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Cerebellum and Eyeblink Conditioning

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Handbook of the Cerebellum and Cerebellar Disorders

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Abstract

The cerebellum and brainstem constitute the essential neural circuit responsible for the acquisition and expression of the classically conditioned eyeblink response in numerous mammalian species, including humans. In this simple form of motor learning, a neutral conditioned stimulus (CS) overlaps and coterminates with a mildly aversive unconditioned stimulus (US), resulting, eventually, in the production of an eyeblink conditioned response (CR) to the CS alone. The forebrain is engaged when this basic delay procedure is made more difficult – for instance, if the CS and US are separated by a brief stimulus-free gap of time. In either case, it is generally accepted that the critical memory trace is formed and stored in the cerebellar interpositus nucleus (IP). The cerebellar cortex also plays a key role in normal acquisition by modulating the amplitude and/or timing characteristics of the eyeblink CR. Owing to the well-defined nature of the neural circuit, and the close correspondence between animal and human studies, eyeblink conditioning has been successfully used to investigate cerebellar dysfunction across a variety of human populations. Herein, research related to three representative disorders is discussed: fetal alcohol syndrome, attention-deficit hyperactivity disorder, and schizophrenia. The results advance understanding of these and similar clinical pathologies and the cerebellar deficits that may underlie them.

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References

  • Anand B, Malhotra C, Singh B, Dua A (1959) Cerebellar projections to limbic system. J Neurophysiol 22(4):451–457

    Article  CAS  PubMed  Google Scholar 

  • Andreasen NC, Pierson R (2008) The role of the cerebellum in schizophrenia. Biol Psychiatry 64:81–88

    Article  PubMed  PubMed Central  Google Scholar 

  • Andreasen NC, Paradiso S, O'Leary DS (1998) “Cognitive dysmetria” as an integrative theory of schizophrenia: a dysfunction in cortical-subcortical-cerebellar circuitry? Schizophrenia Bull 24(2):203–218

    Article  CAS  Google Scholar 

  • Bates E, Wilson SM, Saygin AP, Dick F, Sereno MI, Knight RT, Dronkers NF (2003) Voxel-based lesion-symptom mapping. Nat Neurosci 6:448–450

    Article  CAS  PubMed  Google Scholar 

  • Bayer SA, Altman J, Russo RJ, Zhang X (1993) Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14(1):83–144

    CAS  PubMed  Google Scholar 

  • Bekinschtein TA, Shalom DE, Forcato C, Herrera M, Coleman MR, Manes FF, Sigman M (2009) Classical conditioning in the vegetative and minimally conscious state. Nat Neurosci 12(10):1343–1349

    Article  CAS  PubMed  Google Scholar 

  • Berthier NE, Moore JW (1990) Activity of deep cerebellar nuclear cells during classical conditioning of nictitating membrane extension in rabbits. Exp Brain Res 83:44–54

    Article  CAS  PubMed  Google Scholar 

  • Berthier NE, Desmond JE, Moore JW (1987) Brain stem control of the nictitating membrane response. In: Gormezano I, Prokasy WF, Thompson RF (eds) Classical conditioning. Lawrence Erlbaum, Mahwah, pp 275–286

    Google Scholar 

  • Bolbecker AR, Mehta C, Johannesen JK, Edwards CR, O'Donnell BF, Shekhar A, Nurnberger JI, Steinmetz JE, Hetrick WP (2009a) Eyeblink conditioning anomalies in bipolar disorder suggest cerebellar dysfunction. Bipolar Disord 11(1):19–32

    Article  PubMed  Google Scholar 

  • Bolbecker AR, Mehta CS, Edwards CR, Steinmetz JE, O'Donnell BF, Hetrick WP (2009b) Eye-blink conditioning deficits indicate temporal processing abnormalities in schizophrenia. Schizophrenia Bull 111:182–191

    Google Scholar 

  • Britton GB, Astheimer LB (2004) Fear develops to the conditioned stimulus and to the context during classical eyeblink conditioning in rats. Integr Physiol Behav Sci 39(4):295–306

    Article  PubMed  Google Scholar 

  • Brodal A, Walberg F, Hoddevik GH (1975) The olivocerebellar projection in the cat studied with the method of retrograde axonal transport of horseradish peroxidase. J Comp Neurol 164(4):449–469

    Article  CAS  PubMed  Google Scholar 

  • Brown TH, Byrne JH, Labar K, LeDoux J, Lindquist DH, Thompson RF, Teyler TJ (2003) Learning and memory: basic mechanisms. In: Byrne JH, Roberts JL (eds) Cellular and molecular neuroscience. Academic, San Diego, pp 499–574

    Google Scholar 

  • Castellanos FX, Giedd JN, Marsh WL, Hamburger SD, Vaituzis AC, Dickstein DP, Sarfatti SE, Vauss YC, Snell JW, Lange N, Kaysen D, Krain AL, Ritchie GF, Rajapakse JC, Rapoport JL (1996) Quantitative brain magnetic resonance imaging in attention-deficit hyperactivity disorder. Arch Gen Psychiatry 53(7):607–616

    Article  CAS  PubMed  Google Scholar 

  • Castellanos FX, Giedd JN, Berquin PC, Walter JM, Sharp W, Tran T, Vaituzis AC, Blumenthal JD, Nelson J, Bastain TM, Zijdenbos A, Evans AC, Rapoport JL (2001) Quantitative brain magnetic resonance imaging in girls with attention-deficit/hyperactivity disorder. Arch Gen Psychiatry 58:289–295

    Article  CAS  PubMed  Google Scholar 

  • Cegavske CF, Thompson RF, Patterson MM, Gormezano I (1976) Mechanisms of efferent neuronal control of the reflex nictitating membrane response in rabbit (Oryctolagus cuniculus). J Comp Physiol Psychol 90:411–423

    Article  CAS  PubMed  Google Scholar 

  • Cegavske CF, Harrison TA, Torigoe Y (1987) Identification of the substrates of the unconditioned response in the classically conditioned, rabbit, nictitating-membrane preparation. In: Gormezano I, Prokasy WF, Thompson RF (eds) Classical conditioning. Lawrence Erlbaum, Mahwah, pp 65–93

    Google Scholar 

  • Chess AC, Green JT (2008) Abnormal topography and altered acquisition of conditioned eyeblink responses in a rodent model of attention-deficit/hyperactivity disorder. Behav Neurosci 122(1):63–74

    Article  PubMed  Google Scholar 

  • Clark RE, Gohl EB, Lavond DG (1997) The learning-related activity that develops in the pontine nuclei during classical eye-blink conditioning is dependent on the interpositus nucleus. Learn Mem 3(6):532–544

    Article  CAS  PubMed  Google Scholar 

  • Coffin JM, Roody S, Schneider K, O'Neill J (2005) Impaired cerebellar learning in children with prenatal alcohol exposure: a comparative study of eyeblink conditioning in children with ADHD and dyslexia. Cortex 41:389–398

    Article  PubMed  Google Scholar 

  • Coleman SR, Gormezano I (1971) Classical conditioning of the rabbit’s (Oryctolagus cuniculus) nictitating membrane response under symmetrical CS-US interval shifts. J Comp Physiol Psychol 77(3):447–455

    Article  CAS  PubMed  Google Scholar 

  • Dobbing J, Sands J (1979) The brain growth spurt in various mammalian species. Early Hum Dev 3:79–84

    Article  CAS  PubMed  Google Scholar 

  • Edwards CR, Newman S, Bismark A, Skosnik PD, O'Donnell BF, Shekhar A, Steinmetz JE, Hetrick WP (2008) Cerebellum volume and eyeblink conditioning in schizophrenia. Psychiatry Res 162(3):185–194

    Article  PubMed  PubMed Central  Google Scholar 

  • Fanselow MS, Poulos AM (2005) The neuroscience of mammalian associative learning. Annu Rev Psychol 56:207–234

    Article  PubMed  Google Scholar 

  • Freeman JH, Nicholson DA (2000) Developmental changes in eye-blink conditioning and neuronal activity in the cerebellar interpositus nucleus. J Neurosci 20(2):813–819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freeman JH, Nicholson DA (2001) Ontogenetic changes in the neural mechanisms of eyeblink conditioning. Integr Physiol Behav Sci 36(1):15–35

    Article  PubMed  Google Scholar 

  • Frings M, Gaertner K, Buderath P, Gerwig M, Christiansen H, Schoch B, Gizewski ER, Hebebrand J, Timmann D (2010) Timing of conditioned eyeblink responses is impaired in children with attention-deficit/hyperactivity disorder. Exp Brain Res 201(2):167–176

    Article  PubMed  Google Scholar 

  • Gerwig M, Dimitrova A, Kolb FP, Maschke M, Brol B, Kunnel A, Böring D, Thilmann AF, Forsting M, Diener HC, Timmann D (2003) Comparison of eyeblink conditioning in patients with superior and posterior inferior cerebellar lesions. Brain 126(Pt 1):71–94

    Article  CAS  PubMed  Google Scholar 

  • Gerwig M, Kolb FP, Timmann D (2007) The involvement of the human cerebellum in eyeblink conditioning. Cerebellum 6:38–57

    Article  CAS  PubMed  Google Scholar 

  • Gormezano I, Schneiderman N, Deauz E, Fuentes I (1962) Nictitating membrane: classical conditioning and extinction in the albino rabbit. Science 136:33–34

    Article  Google Scholar 

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

    Google Scholar 

  • Gould TJ, Steinmetz JE (1996) Changes in rabbit cerebellar cortical and interpositus nucleus activity during acquisition, extinction, and backward classical eyelid conditioning. Neurobiol Learn Mem 65:17–34

    Article  CAS  PubMed  Google Scholar 

  • Green JT (2004) The effects of ethanol on the developing cerebellum and eyeblink classical conditioning. Cerebellum 3(3):178–187

    Article  CAS  PubMed  Google Scholar 

  • Green JT, Steinmetz JE (2005) Purkinje cell activity in the cerebellar anterior lobe during rabbit eyeblink conditioning. Learn Mem 12(3):260–269

    Article  PubMed  PubMed Central  Google Scholar 

  • Green JT, Rogers RF, Goodlett CR, Steinmetz JE (2000) Impairment in eyeblink classical conditioning in adult rats exposed to ethanol as neonates. Alcohol Clin Exp Res 24(4):438–447

    Article  CAS  PubMed  Google Scholar 

  • Green JT, Tran T, Steinmetz JE, Goodlett CR (2002) Neonatal ethanol produces cerebellar deep nuclear cell loss and correlated disruption of eyeblink conditioning in adult rats. Brain Res 956:302–311

    Article  CAS  PubMed  Google Scholar 

  • Halverson HE, Freeman JH (2006) Medial auditory thalamic nuclei are necessary for eyeblink conditioning. Behav Neurosci 120:880–887

    Article  PubMed  PubMed Central  Google Scholar 

  • Halverson HE, Porembra A, Freeman JH (2008) Medial auditory thalamus inactivation prevents acquisition and retention of eyeblink conditioning. Learn Mem 15:532–538

    Article  PubMed  PubMed Central  Google Scholar 

  • Halverson HE, Lee I, Freeman JH (2010) Associative plasticity in the medial auditory thalamus and cerebellar interpositus nucleus during eyeblink conditioning. J Neurosci 30(26):8787–8796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill DE, Yeo RA, Campbell RA, Hart B, Vigil J, Brooks W (2003) Magnetic resonance imaging correlates of attention-deficit/hyperactivity disorder in children. Neuropsychology 17(3):496–506

    Article  PubMed  Google Scholar 

  • Jacobson SW, Stanton ME, Molteno CD, Burden MJ, Fuller DS, Hoyme HE, Robinson LK, Khaole N, Jacobson JL (2008) Impaired eyeblink conditioning in children with fetal alcohol syndrome. Alcohol Clin Exp Res 32(2):365–372

    Article  PubMed  Google Scholar 

  • Kalmbach BE, Ohyama T, Kreider JC, Riusech F, Mauk MD (2009) Interactions between prefrontal cortex and cerebellum revealed by trace eyelid conditioning. Learn Mem 16(1):86–95

    Article  PubMed  PubMed Central  Google Scholar 

  • Kalmbach BE, Ohyama T, Mauk MD (2010) Temporal patterns of inputs to cerebellum necessary and sufficient for trace eyelid conditioning. J Neurophysiol 104(2):627–640

    Article  PubMed  PubMed Central  Google Scholar 

  • Kleim JA, Freeman JH, Bruneau R, Nolan BC, Cooper NR, Zook A, Walters D (2002) Synapse formation is associated with memory storage in the cerebellum. Proc Natl Acad Sci 99(20):13228–13231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kronforst-Collins MA, Disterhoft JF (1998) Lesions of the caudal area of rabbit medial prefrontal cortex impair trace eyeblink conditioning. Neurobiol Learn Mem 69:147–162

    Article  CAS  PubMed  Google Scholar 

  • Krupa DJ, Thompson JK, Thompson RF (1993) Localization of a memory trace in the mammalian brain. Science 260:989–991

    Article  CAS  PubMed  Google Scholar 

  • Lavond DG (2002) Role of the nuclei in eyeblink conditioning. Ann N Y Acad Sci 978:93–105

    Article  PubMed  Google Scholar 

  • Lavond DG, Lincoln JS, McCormick DA, Thompson RF (1984) 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 305:323–330

    Article  CAS  PubMed  Google Scholar 

  • Lavond DG, Logan CG, Sohn JH, Garner WD, Kanzawa SA (1990) Lesions of the cerebellar interpositus nucleus abolish both nictitating membrane and eyelid EMG conditioned responses. Brain Res 514(2):238–248

    Article  CAS  PubMed  Google Scholar 

  • Lee T, Kim JJ (2004) Differential effects of cerebellar, amygdalar, and hippocampal lesions on classical eyeblink conditioning in rats. J Neurosci 24(13):3242–3250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindquist DH, Sokoloff G, Steinmetz JE (2007) Ethanol-exposed neonatal rats are impaired as adults in classical eyeblink conditioning at multiple unconditioned stimulus intensities. Brain Res 1150:155–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindquist DH, Vogel RW, Steinmetz JE (2009) Associative and non-associative blinking in classically conditioned adult rats. Physiol Behav 96(3):399–411

    Article  CAS  PubMed  Google Scholar 

  • Lindquist DH, Mahoney LP, Steinmetz JE (2010) Conditioned fear in adult rats is facilitated by the prior acquisition of a classically conditioned motor response. Neurobiol Learn Mem 94(2):167–175

    Article  PubMed  PubMed Central  Google Scholar 

  • Lubow RE (2009) Classical eyeblink conditioning and schizophrenia: a short review. Behav Brain Res 202:1–4

    Article  CAS  PubMed  Google Scholar 

  • McCormick DA, Thompson RF (1984a) Cerebellum: essential involvement in the classically conditioned eyelid response. Science 223(4633):296–299

    Article  CAS  PubMed  Google Scholar 

  • McCormick DA, Thompson RF (1984b) Neuronal responses of the rabbit cerebellum during acquisition and performance of a classically conditioned nictitating membrane-eyelid response. J Neurosci 4(11):2811–2822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCormick DA, Steinmetz JE, Thompson RF (1985) Lesions of the inferior olivary complex cause extinction of the classically conditioned eyelid response. Brain Res 359:120–130

    Article  CAS  PubMed  Google Scholar 

  • McGlinchey-Berroth R, Cermak LS, Carrillo MC, Armfield S, Gabrieli JD, Disterhoft JF (1995) Impaired delay eyeblink conditioning in amnesic Korsakoff's patients and recovered alcoholics. Alcohol Clin Exp Res 19(5):1127–1132

    Article  CAS  PubMed  Google Scholar 

  • McLaughlin J, Skaggs H, Churchwell J, Powell DA (2002) Medial prefrontal cortex and Pavlovian conditioning: trace versus delay conditioning. Behav Neurosci 116:37–47

    Article  PubMed  Google Scholar 

  • Medina JF, Mauk MD (1999) Simulations of cerebellar motor learning: computational analysis of plasticity at the mossy fiber to deep nucleus synapse. J Neurosci 19(16):140–151

    Article  Google Scholar 

  • Medina JF, Nores WL, Mauk MD (2002) Inhibition of climbing fibres is a signal for the extinction of conditioned eyelid responses. Nature 416(6878):330–333

    Article  CAS  PubMed  Google Scholar 

  • Mintz M, Wang-Ninio Y (2001) Two stage theory of conditioning: involvement of the cerebellum and the amygdala. Brain Res 897:150–156

    Article  CAS  PubMed  Google Scholar 

  • Morara S, van der Want JJ, de Weerd H, Provini L, Rosina A (2001) Ultrastructural analysis of climbing fiber-Purkinje cell synaptogenesis in the rat cerebellum. Neuroscience 108:655–671

    Article  CAS  PubMed  Google Scholar 

  • Neufeld M, Mintz M (2001) Involvement of the amygdala in classical conditioning of eyeblink response in the rat. Brain Res 889:112–117

    Article  CAS  PubMed  Google Scholar 

  • Nolan BC, Freeman JH (2005) Purkinje cell loss by OX7-saporin impairs excitatory and inhibitory eyeblink conditioning. Behav Neurosci 119:190–201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oakley DA, Russell IS (1977) Subcortical storage of Pavlovian conditioning in the rabbit. Physiol Behav 18:931–937

    Article  CAS  PubMed  Google Scholar 

  • Perrett SP, Ruiz BP, Mauk MD (1993) Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J Neurosci 13(4):1708–1718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pugh JR, Raman IM (2006) Potentiation of mossy fiber EPSCs in the cerebellar nuclei by NMDA receptor activation followed by postinhibitory rebound current. Neuron 51(1):113–123

    Article  CAS  PubMed  Google Scholar 

  • Pugh JR, Raman IM (2008) Mechanisms of potentiation of mossy fiber EPSCs in the cerebellar nuclei by coincident synaptic excitation and inhibition. J Neurosci 28(42):10549–10560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rogers RF, Britton GB, Steinmetz JE (2001) Learning-related interpositus activity is conserved across species as studies during eyeblink conditioning in the rat. Brain Res 905:171–177

    Article  CAS  PubMed  Google Scholar 

  • Rorick-Kehn LM, Steinmetz JE (2005) Amygdalar unit activity during three learning tasks: eyeblink classical conditioning, Pavlovian fear conditioning, and signaled avoidance conditioning. Behav Neurosci 119(5):1254–1276

    Article  PubMed  Google Scholar 

  • Rubia K, Noorloos J, Smith A, Gunning B, Sergeant J (2003) Motor timing deficits in community and clinical boys with hyperactive behavior: the effect of methylphenidate on motor timing. J Abnorm Child Psychol 31:301–313

    Article  PubMed  Google Scholar 

  • Sagvolden T, Russell VA, Aase H, Johansen EB, Farshbaf M (2005) Rodent models of attention-deficit/hyperactivity disorder. Biol Psychiatry 57:1239–1247

    Article  PubMed  Google Scholar 

  • Schmahmann JD, Pandya DN (1995) Prefrontal cortex projections to the basilar pons in rhesus monkey: implications for the cerebellar contribution to higher function. Neurosci Lett 199(3):175–178

    Article  CAS  PubMed  Google Scholar 

  • Sears LL, Steinmetz JE (1991) Dorsal accessory inferior olive activity diminishes during acquisition of the rabbit classically conditioned eyelid response. Brain Res 545:114–122

    Article  CAS  PubMed  Google Scholar 

  • Sears LL, Finn PR, Steinmetz JE (1994) Abnormal classical eyeblink conditioning in autism. Autism Dev Disord 24:737–751

    Article  CAS  Google Scholar 

  • Skosnik PD, Edwards CR, O'Donnell BF, Steffen A, Steinmetz JE, Hetrick WP (2008) Cannabis use disrupts eyeblink conditioning: evidence for cannabinoid modulation of cerebellar-dependent learning. Psychopharmacology 33(6):1432–1440

    CAS  Google Scholar 

  • Smith A, Taylor E, Rogers JW, Newman S, Rubia K (2002) Evidence for a pure time perception deficit in children with ADHD. J Child Psychol Psychiatry 43:529–542

    Article  PubMed  Google Scholar 

  • Snider R, Maiti A, Snider S (1976) Cerebellar pathways to ventral midbrain and nigra. Exp Neurol 53(3):714–728

    Article  CAS  PubMed  Google Scholar 

  • Sokol RJ, Delaney-Black V, Nordstrom B (2003) Fetal alcohol spectrum disorder. J Am Med Assoc 290:2996–2999

    Article  CAS  Google Scholar 

  • Stanton ME, Goodlett CR (1998) Neonatal ethanol exposure impairs eyeblink conditioning in weanling rats. Alcohol Clin Exp Res 22(1):270–275

    Article  CAS  PubMed  Google Scholar 

  • Steinmetz JE (1990a) Classical nictitating membrane conditioning in rabbits with varying interstimulus intervals and direct activation of cerebellar mossy fibers as the CS. Behav Brain Res 38:97–108

    Article  CAS  PubMed  Google Scholar 

  • Steinmetz JE (1990b) Neural activity in the cerebellar interpositus nucleus during classical NM conditioning with a pontine stimulation CS. Psychol Sci 1:378–382

    Article  Google Scholar 

  • Steinmetz JE (2000) Brain substrates of classical eyeblink conditioning: a highly localized but also distributed system. Behav Brain Res 110:13–24

    Article  CAS  PubMed  Google Scholar 

  • Steinmetz JE, Lindquist DH (2009) Neuronal basis of learning. In: Berntson GG, Cacioppo JT (eds) Handbook of neuroscience for the behavioral sciences. Wiley, Hoboken, pp 507–527

    Google Scholar 

  • Steinmetz JE, Sengelaub DR (1992) Possible conditioned stimulus pathway for classical eyelid conditioning in rabbits. I. Anatomical evidence for direct projections from the pontine nuclei to the cerebellar interpositus nucleus. Behav Neural Biol 57:103–115

    Article  CAS  PubMed  Google Scholar 

  • Steinmetz JE, Logan CG, Rosen DJ, Thompson JK, Lavond DG, Thompson RF (1987) Initial localization of the acoustic conditioned stimulus projection system to the cerebellum essential for classical eyelid conditioning. Proc Natl Acad Sci 84:3531–3535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steinmetz JE, Lavond DG, Ivkovich D, Logan CG, Thompson RF (1992a) Disruption of classical eyelid conditioning after cerebellar lesions: damage to a memory trace system of a simple performance deficit? J Neurosci 12(11):4403–4426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steinmetz JE, Logue SF, Steinmetz SS (1992b) Rabbit classically conditioned eyelid responses do not reappear after interpositus nucleus lesion and extensive post-lesion training. Behav Brain Res 51:103–114

    Article  CAS  PubMed  Google Scholar 

  • Taub AH, Mintz M (2010) Amygdala conditioning modulates sensory input to the cerebellum. Neurobiol Learn Mem 94(4):521–529

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Thompson RF (2005) In search of memory traces. Ann Rev Psychol 56:1–23

    Article  Google Scholar 

  • Thompson RF, Krupa DJ (1994) Organization of memory traces in the mammalian brain. Ann Rev Neurosci 17:519–549

    Article  CAS  PubMed  Google Scholar 

  • Thompson RF, Steinmetz JE (2009) The role of the cerebellum in classical conditioning of discrete behavioral responses. Neuroscience 162(3):732–755

    Article  CAS  PubMed  Google Scholar 

  • Thompson RF, Donegan NH, Clark GA, Lavond DG, Lincoln JS, Madden J, Mamounas LA, Mauk MD, McCormick DA (1987) Neuronal substrates of discrete, defensive conditioned reflexes, conditioned fear states, and their interactions in the rabbit. In: Gormezano I, Prokasy WF, Thompson RF (eds) Classical conditioning, 3rd edn. Erlbaum, Hillsdale, pp 371–399

    Google Scholar 

  • Timmann D, Gerwig M, Frings M, Maschke M, Kolb FP (2005) Eyeblink conditioning in patients with hereditary ataxia: a one-year follow-up study. Exp Brain Res 162(3):332–345

    Article  CAS  PubMed  Google Scholar 

  • Tracy JA, Ghose SS, Stetcher T, McFall RM, Steinmetz JE (1999) Classical conditioning in a nonclinical obsessive-compulsive population. Psychol Sci 10:9–13

    Article  Google Scholar 

  • Vogel RW, Amundson JC, Lindquist DH, Steinmetz JE (2009) Eyeblink conditioning during an interstimulus interval switch in rabbits (Oryctolagus cuniculus) using picrotoxin to disrupt cerebellar cortical input to the interpositus nucleus. Behav Neurosci 123(1):62–74

    Article  PubMed  PubMed Central  Google Scholar 

  • Wagner AR, Brandon SE (1989) Evolution of a structured connectionist model of Pavlovian conditioning (AESOP). In: Klein SB, Mowrer RR (eds) Contemporary learning theories: Pavlovian conditioning and the status of traditional learning theory. Erlbaum, Hillsdale, pp 149–190

    Google Scholar 

  • Weisz DJ, Harden DG, Xiang Z (1992) Effects of amygdala lesions on reflex facilitation and conditioned response acquisition during nictitating membrane response conditioning in rabbit. Behav Neurosci 106(2):262–273

    Article  CAS  PubMed  Google Scholar 

  • Woodruff-Pak DS (2001) Eyeblink classical conditioning differentiates normal aging from Alzheimer’s disease. Integr Physiol Behav Sci 36(2):87–108

    Article  CAS  PubMed  Google Scholar 

  • Woodruff-Pak DS, Disterhoft JF (2008) Where is the trace in trace conditioning? Trends Neurosci 31(2):105–112

    Article  CAS  PubMed  Google Scholar 

  • Woodruff-Pak DS, Steinmetz JE (2000) Past, present, and future of human eyeblink classical conditioning. In: Woodruff-Pak DS, Steinmetz JE (eds) Eyeblink classical conditioning, Applications in humans, vol 1. Kluwer, Boston, pp 1–17

    Chapter  Google Scholar 

  • Woodruff-Pak DS, Lavond DG, Logan CG, Steinmetz JE, Thompson RF (1993) Cerebellar cortical lesions and reacquisition in classical conditioning of the nictitating membrane response in rabbits. Brain Res 608:67–77

    Article  CAS  PubMed  Google Scholar 

  • Yeo CH, Hardiman MJ, Glickstein M (1985) Classical conditioning of the nictitating membrane response of the rabbit: II. Lesions of the cerebellar cortex. Exp Brain Res 63:81–92

    Google Scholar 

  • Yeo CH, Hardiman MJ, Glickstein M (1986) Classical conditioning of nictitating membrane response of the rabbit: IV. Lesions of the inferior olive. Exp Brain Res 63:81–92

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Psychology, The Ohio State University, Columbus, OH, USA

    Derick H. Lindquist & Richard F. Thompson

  2. Department of Psychology, University of Southern California, Los Angeles, CA, USA

    Joseph E. Steinmetz

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  1. Derick H. Lindquist
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  2. Joseph E. Steinmetz
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  3. Richard F. Thompson
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Correspondence to Derick H. Lindquist .

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Editors and Affiliations

  1. CHU-Charleroi, University of Mons, Charleroi, Belgium

    Mario U. Manto

  2. Department of Neuroscience, The Scripps Research Institute, La Jolla, CA, USA

    Donna L. Gruol

  3. Ataxia Center, Laboratory for Neuroanatomy and Cerebellar Neurobiology, Department of Neurology Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA

    Jeremy D. Schmahmann

  4. Department of Integrative Physiology, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan

    Noriyuki Koibuchi

  5. Department of Pathology and Immunology, Baylor College of Medicine, Houston, TX, USA

    Roy V. Sillitoe

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  1. Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA

    Jeremy D. Schmahmann

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Lindquist, D.H., Steinmetz, J.E., Thompson, R.F. (2022). Cerebellum and Eyeblink Conditioning. In: Manto, M.U., Gruol, D.L., Schmahmann, J.D., Koibuchi, N., Sillitoe, R.V. (eds) Handbook of the Cerebellum and Cerebellar Disorders. Springer, Cham. https://doi.org/10.1007/978-3-030-23810-0_50

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