. Lacey JI, Lacey BC (1971) Some autonomic-central nervous system interrelationships. In: Black P (ed) Physiological correlates of emotion Academic Press, New York, pp 205–227

  29. LeDoux JE, Iwata J, Cicchetti P, Reis DJ (1988) Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci 8: 2517–2529

  30. Lippa AS, Pelham RW Beer B, Critchett DJ, Dean RL, Bartus RT (1980) Brain cholinergic dysfunction and memory in aged rats. Neurobiol Aging 1: 13–19

  31. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193: 265–275

  32. Mackintosh NJ (1983) Conditioning and associative learning. Oxford University Press, New York

  33. McCormick DA, Lavond DG, Clark GA, Kettner RE, Rising CE, Thompson RF (1981) The engram found? Role of the cerebellum in classical conditioning of nictitating membrane and eyelid response. Bull Psycho Soc 18: 103–105

  34. Mesulam MM, Mufson EJ, Levey AI, Wainer BH (1982) Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol 214: 170–197

  35. Mesulam MM, Mufson EJ, Levey AI, Wainer BH (1984) Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Neuroscience 12: 669–686

  36. Mishkin M, Petri HL (1984) Memories and habits: some implications for the analysis of learning and retention. In: Squire LR, Butters N (eds) Neuropsychology of memory. The Guilford Press, New York, pp 287–296

  37. Moore JW, Goodell NA, Solomon PR (1976) Central cholinergic blockade by scopolamine and habituation, classical conditioning, and latent inhibition of the rabbit's nictitating membrane response. Physiol Psych 4: 395–399

  38. Powell DA (1979) Peripheral and central muscarinic cholinergic blockade: effects on Pavlovian conditioning. Bull Psychon Soc 14: 161–164

  39. Powell DA, Buchanan SL, Gibbs CM (1990) Role of the prefrontalthalamic axis in classical conditioning. In: Uylings HMB, Van Eden CG, De Bruin JPC, Corner MA, Feenstra MGP (eds), The prefrontal cortex: its structure, function and pathology. Progress in Brain Research, Vol. 85 Elsevier, Amsterdam, The Netherlands pp 423–456

  40. Powell DA, Buchanan SL, Hernandez LL (1991) Classical (Pavlovian) conditioning models of age-related changes in associative learning and their neurobiological substrates. Prog Neurobiol 36: 201–228

  41. Powell DA, Joseph JA (1974) Autonomic-somatic interaction and hippocampal theta activity. J Comp Physiol Psychol 87: 978–986

  42. Powell DA, Kazis E (1976) Blood pressure and heart rate changes accompanying classical eyeblink conditioning in the rabbit (Oryctolagus cuniculus). Psychophysiology 13: 441–447

  43. Powell DA, Levine-Bryce D (1988) A comparison of two model systems of associative learning: heart rate and eyeblink conditioning in the rabbit. Psychophysiology 25: 672–682

  44. Powell DA, Levine-Bryce D (1989) Conditioned bradycardia in the rabbit: effects of knife cuts and ibotenic acid lesions in the lateral hypothalamus. Exp Brain Res 76: 103–121

  45. Powell DA, Mankowski D, Buchanan S (1978) Concomitant heart rate and corneoretinal potential conditioning in the rabbit (Oryctolagus cuniculus): effects of caudate lesions. Physiol Behav 20: 143–150

  46. Pribram KH, McGuinness D (1975) Arousal, activation and effort in the control of attention. Psychol Rev 82: 116–149

  47. Rescorla RA (1988) Pavlovian conditioning — its not what you think it is. Am Psychol 43: 151–160

  48. Rigdon GC, Pirch JH (1984) Microinjection of procaine or GABA into the nucleus basalis magnocellularis affects cue-elicited unit responses in the rat frontal cortex. Exp Neurol 85: 283–296

  49. Robbins TW, Everitt BJ, Ryan CN, Marston HM, Jones GH, Page KJ (1989) Comparative effects of quisqualic and ibotenic acid-induced lesions of the substantia innominata and globus pallidus on the aquisition of a conditional visual discrimination: differential effects on cholinergic mechanisms. Neuroscience 28: 337–352

  50. Rosenfield ME, Moore JW (1983) Red nucleus lesions disrupt the classically conditioned nictitating membrane response in rabbits. Behav Brain Res 10: 393–398

  51. Schwaber JS, Kapp BS, Higgins GA, Rapp PR (1982) Amygdaloid and basal forebrain direct connections with the nucleus of the solitary tract and the dorsal motor nucleus. J Neurosci 2: 1424–1438

  52. Soloman PR, Gottfried KE (1981) The septohippocampal cholinergic system and classical conditioning of the rabbit's nictitating membrane response. J Comp Physiol Psychol 95: 322–330

  53. Spencer DG, Lal H (1983) Effects of anticholinergic drugs on learning and memory. Drug Dev Res 3: 489–502

  54. Squire LR (1986) Mechanisms of memory. Science 232: 1612–1619

  55. Stephens PH, Cuello AC, Sofroniew MV, Pearson RCA, Tagari P (1985) Effect of unilateral decortication on choline acetyltransferase activity in the nucleus basalis and other areas of the rat brain. J Neurochem 45: 1021–1026

  56. Thompson RF (1986) The neurobiology of learning and memory. Science 233: 941–947

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Correspondence to D. A. Pow1ell.

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Ginn, S.R., Pow1ell, D.A. Nucleus basalis lesions attenuate aquisition, but not retention, of Pavlovian heart rate conditioning and have no effect on eyeblink conditioning. Exp Brain Res 89, 501–510 (1992). https://doi.org/10.1007/BF00229874

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Key words

  • nBM
  • Classical conditioning
  • Lesions
  • Heart rate
  • Eyeblink
  • Rabbits