Abstract
OBJECTIVE—To investigate whether the human cerebellum takes part in fear conditioned potentiation of the acoustic blink reflex. METHODS—A group of 10 cerebellar patients (eight patients with lesions involving the medial cerebellum, two patients with circumscribed lesions of the cerebellar hemispheres) was compared with a group of 16 age and sex matched healthy control subjects. The fear conditioned potentiation paradigm consisted of three phases. During the first, habituation phase subjects received 20 successive acoustic blink stimuli. In the subsequent fear conditioning phase, subjects passed through 20 paired presentations of the unconditioned fear stimulus (US; an electric shock) and the conditioned stimulus (CS; a light). Thereafter, subjects underwent the potentiation phase, which consisted of a pseudorandom order of 12 trials of the acoustic blink stimulus alone, 12 acoustic blink stimuli paired with the conditioned stimulus, and six conditioned stimuli paired with the unconditioned stimulus. The EMG of the acoustic blink reflex was recorded at the orbicularis oculi muscles. The potentiation effect was determined as the difference in normalised peak amplitude of the blink reflex evoked by pairs of CS and acoustic blink stimuli and evoked by the acoustic stimulus alone. RESULTS—In the habituation phase, short term habituation of the acoustic blink reflex was preserved in all cerebellar patients. However, in the potentiation phase, the potentiation effect of the blink reflex was significantly reduced in patients with medial cerebellar lesions compared with the controls (mean (SD) potentiation effect (%), patients: −6.4 (15.3), controls: 21.6 (35.6)), but was within normal limits in the two patients with lateral lesions. CONCLUSIONS—The present findings suggest that the human medial cerebellum is involved in associative learning of non-specific aversive reactions—that is, the fear conditioned potentiation of the acoustic blink reflex.
Full Text
The Full Text of this article is available as a PDF (177.4 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Albert T. J., Dempesy C. W., Sorenson C. A. Anterior cerebellar vermal stimulation: effect on behavior and basal forebrain neurochemistry in rat. Biol Psychiatry. 1985 Dec;20(12):1267–1276. doi: 10.1016/0006-3223(85)90111-8. [DOI] [PubMed] [Google Scholar]
- BROWN J. S., KALISH H. I., FARBER I. E. Conditioned fear as revealed by magnitude of startle response to an auditory stimulus. J Exp Psychol. 1951 May;41(5):317–328. doi: 10.1037/h0060166. [DOI] [PubMed] [Google Scholar]
- Berquin P. C., Giedd J. N., Jacobsen L. K., Hamburger S. D., Krain A. L., Rapoport J. L., Castellanos F. X. Cerebellum in attention-deficit hyperactivity disorder: a morphometric MRI study. Neurology. 1998 Apr;50(4):1087–1093. doi: 10.1212/wnl.50.4.1087. [DOI] [PubMed] [Google Scholar]
- Bloedel J. R., Bracha V. On the cerebellum, cutaneomuscular reflexes, movement control and the elusive engrams of memory. Behav Brain Res. 1995 Apr;68(1):1–44. doi: 10.1016/0166-4328(94)00171-b. [DOI] [PubMed] [Google Scholar]
- Brown P., Rothwell J. C., Thompson P. D., Britton T. C., Day B. L., Marsden C. D. New observations on the normal auditory startle reflex in man. Brain. 1991 Aug;114(Pt 4):1891–1902. doi: 10.1093/brain/114.4.1891. [DOI] [PubMed] [Google Scholar]
- Daum I., Schugens M. M., Ackermann H., Lutzenberger W., Dichgans J., Birbaumer N. Classical conditioning after cerebellar lesions in humans. Behav Neurosci. 1993 Oct;107(5):748–756. doi: 10.1037//0735-7044.107.5.748. [DOI] [PubMed] [Google Scholar]
- Hamm A. O., Greenwald M. K., Bradley M. M., Lang P. J. Emotional learning, hedonic change, and the startle probe. J Abnorm Psychol. 1993 Aug;102(3):453–465. doi: 10.1037//0021-843x.102.3.453. [DOI] [PubMed] [Google Scholar]
- Harding A. E. Clinical features and classification of inherited ataxias. Adv Neurol. 1993;61:1–14. [PubMed] [Google Scholar]
- Hitchcock J., Davis M. Lesions of the amygdala, but not of the cerebellum or red nucleus, block conditioned fear as measured with the potentiated startle paradigm. Behav Neurosci. 1986 Feb;100(1):11–22. doi: 10.1037//0735-7044.100.1.11. [DOI] [PubMed] [Google Scholar]
- Lang P. J., Greenwald M. K., Bradley M. M., Hamm A. O. Looking at pictures: affective, facial, visceral, and behavioral reactions. Psychophysiology. 1993 May;30(3):261–273. doi: 10.1111/j.1469-8986.1993.tb03352.x. [DOI] [PubMed] [Google Scholar]
- Lavond D. G., Lincoln J. S., McCormick D. A., Thompson R. F. Effect of bilateral lesions of the dentate and interpositus cerebellar nuclei on conditioning of heart-rate and nictitating membrane/eyelid responses in the rabbit. Brain Res. 1984 Jul 9;305(2):323–330. doi: 10.1016/0006-8993(84)90438-4. [DOI] [PubMed] [Google Scholar]
- Leaton R. N., Supple W. F., Jr Cerebellar vermis: essential for long-term habituation of the acoustic startle response. Science. 1986 Apr 25;232(4749):513–515. doi: 10.1126/science.3961494. [DOI] [PubMed] [Google Scholar]
- Leaton R. N., Supple W. F., Jr Medial cerebellum and long-term habituation of acoustic startle in rats. Behav Neurosci. 1991 Dec;105(6):804–816. doi: 10.1037//0735-7044.105.6.804. [DOI] [PubMed] [Google Scholar]
- Lipp O. V., Sheridan J., Siddle D. A. Human blink startle during aversive and nonaversive Pavlovian conditioning. J Exp Psychol Anim Behav Process. 1994 Oct;20(4):380–389. [PubMed] [Google Scholar]
- Lopiano L., de'Sperati C., Montarolo P. G. Long-term habituation of the acoustic startle response: role of the cerebellar vermis. Neuroscience. 1990;35(1):79–84. doi: 10.1016/0306-4522(90)90122-k. [DOI] [PubMed] [Google Scholar]
- Powell D. A. Rapid associative learning: conditioned bradycardia and its central nervous system substrates. Integr Physiol Behav Sci. 1994 Apr-Jun;29(2):109–133. doi: 10.1007/BF02691009. [DOI] [PubMed] [Google Scholar]
- Schmahmann J. D., Sherman J. C. The cerebellar cognitive affective syndrome. Brain. 1998 Apr;121(Pt 4):561–579. doi: 10.1093/brain/121.4.561. [DOI] [PubMed] [Google Scholar]
- Supple W. F., Jr, Leaton R. N. Cerebellar vermis: essential for classically conditioned bradycardia in the rat. Brain Res. 1990 Feb 12;509(1):17–23. doi: 10.1016/0006-8993(90)90303-s. [DOI] [PubMed] [Google Scholar]
- Thompson R. F., Krupa D. J. Organization of memory traces in the mammalian brain. Annu Rev Neurosci. 1994;17:519–549. doi: 10.1146/annurev.ne.17.030194.002511. [DOI] [PubMed] [Google Scholar]
- Timmann D., Kolb F. P., Baier C., Rijntjes M., Müller S. P., Diener H. C., Weiller C. Cerebellar activation during classical conditioning of the human flexion reflex: a PET study. Neuroreport. 1996 Aug 12;7(12):2056–2060. doi: 10.1097/00001756-199608120-00041. [DOI] [PubMed] [Google Scholar]
- Timmann D., Musso C., Kolb F. P., Rijntjes M., Jüptner M., Müller S. P., Diener H. C., Weiller C. Involvement of the human cerebellum during habituation of the acoustic startle response: a PET study. J Neurol Neurosurg Psychiatry. 1998 Nov;65(5):771–773. doi: 10.1136/jnnp.65.5.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Trouillas P., Takayanagi T., Hallett M., Currier R. D., Subramony S. H., Wessel K., Bryer A., Diener H. C., Massaquoi S., Gomez C. M. International Cooperative Ataxia Rating Scale for pharmacological assessment of the cerebellar syndrome. The Ataxia Neuropharmacology Committee of the World Federation of Neurology. J Neurol Sci. 1997 Feb 12;145(2):205–211. doi: 10.1016/s0022-510x(96)00231-6. [DOI] [PubMed] [Google Scholar]
- Wilkins D. E., Hallett M., Wess M. M. Audiogenic startle reflex of man and its relationship to startle syndromes. A review. Brain. 1986 Jun;109(Pt 3):561–573. doi: 10.1093/brain/109.3.561. [DOI] [PubMed] [Google Scholar]
- Yeomans J. S., Frankland P. W. The acoustic startle reflex: neurons and connections. Brain Res Brain Res Rev. 1995 Nov;21(3):301–314. doi: 10.1016/0165-0173(96)00004-5. [DOI] [PubMed] [Google Scholar]