Effects of cholinergic enhancement on conditioning-related responses in human auditory cortex

European Journal of Neuroscience

Volumn 16, Issue 11, 2002, Pages 2199-2206

  Thiel, C M ^a,b   Bentley, P ^b   Dolan, R J ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

Acetylcholine; Learning; Neuroimaging; Plasticity; Psychopharmacology

Indexed keywords

CHOLINESTERASE INHIBITOR; PHYSOSTIGMINE; PLACEBO;

ADULT; ARTICLE; AUDITORY CORTEX; AVERSIVE BEHAVIOR; BLOOD OXYGENATION; CHOLINERGIC STIMULATION; CHOLINERGIC SYSTEM; CLINICAL TRIAL; CONDITIONING; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; ELECTRIC SHOCK; FEMALE; HUMAN; MALE; NAUSEA; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; STIMULUS RESPONSE; VOMITING; XEROSTOMIA;

EID: 0036454892     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02272.x     Document Type: Article

References (52)

1. Acquas, E., Wilson, C. & Fibiger, H.C. (1996) Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: Effects of novelty, habituation and fear. J. Neuroscience, 16, 3089-3096.
2. Ashburner, J. & Friston, K. (1999) Nonlinear spatial normalization using basis functions. Human Brain Mapping, 7, 254-266.
3. Ashe, J.H., McKenna, T.M. & Weinberger, N.M. (1989) Cholinergic modulation of frequency receptive fields in auditory cortex. II. Frequency-specific effects of anticholinesterases provide evidence for a modulatory action of endogenous ACh. Synapse, 4, 44-54.
4. Asthana, S., Raffaele, K.C., Berardi, A., Greig, N.H., Haxby, J.V., Schapiro, M.B. & Soncrant, T.T. (1995) Treatment of Alzheimer disease by continuous intravenous infusion of physostigmine. Alzheimer Dis. Assoc. Disord., 9, 223-232.
5. Bakin, J.S. & Weinberger, N.M. (1990) Classical conditioning induces CS-specific receptive field plasticity in the auditory cortex of the guinea pig. Brain Res., 536, 271-286.
6. Bond, A. & Lader, M. (1974) The use of analogue scales in rating subjective feelings. Br. J. Med. Psychol., 47, 211-218.
7. Buchel, C., Morris, J., Dolan, R.J. & Friston, K.J. (1998) Brain systems mediating aversive conditioning: An event-related fMRI study. Neuron, 20, 947-957.
8. Davis, K.L., Hollister, L.E., Overall, J., Johnson, A. & Train, K. (1976) Physostigmine: Effects on cognition and affect in normal subjects. Psychoparmacologia, 51, 23-27.
9. Davis, K.L. & Mohs, R.C. (1982) Enhancement of memory processes in Alzheimer's disease with multiple-dose intravenous physostigmine. Am. J. Psychiatry, 139, 1421-1424.
10. Descarries, L., Gisiger, V. & Steriade, M. (1997) Diffuse transmission by acetylcholine in the CNS. Prog. Neurobiol., 53, 603-625.
11. Edeline, J.M. (1999) Learning-induced physiological plasticity in the thalamo-cortical sensory systems: A critical evaluation of receptive field plasticity, map changes and their potential mechanisms. Prog. Neurobiol., 57, 165-224.
12. Everitt, B.J. & Robbins, T.W. (1997) Central cholinergic systems and cognition. Annu. Rev. Psychol., 48, 649-684.
13. Friston, K.J., Holmes, A.P., Price, C.J., Buchel, C. & Worsley, K.J. (1999) Multisubject fMRI studies and conjunction analyses. Neuroimage, 10, 385-396.
14. Friston, K.J., Holmes, A.P., Worsley, K.J., Poline, J.-P., Frith, C.D. & Frackowiak, R.S. (1995) Statistical parametric maps in functional imaging: A general linear approach. Hum. Brain Mapp., 2, 189-210.
15. Furey, M.L., Pietrini, P., Alexander, G.E., Mentis, M.J., Szczepanik, J., Shetty, U., Greig, N.H., Holloway, H.W., Schapiro, M.B. & Freo, U. (2000a) Time course of pharmacodynamic and pharmacokinetic effects of physostigmine assessed by functional brain imaging in humans. Pharmacol. Biochem. Behav., 66, 475-481.
16. Furey, M.L., Pietrini, P. & Haxby, J.V. (2000b) Cholinergic enhancement and increased selectivity of perceptual processing during working memory. Science, 290, 2315-2319.
17. Furey, M.L., Pietrini, P., Haxby, J.V., Alexander, G.E., Lee, H.C., VanMeter, J., Grady, C.L., Shetty, U., Rapoport, S.I., Schapiro, M.B. & Freo, U. (1997) Cholinergic stimulation alters performance and task-specific regional cerebral blood flow during working memory. Proc. Natl Acad. Sci. U S A, 94, 6512-6516.
18. Grasby, P.M., Frith, C.D., Paulesu, E., Friston, K.J., Frackowiak, R.S. & Dolan, R.J. (1995) The effect of the muscarinic antagonist scopolamine on regional cerebral blood flow during the performance of a memory task. Exp. Brain Res., 104, 337-348.
19. Hars, B., Maho, C., Edeline, J.M. & Hennevin, E. (1993) Basal forebrain stimulation facilitates tone-evoked responses in the auditory cortex of awake rat. Neuroscience, 56, 61-74.
20. Hasselmo, M.E. (1995) Neuromodulation and cortical function: Modeling the physiological basis of behavior. Behav. Brain Res., 67, 1-27.
21. Holley, L.A., Turchi, J., Apple, C. & Sarter, M. (1995) Dissociation between the attentional effects of infusions of a benzodiazepine receptor agonist and an inverse agonist into the basal forebrain. Psychopharmacology (Berl), 120, 99-108.
22. Josephs, O. & Henson, R.N. (1999) Event-related functional magnetic resonance imaging: Modelling, inference and optimization. Philos. Trans. R. Soc. Lond. B Biol. Sci., 354, 1215-1228.
23. Kimura, F., Fukuda, M. & Tsumoto, T. (1999) Acetylcholine suppresses the spread of excitation in the visual cortex revealed by optical recording: Possible differential effect depending on the source of input. Eur. J. Neurosci., 11, 3597-3609.
24. Krnjevic, K. & Phillis, J.W. (1963) Acetylcholine-sensitive cells in the cerebral cortex. J. Physiol. (Lond.), 166, 296-327.
25. Maho, C., Hars, B., Edeline, J.M. & Hennevin, E. (1995) Conditioned changes in the basal forebrain: Relations with learning-induced cortical plasticity. Psychobiology, 23, 10-25.
26. McLin, D.E. III, Miasnikov, A.A. & Weinberger, N.M. (2002) Induction of behavioral associative memory by stimulation of the nucleus basalis. Proc. Natl Acad. Sci. U S A, 99, 4002-4007.
27. Messamore, E., Warpman, U., Ogane, N. & Giacobini, E. (1993) Cholineserase inhibitor effects on extracellular acetylcholine in rat cortex. Neuropharmacology, 32, 745-750.
28. Metherate, R. & Ashe, J.H. (1991) Basal forebrain stimulation modifies auditory cortex responsiveness by an action at muscarinic receptors. Brain Res., 559, 163-167.
29. Miasnikov, A.A., McLin, D. & Weinberger, N.M. (2001) Muscarinic dependence of nucleus basalis induced conditioned receptive field plasticity. Neuroreport, 12, 1537-1542.
30. Molchan, S.E., Sunderland, T., McIntosh, A.R., Herscovitch, P. & Schreurs, B.G. (1994) A functional anatomical study of associative learning in humans. Proc. Natl Acad. Sci. U S A, 91, 8122-8126.
31. Moore, H., Stuckman, S., Sarter, M. & Bruno, J.P. (1995) Stimulation of cortical acetylcholine efflux by FG 7142 measured with repeated microdialysis sampling. Synapse, 21, 324-331.
32. Pirch, J.H., Turco, K. & Rucker, H.K. (1992) A role for acetylcholine in conditioning-related responses of rat frontal cortex neurons: Microiontophoretic evidence. Brain Res., 586, 19-26.
33. Quigley, K.S., Sarter, M.F., Hart, S.L. & Berntson, G.G. (1994) Cardiovascular effects of the benzodiazepine receptor partial inverse agonist FG 7142 in rats. Behav. Brain Res., 62, 11-20.
34. Rasmusson, D.D. (2000) The role of acetylcholine in cortical synaptic plasticity. Behav. Brain Res., 115, 205-218.
35. Rivier, F. & Clarke, S. (1997) Cytochrome oxidase, acetylcholinesterase, and NADPH-diaphorase staining in human supratemporal and insular cortex: Evidence for multiple auditory areas. Neuroimage, 6, 288-304.
36. Rosier, A.M., Cornette, L., Dupont, P., Bormans, G., Mortelmans, L. & Orban, G.A. (1999) Regional brain activity during shape recognition impaired by a scopolamine challenge to encoding. Eur. J. Neurosci., 11, 3701-3714.
37. Sahakian, B.J. (1988) Cholinergic drugs and human cognitive performance. In Iversen, L.L., Iversen, S.D. & Snyder, S.H. (eds), Handbook of Psychopharmacology, Vol. 20. Plenum Press, New York and London, pp. 393-424.
38. Sarter, M. & Bruno, J.P. (1997) Cognitive functions of cortical acetylcholine: Toward a unifying hypothesis. Brain Res. Rev., 23, 28-46.
39. Sato, H., Hata, Y., Masui, H. & Tsumoto, T. (1987) A functional role of cholinergic innervation to neurons in the cat visual cortex. J. Neurophysiol., 58, 765-780.
40. Schreurs, B.G., McIntosh, A.R., Bahro, M., Herscovitch, P., Sunderland, T. & Molchan, S.E. (1997) Lateralization and behavioral correlation of changes in regional cerebral blood flow with classical conditioning of the human eyeblink response. J. Neurophysiol., 77, 2153-2163.
41. Sperling, R., Greve, D., Dale, A., Killiany, R., Holmes, J., Rosas, H.D., Cocchiarella, A., Firth, P., Rosen, B., Lake, S., Lange, N., Routledge, C. & Albert, M. (2002) Functional MRI detection of pharmacologically induced memory impairment. Proc. Natl. Acad. Sci. U.S.A, 99, 455-460.
42. Sweeney, J.E., Bachman, E.S. & Coyle, J.T. (1990) Effects of different doses of galanthamine, a long-acting acetylcholinesterase inhibitor, on memory in mice. Psychopharmacology (Berl), 102, 191-200.
43. Tailairach, J. & Tournoux, P. (1988) Co-Planar Stereotaxic A+L as of the Human Brain, George Thieme Verlag, Stuttgart.
44. Tandon, R., Greden, J.F. & Haskett, R.F. (1993) Cholinergic hyperactivity and negative symptoms: Behavioral effects of physostigmine in normal controls. Schizophr. Res., 9, 19-23.
45. Thiel, C.M., Friston, K.J. & Dolan, R.J. (2002a) Cholinergic modulation of experience-dependent plasticity in human auditory cortex. Neuron, 35, 567-574.
46. Thiel, C.M., Henson, R.A., Morris, J.S., Friston, K.J. & Dolan, R.J. (2001) Pharmacological modulation of behavioural and neuronal correlates of repetition priming. J. Neuroscience, 21, 6846-6852.
47. Thiel, C.M., Huston, J.P. & Schwarting, R.K.W. (1998) Cholinergic activation in frontal cortex and nucleus accumbens related to basic behavioral manipulations. Handling and the role of post-handling experience. Brain Res., 812, 121-132.
48. Tremblay, N., Warren, R.A. & Dykes, R.W. (1990) Electrophysiological studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat. II. Cortical neurons excited by somatic stimuli. J. Neurophysiol., 64, 1212-1222.
49. Tsukada, H., Sato, K., Kakiuchi, T. & Nishiyama, S. (2000) Age-related impairment of coupling mechanism between neuronal activation and functional cerebral blood flow response was restored by cholinesterase inhibition: PET study with microdialysis in the awake monkey brain. Brain Res., 857, 158-164.
50. Vitiello, B., Martin, A., Hill, J., Mack, C., Molchan, S., Martinez, R., Murphy, D.L. & Sunderland, T. (1997) Cognitive and behavioral effects of cholinergic, dopaminergic, and serotonergic blockade in humans. Neuropsychopharmacology, 16, 15-24.
51. Xiang, Z., Huguenard, J.R. & Prince, D.A. (1998) Cholinergic switching within neocortical inhibitory networks. Science, 281, 985-988.
52. Zilles, K. & Palomero-Gallagher, N. (2001) Cyto-, myelo-, and receptor architectonics of the human parietal cortex. Neuroimage, 14, S8-S20.