Exploration of cerebellar-dependent associative learning in schizophrenia: Effects of varying and shifting interstimulus interval on eyeblink conditioning

Behavioral Neuroscience

Volumn 125, Issue 5, 2011, Pages 687-698

  Bolbecker, Amanda R ^a   Steinmetz, Adam B ^b   Mehta, Crystal S ^c   Forsyth, Jennifer K ^a   Klaunig, Mallory J ^a   Lazar, Emily K ^b,d   Steinmetz, Joseph E ^e   O'Donnell, Brian F ^a,f   Hetrick, William P ^a,f  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c A T STILL UNIVERSITY   (United States)

^d BUTLER UNIVERSITY   (United States)

^e OHIO STATE UNIVERSITY   (United States)

^f INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Associative learning; Cerebellum; Eyeblink conditioning; Interstimulus interval; Schizophrenia

Indexed keywords

ACTION POTENTIAL; ADULT; AGE; ARTICLE; CEREBELLUM DISEASE; CONDITIONED REFLEX; CONTROLLED STUDY; DIAGNOSTIC AND STATISTICAL MANUAL OF MENTAL DISORDERS; EYELID REFLEX; FEMALE; HUMAN; INTERSTIMULUS INTERVAL; LATENT PERIOD; MAJOR CLINICAL STUDY; MALE; SCHIZOPHRENIA; STATE DEPENDENT LEARNING; STIMULUS RESPONSE; SYMPTOMATOLOGY;

ADULT; ASSOCIATION LEARNING; CEREBELLUM; CONDITIONING, CLASSICAL; CONDITIONING, EYELID; FEMALE; HUMANS; MALE; MIDDLE AGED; REACTION TIME; SCHIZOPHRENIA;

EID: 80053605111     PISSN: 07357044     EISSN: 19390084     Source Type: Journal    
DOI: 10.1037/a0025150     Document Type: Article

References (58)

1. Andreasen N.C., Paradiso S., O'Leary D.S. " Cognitive dysmetria" as an integrative theory of schizophrenia: A dysfunction in cortical-subcortical-cerebellar circuitry?. Schizophrenia Bulletin 1998, 4:203-218.
2. Andreasen N.C., Pierson R. The role of the cerebellum in schizophrenia. Biological Psychiatry 2008, 64:81-88. 10.1016/j.biopsych.2008.01.003.
3. Avanzino L., Bove M., Tacchino A., Ruggeri P., Giannini A., Trompetto C., Abbruzzese G. Cerebellar involvement in timing accuracy of rhythmic finger movements in essential tremor. European Journal of Neuroscience 2009, 30:1971-1979.
4. Bolbecker A.R., Hetrick W.P., Johannesen J.K., O'Donnell B.F., Steinmetz J.E., Shekhar A.S. Secretin effects on cerebellar-dependent motor learning in schizophrenia. American Journal of Psychiatry 2009, 166:460-466. 10.1176/appi.ajp.2008.08040597.
5. Bolbecker A.R., Mehta C., Johannesen J.K., Edwards C.R., O'Donnell B.F., Shekhar A., Hetrick W.P. Eyeblink conditioning anomalies in bipolar disorder suggest cerebellar dysfunction. Bipolar Disorders 2009, 11:19-32. 10.1111/j.1399-5618.2008.00642.x.
6. Bolbecker A.R., Mehta C.S., Edwards C.R., Steinmetz J.E., O'Donnell B.F., Hetrick W.P. Eye-blink conditioning deficits indicate temporal processing abnormalities in schizophrenia. Schizophrenia Research 2009, 111:182-191. 10.1016/j.schres.2009.03.016.
7. Brown S.M., Kieffaber P.D., Carroll C.A., Vohs J.L., Tracy J.A., Shekhar A., Hetrick W.P. Eyeblink conditioning deficits indicate timing and cerebellar abnormalities in schizophrenia. Brain & Cognition 2005, 58:94-108. 10.1016/j.bandc.2004.09.011.
8. Christian K.M., Thompson R.F. Neural substrates of eyeblink conditioning: Acquisition and retention. Learning & Memory 2003, 10:427-455. 10.1101/lm.59603.
9. Cohen J. Eta-squared and partial eta-squared in communication science. Human Communication Research 1973, 28:473-490.
10. Demirtas-Tatlidede A., Freitas C., Cromer J.R., Safar L., Ongur D., Stone W.S., Pascual-Leone A. Safety and proof of principle study of cerebellar vermal theta burst stimulation in refractory schizophrenia. Schizophrenia Research 2010, 124:91-100. 10.1016/j.schres.2010.08.015.
11. Edwards C.R., Newman S., Bismark A., Skosnik P.D., O'Donnell B.F., Shekhar A., Hetrick W.P. Cerebellum volume and eyeblink conditioning in schizophrenia. Psychiatry Research 2008, 162:185-194. 10.1016/j.pscychresns.2007.06.001.
12. First M., Spitzer R.L., Williams J.B.W., Gibbon M. Structured Clinical Interview for DSM-IV (SCID) 1995, American Psychiatric Association, Washington, DC.
13. Forsyth, J. K., Bolbecker, A. R., Mehta, C. S., Klaunig, M. J., Steinmetz, J. E., O'Donnell, B. F., & Hetrick, W. P. (2010). Cerebellar-Dependent Eyeblink Conditioning Deficits in Schizophrenia Spectrum Disorders. Schizophrenia Bulletin. [Epub ahead of print] PubMed PMID: 21148238.
14. Freed W. Eye-blink rates and platelet monoamine oxidase activity in chronic schizophrenic patients. Biological Psychiatry 1980, 15:329-332.
15. Garcia K.S., Steele P.M., Mauk M.D. Cerebellar cortex lesions prevent acquisition of conditioned eyelid responses. Journal of Neuroscience 1999, 19:10940-10947.
16. Ho B.C., Mola C., Andreasen N.C. Cerebellar dysfunction in neuroleptic naïve schizophrenia patients: Clinical, cognitive, and neuroanatomic correlates of cerebellar neurologic signs. Biological Psychiatry 2004, 55:1146-1153. 10.1016/j.biopsych.2004.02.020.
17. Hofer E., Doby D., Anderer P., Dantendorfer K. Impaired conditional discrimination learning in schizophrenia. Schizophrenia Research 2001, 51:127-136. 10.1016/S0920-9964(00)00118-3.
18. Honey G.D., Pomarol-Clotet E., Corlett P.R., Honey R.A., McKenna P.J., Bullmore E.T., Fletcher P.C. Functional dysconnectivity in schizophrenia associated with attentional modulation of motor function. Brain 2005, 128:2597-2611. 10.1093/brain/awh632.
19. Ichimiya T., Okubo Y., Suhara T., Sudo Y. Reduced volume of the cerebellar vermis in neuroleptic-naive schizophrenia. Biological Psychiatry 2001, 49:20-27. 10.1016/S0006-3223(00)01081-7.
20. Ivry R.B., Keele S.W. Timing of functions of the cerebellum. Journal of Cognitive Neuroscience 1989, 1:136-152. 10.1162/jocn.1989.1.2.136.
21. Ivry R.B., Keele S.W., Diener H.C. Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Experimental Brain Research 1988, 73:167-180. 10.1007/BF00279670.
22. Katz D.B., Steinmetz J.E. Psychological functions of the cerebellum. Behavioral and Cognitive Neuroscience Reviews 2002, 1:229-241. 10.1177/1534582302001003004.
23. Kim J.J., Thompson R.F. Cerebellar circuits and synaptic mechanisms involved in classical eyeblink conditioning. Trends in Neurosciences 1997, 20:177-181. 10.1016/S0166-2236(96)10081-3.
24. Lang P.J., Greenwald M.K. The International Affective Picture System standardization procedure and initial group results for affective judgements: Technical Report 1A 1988, The Center for Research in Psychophysiology, University of Florida, Gainseville, FL.
25. Lavond D.G., Kim J.J., Thompson R.F. Mammalian brain substrates of aversive classical conditioning. Annual Review of Psychology 1993, 44:317-342. 10.1146/annurev.ps.44.020193.001533.
26. Lavond D.G., Steinmetz J.E. Acquisition of classical conditioning without cerebellar cortex. Behavioural Brain Research 1989, 33:113-164. 10.1016/S0166-4328(89)80047-6.
27. Leiner H.C., Leiner A.L., Dow R.S. Does the cerebellum contribute to mental skills?. Behavioral Neuroscience 1986, 100:443-454. 10.1037/0735-7044.100.4.443.
28. Marenco S., Weinberger D.R., Schreurs B.G. Single-cue delay and trace classical conditioning in schizophrenia. Biological Psychiatry 2003, 53:390-402. 10.1016/S0006-3223(02)01506-8.
29. McAllister W.R. The effect on eyelid conditioning of shifting the CS-US interval. Journal of Experimental Psychology 1953, 45:423-428. 10.1037/h0057118.
30. Middleton F.A., Strick P.L. Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. Science 1994, 266:458-461.
31. Middleton F.A., Strick P.L. Cerebellar projections to the prefrontal cortex of the primate. Journal of Neuroscience 2001, 21:700-712.
32. Nopoulos P.C., Ceilley J.W., Gailis E.A., Andreasen N.C. An MRI study of cerebellar vermis morphology in patients with schizophrenia: Evidence in support of the cognitive dysmetria concept. Biological Psychiatry 1999, 46:703-711. 10.1016/S0006-3223(99)00093-1.
33. Okugawa G., Nobuhara K., Minami T., Takase K., Sugimoto T., Saito Y., Kinoshita T. Neural disorganization in the superior cerebellar peduncle and cognitive abnormality in patients with schizophrenia: A diffusion tensor imaging study. Progress in Neuropsychopharmacology & Biological Psychiatry 2006, 30:1408-1412.
34. Okugawa G., Nobuhara K., Sugimoto T., Kinoshita T. Diffusion tensor imaging study of the middle cerebellar peduncles in patients with schizophrenia. Cerebellum 2005, 4:123-127. 10.1080/14734220510007879.
35. Perrett S.P., Ruiz B.P., Mauk M.D. Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. Journal of Neuroscience 1993, 13:1708-1718.
36. Picard H., Amado I., Mouchet-Mages S., Olie J.P., Krebs M.O. The role of the cerebellum in schizophrenia: An update of clinical, cognitive, and functional evidences. Schizophrenia Bulletin 2008, 34:155-172. 10.1093/schbul/sbm049.
37. Ramnani N., Behrens T.E., Johansen-Berg H., Richter M.C., Pinsk M.A., Andersson J.L., Matthews P.M. The evolution of prefrontal inputs to the cortico-pontine system: diffusion imaging evidence from Macaque monkeys and humans. Cerebral Cortex 2006, 16:811-818.
38. Schmahmann J.D. Disorders of the cerebellum: Ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. Journal of Neuropsychiatry and Clinical Neurosciences 2004, 16:367-378. 10.1176/appi.neuropsych.16.3.367.
39. Schmahmann J.D., Pandya D.N. Prefrontal cortex projections to the basilar pons in rhesus monkey: Implications for the cerebellar contribution to higher function. Neuroscience Letters 1995, 199:175-178. 10.1016/0304-3940(95)12056-A.
40. Schmahmann J.D., Sherman J.C. The cerebellar cognitive affective syndrome. Brain 1998, 121:561-579. 10.1093/brain/121.4.561.
41. Schutter D.J., van Honk J. The cerebellum on the rise in human emotion. Cerebellum 2005, 4:290-294. 10.1080/14734220500348584.
42. Sears L.L., Andreasen N.C., O'Leary D.S. Cerebellar functional abnormalities in schizophrenia are suggested by classical eyeblink conditioning. Biological Psychiatry 2000, 48:204-209. 10.1016/S0006-3223(00)00247-X.
43. Siever L.J., Davis K.L. The pathophysiology of schizophrenia disorders: Perspectives from the spectrum. American Journal of Psychiatry 2004, 161:398-413. 10.1176/appi.ajp.161.3.398.
44. Silver H., Feldman P., Bilker W., Gur R.C. Working memory deficit as a core neuropsychological dysfunction in schizophrenia. American Journal of Psychiatry 2003, 160:1809-1816. 10.1176/appi.ajp.160.10.1809.
45. Solomon P.R., Blanchard S., Levine E., Velazquez E., Groccia-Ellison M. Attenuation of age-related conditioning deficits in humans by extension of the interstimulus interval. Psychology and Aging 1991, 6:36-42. 10.1037/0882-7974.6.1.36.
46. Spain B. Eyelid conditioning and arousal in schizophrenic and normal subjects. Journal of Abnormal Psychology 1966, 71:260-266. 10.1037/h0023596.
47. Stanton M.E. Multiple memory systems, development and conditioning. Behavioral Brain Research 2000, 110:25-37.
48. Steinmetz J.E. Brain substrates of classical eyeblink conditioning: a highly localized but also distributed system. Behavioral Brain Research 2000, 110:13-24.
49. Steinmetz, A. B., Skosnik, P. D., Edwards, C. R., Steinmetz, J. E., & Hetrick, W. P. (2010). Evaluation of bidirectional interstimulus interval shift in auditory delay eyeblink conditioning in healthy humans. Manuscript submitted for publication.
50. Thompson R.F., Steinmetz J.E. The role of the cerebellum in classical conditioning of discrete behavioral responses. Neuroscience 2009, 162:732-755. 10.1016/j.neuroscience.2009.01.041.
51. Timmann D., Daum I. Cerebellar contributions to cognitive functions: A progress report after two decades of research. Cerebellum 2007, 6:159-162. 10.1080/14734220701496448.
52. Timmann D., Drepper J., Frings M., Maschke M., Richter S., Gerwig M., Kolb F.P. The human cerebellum contributes to motor, emotional and cognitive associative learning. Cortex 2010, 46:845-857. 10.1016/j.cortex.2009.06.009.
53. Wassink T.H., Andreasen N.C., Nopoulos P., Flaum M. Cerebellar morphology as a predictor of symptom and psychosocial outcome in schizophrenia. Biological Psychiatry 1999, 45:41-48. 10.1016/S0006-3223(98)00175-9.
54. Wilson T.W., Slason E., Hernandez O.O., Asherin R., Reite M.L., Teale P.D., Rojas D.C. Aberrant high-frequency desynchronization of cerebellar cortices in early-onset psychosis. Psychiatry Research 2009, 174:47-56.
55. Woodruff-Pak D.S., Finkbiner R.G. Larger nondeclarative than declarative deficits in learning and memory in human aging. Psychology and Aging 1995, 10:416-426. 10.1037/0882-7974.10.3.416.
56. Woodruff-Pak D.S., Goldenberg G., Downey-Lamb M.M., Boyko O.B., Lemieux S.K. Cerebellar volume in humans related to magnitude of classical conditioning. Neuroreport 2000, 11:609-615. 10.1097/00001756-200002280-00035.
57. Woodruff-Pak D.S., Jaeger M.E., Gorman C., Wesnes K.A. Relationships among age, conditioned stimulus-unconditioned stimulus interval, and neuropsychological test performance. Neuropsychology 1999, 13:90-102. 10.1037/0894-4105.13.1.90.
58. Yeo C.H., Hardiman M.J., Glickstein M. Classical conditioning of the nictitating membrane response of the rabbit. II. Lesions of the cerebellar cortex. Experimental Brain Research 1985, 60:99-113.