The Anatomy and Physiology of Eyeblink Classical Conditioning

  • Kaori Takehara-Nishiuchi
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 37)


This chapter reviews the past research toward identifying the brain circuit and its computation underlying the associative memory in eyeblink classical conditioning. In the standard delay eyeblink conditioning paradigm, the conditioned stimulus (CS) and eyeblink-eliciting unconditioned stimulus (US) converge in the cerebellar cortex and interpositus nucleus (IPN) through the pontine nuclei and inferior olivary nucleus. Repeated pairings of CS and US modify synaptic weights in the cerebellar cortex and IPN, enabling IPN neurons to activate the red nucleus and generate the conditioned response (CR). In a variant of the standard paradigm, trace eyeblink conditioning, the CS and US are separated by a brief stimulus-free trace interval. Acquisition in trace eyeblink conditioning depends on several forebrain regions, including the hippocampus and medial prefrontal cortex as well as the cerebellar–brainstem circuit. Details of computations taking place in these regions remain unclear; however, recent evidence supports a view that the forebrain encodes a temporal sequence of the CS, trace interval, and US in a specific environmental context and signals the cerebellar–brainstem circuit to execute the CR when the US is likely to occur. Together, delay eyeblink conditioning represents one of the most successful cases of understanding the neural substrates of long-term memory in mammals, while trace eyeblink conditioning demonstrates its utility for uncovering detailed computations in the whole brain network underlying long-term memory.


Associative memory Nictitating membrane Cerebellum Hippocampus 



The author thanks Drs. Craig Weiss and Nathan Insel for their helpful comments. This work was supported by NSERC Discovery Grant (KT).


  1. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, Tonegawa S (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79(2):377–388PubMedCrossRefGoogle Scholar
  2. Akase E, Alkon D, Disterhoft JF (1989) Hippocampal lesions impair memory of short-delay conditioned eye blink in rabbits. Behav Neurosci 103(5):935–943PubMedCrossRefGoogle Scholar
  3. Baeg EH, Kim YB, Jang J, Kim HT, Mook-Jung I, Jung MW (2001) Fast spiking and regular spiking neural correlates of fear conditioning in the medial prefrontal cortex of the rat. Cereb Cortex 11(5):441–451PubMedCrossRefGoogle Scholar
  4. Bao S, Chen L, Thompson RF (2000) Learning- and cerebellum-dependent neuronal activity in the lateral pontine nucleus. Behav Neurosci 114(2):254–261PubMedCrossRefGoogle Scholar
  5. Bao S, Chen L, Kim JJ, Thompson RF (2002) Cerebellar cortical inhibition and classical eyeblink conditioning. Proc Natl Acad Sci USA 99(3):1592–1597PubMedPubMedCentralCrossRefGoogle Scholar
  6. Berger TW, Orr WB (1983) Hippocampectomy selectively disrupts discrimination reversal conditioning of the rabbit nictitating membrane response. Behav Brain Res 8(1):49–68PubMedCrossRefGoogle Scholar
  7. Berger TW, Alger B, Thompson RF (1976) Neuronal substrate of classical conditioning in the hippocampus. Science 192(4238):483–485PubMedCrossRefGoogle Scholar
  8. Berthier NE, Moore JW (1986) Cerebellar Purkinje cell activity related to the classically conditioned nictitating membrane response. Exp Brain Res 63(2):341–350PubMedCrossRefGoogle Scholar
  9. Berthier NE, Moore JW (1990) Activity of deep cerebellar nuclear cells during classical conditioning of nictitating membrane extension in rabbits. Exp Brain Res 83(1):44–54PubMedCrossRefGoogle Scholar
  10. Beylin AV, Gandhi CC, Wood GE, Talk AC, Matzel LD, Shors TJ (2001) The role of the hippocampus in trace conditioning: temporal discontinuity or task difficulty? Neurobiol Learn Mem 76(3):447–461PubMedCrossRefGoogle Scholar
  11. Bostan AC, Dum RP, Strick PL (2013) Cerebellar networks with the cerebral cortex and basal ganglia. Trends Cogn Sci 17(5):241–254PubMedPubMedCentralCrossRefGoogle Scholar
  12. Brown KL, Agelan A, Woodruff-Pak DS (2010) Unimpaired trace classical eyeblink conditioning in Purkinje cell degeneration (pcd) mutant mice. Neurobiol Learn Mem 93(3):303–311PubMedCrossRefGoogle Scholar
  13. Brun VH, Leutgeb S, Wu H-Q, Schwarcz R, Witter MP, Moser EI, Moser M-B (2008) Impaired spatial representation in CA1 after lesion of direct input from entorhinal cortex. Neuron 57(2):290–302PubMedCrossRefGoogle Scholar
  14. Buchanan SL, Thompson RH, Maxwell BL, Powell DA (1994) Efferent connections of the medial prefrontal cortex in the rabbit. Exp Brain Res 100(3):469–483PubMedCrossRefGoogle Scholar
  15. Burton BG, Hok V, Save E, Poucet B (2009) Lesion of the ventral and intermediate hippocampus abolishes anticipatory activity in the medial prefrontal cortex of the rat. Behav Brain Res 199(2):222–234PubMedCrossRefGoogle Scholar
  16. Cartford MC, Gohl EB, Singson M, Lavond DG (1997) The effects of reversible inactivation of the red nucleus on learning-related and auditory-evoked unit activity in the pontine nuclei of classically conditioned rabbits. Learn Mem 3(6):519–531PubMedCrossRefGoogle Scholar
  17. Cerminara NL, Rawson JA (2004) Evidence that climbing fibers control an intrinsic spike generator in cerebellar Purkinje cells. J Neurosci 24(19):4510–4517PubMedCrossRefGoogle Scholar
  18. Chen C, Thompson RF (1995) Temporal specificity of long-term depression in parallel-fiber Purkinje synapses in rat cerebellar slice. Learn Mem 2(1):185–198PubMedCrossRefGoogle Scholar
  19. Chen C, Kano M, Abeliovich A, Chen L, Bao S, Kim JJ, Hashimoto K, Thompson RF, Tonegawa S (1995) Impaired motor coordination correlates with persistent multiple climbing fiber innervation in PKC gamma mutant mice. Cell 83(7):1233–1242PubMedCrossRefGoogle Scholar
  20. Chen L, Bao S, Lockard JM, Kim JK, Thompson RF (1996) Impaired classical eyeblink conditioning in cerebellar-lesioned and Purkinje cell degeneration (pcd) mutant mice. J Neurosci 16(8):2829–2838PubMedGoogle Scholar
  21. Chen L, Bao S, Thompson RF (1999) Bilateral lesions of the interpositus nucleus completely prevent eyeblink conditioning in Purkinje cell-degeneration mutant mice. Behav Neurosci 113(1):204–210PubMedCrossRefGoogle Scholar
  22. Christian KM, Thompson RF (2003) Neural substrates of eyeblink conditioning: acquisition and retention. Learn Mem 10(6):427–455PubMedCrossRefGoogle Scholar
  23. Clark RE, Gohl E (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(1):532–544PubMedCrossRefGoogle Scholar
  24. Clark RE, Squire LR (1998) Classical conditioning and brain systems: the role of awareness. Science 280(5360):77–81PubMedCrossRefGoogle Scholar
  25. Clark RE, Squire LR (1999) Human eyeblink classical conditioning: Effects of manipulating awareness of the stimulus contingencies. Psychol Sci 10(1):14–18CrossRefGoogle Scholar
  26. Clark GA, McCormick DA, Lavond DG, Thompson RF (1984) Effects of lesions of cerebellar nuclei on conditioned behavioral and hippocampal neuronal responses. Brain Res 291(1):125–136PubMedCrossRefGoogle Scholar
  27. Clark RE, Zhang AA, Lavond DG (1992) Reversible lesions of the cerebellar interpositus nucleus during acquisition and retention of a classically conditioned behavior. Behav Neurosci 106(6):879–888PubMedCrossRefGoogle Scholar
  28. Davachi L, DuBrow S (2015) How the hippocampus preserves order: the role of prediction and context. Trends Cogn Sci 19(2):92–99PubMedPubMedCentralCrossRefGoogle Scholar
  29. De Zeeuw CI, Hansel C, Bian F, Koekkoek SK, van Alphen AM, Linden DJ, Oberdick J (1998) Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 20(3):495–508PubMedCrossRefGoogle Scholar
  30. Disterhoft JF, Quinn KJ, Weiss C, Shipley MT (1985) Accessory abducens nucleus and conditioned eye retraction/nictitating membrane extension in rabbit. J Neurosci 5(4):941–950PubMedGoogle Scholar
  31. Eccles JC, Llinas R, Sasaki K (1966a) The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum. J Physiol 182(2):268–296PubMedPubMedCentralCrossRefGoogle Scholar
  32. Eccles JC, Llinas R, Sasaki K (1966b) Parallel fibre stimulation and the responses induced thereby in the Purkinje cells of the cerebellum. Exp Brain Res 1(1):17–39PubMedGoogle Scholar
  33. Feil R, Hartmann J, Luo C, Wolfsgruber W, Schilling K, Feil S, Barski JJ et al (2003) Impairment of LTD and cerebellar learning by Purkinje cell-specific ablation of cGMP-dependent protein kinase I. J Cell Biol 163(2):295–302PubMedPubMedCentralCrossRefGoogle Scholar
  34. Flores LC, Disterhoft JF (2009) Caudate nucleus is critically involved in trace eyeblink conditioning. J Neurosci 29(46):14511–14520PubMedPubMedCentralCrossRefGoogle Scholar
  35. Flores LC, Disterhoft JF (2013) Caudate nucleus in retrieval of trace eyeblink conditioning after consolidation. J Neurosci 33(7):2828–2836PubMedPubMedCentralCrossRefGoogle Scholar
  36. Frankland PW, Bontempi B (2005) The organization of recent and remote memories. Nat Rev Neurosci 6(2):119–130PubMedCrossRefGoogle Scholar
  37. Fredette BJ, Mugnaini E (1991) The GABAergic cerebello-olivary projection in the rat. Anat Embryol (Berl) 184(3):225–243CrossRefGoogle Scholar
  38. Freeman JH Jr, Nicholson DA (2000) Developmental changes in eye-blink conditioning and neuronal activity in the cerebellar interpositus nucleus. J Neurosci 20(2):813–819PubMedGoogle Scholar
  39. Gahwiler BH (1975) The effects of GABA, picrotoxin and bicuculline on the spontaneous bioelectric activity of cultured cerebellar Purkinje cells. Brain Res 99(1):85–95PubMedCrossRefGoogle Scholar
  40. Galvez R, Weible AP, Disterhoft JF (2007) Cortical barrel lesions impair whisker-CS trace eyeblink conditioning. Learn Mem 14(1–2):94–100PubMedPubMedCentralCrossRefGoogle Scholar
  41. Gao Z, van Beugen BJ, De Zeeuw CI (2012) Distributed synergistic plasticity and cerebellar learning. Nat Rev Neurosci 13(9):619–635PubMedCrossRefGoogle Scholar
  42. Garcia KS, Mauk MD (1998) Pharmacological analysis of cerebellar contributions to the timing and expression of conditioned eyelid responses. Neuropharmacology 37(4–5):471–480PubMedCrossRefGoogle Scholar
  43. Gerwig M, Kolb FP, Timmann D (2007) The involvement of the human cerebellum in eyeblink conditioning. Cerebellum 6(1):38–57PubMedCrossRefGoogle Scholar
  44. Gilmartin MR, McEchron MD (2005) Single neurons in the medial prefrontal cortex of the rat exhibit tonic and phasic coding during trace fear conditioning. Behav Neurosci 119(6):1496–1510PubMedCrossRefGoogle Scholar
  45. 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(1):17–34PubMedCrossRefGoogle Scholar
  46. Green JT, Steinmetz JE (2005) Purkinje cell activity in the cerebellar anterior lobe after rabbit eyeblink conditioning. Learn Mem 12(3):260–269PubMedPubMedCentralCrossRefGoogle Scholar
  47. Green JT, Woodruff-Pak DS (2000) Eyeblink classical conditioning: hippocampal formation is for neutral stimulus associations as cerebellum is for association-response. Psychol Bull 126(1):138–158PubMedCrossRefGoogle Scholar
  48. Gruart A, Blazquez P, Delgado-Garcia JM (1995) Kinematics of spontaneous, reflex, and conditioned eyelid movements in the alert cat. J Neurophysiol 74(1):226–248PubMedCrossRefGoogle Scholar
  49. Gruart A, Schreurs BG, del Toro ED, Delgado-Garcia JM (2000) Kinetic and frequency-domain properties of reflex and conditioned eyelid responses in the rabbit. J Neurophysiol 83(2):836–852PubMedCrossRefGoogle Scholar
  50. Hattori S, Yoon T, Disterhoft JF, Weiss C (2014) Functional reorganization of a prefrontal cortical network mediating consolidation of trace eyeblink conditioning. J Neurosci 34(4):1432–1445PubMedPubMedCentralCrossRefGoogle Scholar
  51. Hattori S, Chen L, Weiss C, Disterhoft JF (2015) Robust hippocampal responsivity during retrieval of consolidated associative memory: hippocampal involvement after memory consolidation. Hippocampus 25:655–669 PubMedPubMedCentralCrossRefGoogle Scholar
  52. Hausser M, Clark BA (1997) Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19(3):665–678PubMedCrossRefGoogle Scholar
  53. Heiney SA, Kim J, Augustine GJ, Medina JF (2014) Precise control of movement kinematics by optogenetic inhibition of Purkinje cell activity. J Neurosci 34(6):2321–2330PubMedPubMedCentralCrossRefGoogle Scholar
  54. Hesslow G, Ivarsson M (1994) Suppression of cerebellar Purkinje cells during conditioned responses in ferrets. NeuroReport 5(5):649–652PubMedCrossRefGoogle Scholar
  55. Hesslow G, Ivarsson M (1996) Inhibition of the inferior olive during conditioned responses in the decerebrate ferret. Exp Brain Res 110(1):36–46PubMedCrossRefGoogle Scholar
  56. Hesslow G, Svensson P, Ivarsson M (1999) Learned movements elicited by direct stimulation of cerebellar mossy fiber afferents. Neuron 24(1):179–185PubMedCrossRefGoogle Scholar
  57. Hirsh R (1974) The hippocampus and contextual retrieval of information from memory: a theory. Behav Biol 12(4):421–444PubMedCrossRefGoogle Scholar
  58. Hu B, Chen H, Feng H, Zeng Y, Yang L, Fan ZL, Wu YM, Sui JF (2010) Disrupted topography of the acquired trace-conditioned eyeblink responses in guinea pigs after suppression of cerebellar cortical inhibition to the interpositus nucleus. Brain Res 1337:41–55PubMedCrossRefGoogle Scholar
  59. Insel N, Barnes CA (2014) Differential activation of fast-spiking and regular-firing neuron populations during movement and reward in the dorsal medial frontal cortex. Cereb Cortex 25(9):2631–2647PubMedPubMedCentralCrossRefGoogle Scholar
  60. Insel N, Takehara-Nishiuchi K (2013) The cortical structure of consolidated memory: a hypothesis on the role of the cingulate-entorhinal cortical connection. Neurobiol Learn Mem 106:343–350PubMedCrossRefGoogle Scholar
  61. Ito M, Kano M (1982) Long-lasting depression of parallel fiber-Purkinje cell transmission induced by conjunctive stimulation of parallel fibers and climbing fibers in the cerebellar cortex. Neurosci Lett 33(3):253–258PubMedCrossRefGoogle Scholar
  62. Jay TM, Witter MP (1991) Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. J Comp Neurol 313(4):574–586PubMedPubMedCentralCrossRefGoogle Scholar
  63. Jirenhed DA, Bengtsson F, Hesslow G (2007) Acquisition, extinction, and reacquisition of a cerebellar cortical memory trace. J Neurosci 27(10):2493–2502PubMedCrossRefGoogle Scholar
  64. Jorntell H, Ekerot CF (2002) Reciprocal bidirectional plasticity of parallel fiber receptive fields in cerebellar Purkinje cells and their afferent interneurons. Neuron 34(5):797–806PubMedCrossRefGoogle Scholar
  65. Jorntell H, Ekerot CF (2003) Receptive field plasticity profoundly alters the cutaneous parallel fiber synaptic input to cerebellar interneurons in vivo. J Neurosci 23(29):9620–9631PubMedGoogle Scholar
  66. Jorntell H, Bengtsson F, Schonewille M, De Zeeuw CI (2010) Cerebellar molecular layer interneurons—computational properties and roles in learning. Trends Neurosci 33(11):524–532PubMedCrossRefGoogle Scholar
  67. 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):86–95PubMedPubMedCentralCrossRefGoogle Scholar
  68. Kalmbach BE, Davis T, Ohyama T, Riusech F, Nores WL, Mauk MD (2010) Cerebellar cortex contributions to the expression and timing of conditioned eyelid responses. J Neurophysiol 103(4):2039–2049PubMedPubMedCentralCrossRefGoogle Scholar
  69. Kim JJ, Clark RE, Thompson RF (1995) Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behav Neurosci 109(2):195–203PubMedCrossRefGoogle Scholar
  70. Kishimoto Y, Hirono M, Sugiyama T, Kawahara S, Nakao K, Kishio M, Katsuki M, Yoshioka T, Kirino Y (2001a) Impaired delay but normal trace eyeblink conditioning in PLCbeta4 mutant mice. NeuroReport 12(13):2919–2922PubMedCrossRefGoogle Scholar
  71. Kishimoto Y, Kawahara S, Suzuki M, Mori H, Mishina M, Kirino Y (2001b) Classical eyeblink conditioning in glutamate receptor subunit delta 2 mutant mice is impaired in the delay paradigm but not in the trace paradigm. Eur J Neurosci 13(6):1249–1253PubMedCrossRefGoogle Scholar
  72. Kleim JA, Freeman JH Jr, 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 U S A 99(20):13228–13231PubMedPubMedCentralCrossRefGoogle Scholar
  73. Knuttinen MG, Power JM, Preston AR, Disterhoft JF (2001) Awareness in classical differential eyeblink conditioning in young and aging humans. Behav Neurosci 115(4):747–757PubMedCrossRefGoogle Scholar
  74. Koekkoek SK, Hulscher HC, Dortland BR, Hensbroek RA, Elgersma Y, Ruigrok TJ, De Zeeuw CI (2003) Cerebellar LTD and learning-dependent timing of conditioned eyelid responses. Science 301(5640):1736–1739PubMedCrossRefGoogle Scholar
  75. Kotani S, Kawahara S, Kirino Y (2006) Purkinje cell activity during classical eyeblink conditioning in decerebrate guinea pigs. Brain Res 1068(1):70–81PubMedCrossRefGoogle Scholar
  76. Kronforst-Collins MA, Disterhoft JF (1998) Lesions of the caudal area of rabbit medial prefrontal cortex impair trace eyeblink conditioning. Neurobiol Learn Mem 69(2):147–162PubMedCrossRefGoogle Scholar
  77. Krupa DJ, Thompson RF (1997) Reversible inactivation of the cerebellar interpositus nucleus completely prevents acquisition of the classically conditioned eye-blink response. Learn Mem 3(6):545–556PubMedCrossRefGoogle Scholar
  78. Krupa DJ, Thompson JK, Thompson RF (1993) Localization of a memory trace in the mammalian brain. Science 260(5110):989–991PubMedCrossRefGoogle Scholar
  79. Kumaran D, Maguire EA (2006) An unexpected sequence of events: mismatch detection in the human hippocampus. PLoS Biol 4(12):e424PubMedPubMedCentralCrossRefGoogle Scholar
  80. Lavond DG, Steinmetz JE (1989) Acquisition of classical conditioning without cerebellar cortex. Behav Brain Res 33(2):113–164PubMedCrossRefGoogle Scholar
  81. Lavond DG, Hembree TL, Thompson RF (1985) Effect of kainic acid lesions of the cerebellar interpositus nucleus on eyelid conditioning in the rabbit. Brain Res 326(1):179–182PubMedCrossRefGoogle Scholar
  82. Lavond DG, Steinmetz JE, Yokaitis MH, Thompson RF (1987) Reacquisition of classical conditioning after removal of cerebellar cortex. Exp Brain Res 67(3):569–593PubMedCrossRefGoogle Scholar
  83. Lee I, Yoganarasimha D, Rao G, Knierim JJ (2004) Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430(6998):456–459PubMedCrossRefGoogle Scholar
  84. Lee KH, Mathews PJ, Reeves AM, Choe KY, Jami SA, Serrano RE, Otis TS (2015) Circuit mechanisms underlying motor memory formation in the cerebellum. Neuron 86(2):529–540PubMedPubMedCentralCrossRefGoogle Scholar
  85. Leutgeb S, Leutgeb JK, Treves A, Moser MB, Moser EI (2004) Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305(5688):1295–1298PubMedCrossRefGoogle Scholar
  86. Lincoln JS, McCormick DA, Thompson RF (1982) Ipsilateral cerebellar lesions prevent learning of the classically conditioned nictitating membrane/eyelid response. Brain Res 242(1):190–193PubMedCrossRefGoogle Scholar
  87. Linden DJ, Connor JA (1995) Long-term synaptic depression. Annu Rev Neurosci 18(1):319–357PubMedCrossRefGoogle Scholar
  88. Lisman J, Redish AD (2009) Prediction, sequences and the hippocampus. Philos T R Soc B 364(1521):1193–1201CrossRefGoogle Scholar
  89. Liu SJ, Cull-Candy SG (2005) Subunit interaction with PICK and GRIP controls Ca2+ permeability of AMPARs at cerebellar synapses. Nat Neurosci 8(6):768–775PubMedCrossRefGoogle Scholar
  90. Lu L, Leutgeb JK, Tsao A, Henriksen EJ, Leutgeb S, Barnes CA, Witter MP, Moser M-B, Moser EI (2013) Impaired hippocampal rate coding after lesions of the lateral entorhinal cortex. Nat Neurosci 16(8):1085–1093PubMedCrossRefGoogle Scholar
  91. Manns JR, Clark RE, Squire LR (2000a) Awareness predicts the magnitude of single-cue trace eyeblink conditioning. Hippocampus 10(2):181–186PubMedCrossRefGoogle Scholar
  92. Manns JR, Clark RE, Squire LR (2000b) Parallel acquisition of awareness and trace eyeblink classical conditioning. Learn Mem 7(5):267–272PubMedPubMedCentralCrossRefGoogle Scholar
  93. Manns JR, Clark RE, Squire L (2001) Single-cue delay eyeblink conditioning is unrelated to awareness. Cogn Affect Behav Neurosci 1(2):192–198PubMedCrossRefGoogle Scholar
  94. Matsushita M, Ikeda M (1970) Olivary projections to the cerebellar nuclei in the cat. Exp Brain Res 10(5):488–500PubMedGoogle Scholar
  95. Mauk MD, Steinmetz JE, Thompson RF (1986) Classical conditioning using stimulation of the inferior olive as the unconditioned stimulus. Proc Natl Acad Sci USA 83(14):5349–5353PubMedPubMedCentralCrossRefGoogle Scholar
  96. McClelland JL, McNaughton BL, O’Reilly RC (1995) Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol Rev 102(3):419–457PubMedCrossRefGoogle Scholar
  97. McCormick DA, Thompson RF (1984a) Cerebellum: essential involvement in the classically conditioned eyelid response. Science 223(4633):296–299PubMedCrossRefGoogle Scholar
  98. 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):2811–2822PubMedGoogle Scholar
  99. McCormick DA, Clark GA, Lavond DG, Thompson RF (1982) Initial localization of the memory trace for a basic form of learning. Proc Natl Acad Sci USA 79(8):2731–2735PubMedPubMedCentralCrossRefGoogle Scholar
  100. McCormick DA, Lavond DG, Thompson RF (1983) Neuronal responses of the rabbit brainstem during performance of the classically conditioned nictitating membrane (NM)/eyelid response. Brain Res 271(1):73–88PubMedCrossRefGoogle Scholar
  101. McCormick DA, Steinmetz JE, Thompson RF (1985) Lesions of the inferior olivary complex cause extinction of the classically conditioned eyeblink response. Brain Res 359(1–2):120–130PubMedCrossRefGoogle Scholar
  102. McEchron MD, Disterhoft JF (1997) Sequence of single neuron changes in CA1 hippocampus of rabbits during acquisition of trace eyeblink conditioned responses. J Neurophysiol 78(1):1030–1044PubMedCrossRefGoogle Scholar
  103. McEchron MD, Weible AP, Disterhoft JF (2001) Aging and learning-specific changes in single-neuron activity in CA1 hippocampus during rabbit trace eyeblink conditioning. J Neurophysiol 86(4):1839–1857PubMedCrossRefGoogle Scholar
  104. McLaughlin J, Skaggs H, Churchwell J, Powell DA (2002) Medial prefrontal cortex and pavlovian conditioning: trace versus delay conditioning. Behav Neurosci 116(1):37–47PubMedCrossRefGoogle Scholar
  105. Mihailoff GA (1993) Cerebellar nuclear projections from the basilar pontine nuclei and nucleus reticularis tegmenti pontis as demonstrated with PHA-L tracing in the rat. J Comp Neurol 330(1):130–146PubMedCrossRefGoogle Scholar
  106. Mintz M, Lavond David G, Zhang AA, Yun Y, Thompson Richard F (1994) Unilateral inferior olive NMDA lesion leads to unilateral deficit in acquisition and retention of eyelid classical conditioning. Behav Neural Biol 61(1):218–224PubMedCrossRefGoogle Scholar
  107. Miyata M, Kim HT, Hashimoto K, Lee TK, Cho SY, Jiang H, Wu Y et al (2001) Deficient long-term synaptic depression in the rostral cerebellum correlated with impaired motor learning in phospholipase C beta4 mutant mice. Eur J Neurosci 13(10):1945–1954PubMedCrossRefGoogle Scholar
  108. Modi MN, Dhawale AK, Bhalla US (2014) CA1 cell activity sequences emerge after reorganization of network correlation structure during associative learning. Elife 3:e01982PubMedPubMedCentralCrossRefGoogle Scholar
  109. Moita MA, Rosis S, Zhou Y, LeDoux JE, Blair HT (2003) Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning. Neuron 37(3):485–497PubMedPubMedCentralCrossRefGoogle Scholar
  110. Morrissey MD, Maal-Bared G, Brady S, Takehara-Nishiuchi K (2012) Functional dissociation within the entorhinal cortex for memory retrieval of an association between temporally discontiguous stimuli. J Neurosci 32(16):5356–5361PubMedCrossRefGoogle Scholar
  111. Moustafa AA, Wufong E, Servatius RJ, Pang KCH, Gluck MA, Myers CE (2013) Why trace and delay conditioning are sometimes (but not always) hippocampal dependent: a computational model. Brain Res 1493:48–67PubMedCrossRefGoogle Scholar
  112. Moya MV, Siegel JJ, McCord ED, Kalmbach BE, Dembrow N, Johnston D, Chitwood RA (2014) Species-specific differences in the medial prefrontal projections to the pons between rat and rabbit. J Comp Neurol 522(13):3052–3074PubMedPubMedCentralCrossRefGoogle Scholar
  113. Moyer JR, Deyo RA, Disterhoft JF (1990) Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behav Neurosci 104(2):243–252PubMedCrossRefGoogle Scholar
  114. Munera A, Gruart A, Munoz MD, Fernandez-Mas R, Delgado-Garcia JM (2001) Hippocampal pyramidal cell activity encodes conditioned stimulus predictive value during classical conditioning in alert cats. J Neurophysiol 86(5):2571–2582PubMedCrossRefGoogle Scholar
  115. Nadel L, Moscovitch M (1997) Memory consolidation, retrograde amnesia and the hippocampal complex. Curr Opin Neurobiol 7(2):217–227PubMedPubMedCentralCrossRefGoogle Scholar
  116. Nguyen-Vu TD, Kimpo RR, Rinaldi JM, Kohli A, Zeng H, Deisseroth K, Raymond JL (2013) Cerebellar Purkinje cell activity drives motor learning. Nat Neurosci 16(12):1734–1736PubMedPubMedCentralCrossRefGoogle Scholar
  117. Nicholson DA, Freeman JH Jr (2003) Addition of inhibition in the olivocerebellar system and the ontogeny of a motor memory. Nat Neurosci 6(5):532–537PubMedPubMedCentralCrossRefGoogle Scholar
  118. O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Clarendon Press, OxfordGoogle Scholar
  119. Oswald B, Knuckley B, Mahan K, Sanders C, Powell DA (2006) Prefrontal control of trace versus delay eyeblink conditioning: role of the unconditioned stimulus in rabbits (Oryctolagus cuniculus). Behav Neurosci 120(5):1033–1042PubMedCrossRefGoogle Scholar
  120. Oswald BB, Knuckley B, Maddox SA, Powell DA (2007) Ibotenic acid lesions to ventrolateral thalamic nuclei disrupts trace and delay eyeblink conditioning in rabbits. Behav Brain Res 179(1):111–117PubMedCrossRefGoogle Scholar
  121. Oswald BB, Maddox SA, Powell DA (2008) Prefrontal control of trace eyeblink conditioning in rabbits: role in retrieval of the CR? Behav Neurosci 122(4):841–848PubMedCrossRefGoogle Scholar
  122. Oswald BB, Maddox SA, Tisdale N, Powell DA (2010) Encoding and retrieval are differentially processed by the anterior cingulate and prelimbic cortices: a study based on trace eyeblink conditioning in the rabbit. Neurobiol Learn Mem 93(1):37–45PubMedCrossRefGoogle Scholar
  123. Pakaprot N, Kim S, Thompson RF (2009) The role of the cerebellar interpositus nucleus in short and long term memory for trace eyeblink conditioning. Behav Neurosci 123(1):54–61PubMedPubMedCentralCrossRefGoogle Scholar
  124. Palay SL, Chan-Palay V (1974) Cerebellar xortex. Cytology and organization. Springer, BerlinCrossRefGoogle Scholar
  125. Patterson MM, Berger TW, Thompson RF (1979) Neuronal plasticity recorded from cat hippocampus during classical conditioning. Brain Res 163(2):339–343PubMedCrossRefGoogle Scholar
  126. Penick S, Solomom PR (1991) Hippocampus, context, and conditioning. Behav Neurosci 105(5):611–617PubMedCrossRefGoogle Scholar
  127. Perrett SP, Ruiz BP, Mauk MD (1993) Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J Neurosci 13(4):1708–1718PubMedGoogle Scholar
  128. Powell DA, Churchwell J (2002) Mediodorsal thalamic lesions impair trace eyeblink conditioning in the rabbit. Learn Mem 9(1):10–17PubMedPubMedCentralCrossRefGoogle Scholar
  129. Pratt WE, Mizumori SJY (2001) Neurons in rat medial prefrontal cortex show anticipatory rate changes to predictable differential rewards in a spatial memory task. Behav Brain Res 123(2):165–183PubMedCrossRefGoogle Scholar
  130. 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):113–123PubMedCrossRefGoogle Scholar
  131. 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):10549–10560PubMedPubMedCentralCrossRefGoogle Scholar
  132. Raman IM, Bean BP (1997) Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J Neurosci 17(12):4517–4526PubMedGoogle Scholar
  133. Rescorla RA, Wagner AR (1972) A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. In Black AH, Prokasy WF (eds) Classical conditioning II. Appleton-Century-Crofts, pp 64–99Google Scholar
  134. Rogers RF, Britton GB, Steinmetz JE (2001) Learning-related interpositus activity is conserved across species as studied during eyeblink conditioning in the rat. Brain Res 905(1–2):171–177PubMedCrossRefGoogle Scholar
  135. Rudy JW, Biedenkapp JC, O’Reilly RC (2005) Prefrontal cortex and the organization of recent and remote memories: an alternative view. Learn Mem 12(5):445–446PubMedCrossRefGoogle Scholar
  136. Ryou JW, Cho SY, Kim HT (2001) Lesions of the entorhinal cortex impair acquisition of hippocampal-dependent trace conditioning. Neurobiol Learn Mem 75(2):121–127PubMedCrossRefGoogle Scholar
  137. Schade Powers A, Coburn-Litvak P, Evinger C (2010) Conditioned eyelid movement is not a blink. J Neurophysiol 103(2):641–647PubMedCrossRefGoogle Scholar
  138. Schmahmann JD, Pandya DN (1997) Anatomic organization of the basilar pontine projections from prefrontal cortices in rhesus monkey. J Neurosci 17(1):438–458PubMedGoogle Scholar
  139. Schmajuk NA, Lam Y-W, Christiansen BA (1994) Latent inhibition of rat eyeblink response. Physiol Behav 55(3):597–601PubMedCrossRefGoogle Scholar
  140. Schmaltz LW, Theios J (1972) Acquisition and extinction of a classically conditioned response in hippocampectomized rabbits (Oryctolagus cuniculus). J Comp Physiol Psych 79(2):328–333CrossRefGoogle Scholar
  141. Schonewille M, Gao Z, Boele H-J, Vinueza Veloz MF, Amerika WE, Šimek AAM, De Jeu MT et al (2011) Reevaluating the role of LTD in cerebellar motor learning. Neuron 70(1):43–50PubMedPubMedCentralCrossRefGoogle Scholar
  142. Sears LL, Steinmetz JE (1990) Acquisition of classically conditioned-related activity in the hippocampus is affected by lesions of the cerebellar interpositus nucleus. Behav Neurosci 104(5):681–692PubMedCrossRefGoogle Scholar
  143. Sears LL, Steinmetz JE (1991) Dorsal accessory inferior olive activity diminishes during acquisition of the rabbit classically conditioned eyelid response. Brain Res 545(1–2):114–122PubMedCrossRefGoogle Scholar
  144. Sears LL, Logue SF, Steinmetz JE (1996) Involvement of the ventrolateral thalamic nucleus in rabbit classical eyeblink conditioning. Behav Brain Res 74(1–2):105–117PubMedCrossRefGoogle Scholar
  145. Shibuki K, Gomi H, Chen L, Bao S, Kim JJ, Wakatsuki H, Fujisaki T et al (1996) Deficient cerebellar long-term depression, impaired eyeblink conditioning, and normal motor coordination in GFAP mutant mice. Neuron 16(3):587–599PubMedCrossRefGoogle Scholar
  146. Shohamy D, Allen MT, Gluck MA (2000) Dissociating entorhinal and hippocampal involvement in latent inhibition. Behav Neurosci 114(5):867–874PubMedCrossRefGoogle Scholar
  147. Siegel JJ, Mauk MD (2013) Persistent activity in prefrontal cortex during trace eyelid conditioning: dissociating responses that reflect cerebellar output from those that do not. J Neurosci 33(38):15272–15284PubMedPubMedCentralCrossRefGoogle Scholar
  148. Siegel JJ, Kalmbach B, Chitwood RA, Mauk MD (2012) Persistent activity in a cortical-to-subcortical circuit: bridging the temporal gap in trace eyelid conditioning. J Neurophysiol 107(1):50–64PubMedCrossRefGoogle Scholar
  149. Simon B, Knuckley B, Churchwell J, Powell DA (2005) Post-training lesions of the medial prefrontal cortex interfere with subsequent performance of trace eyeblink conditioning. J Neurosci 25(46):10740–10746PubMedCrossRefGoogle Scholar
  150. Soler-Llavina GJ, Sabatini BL (2006) Synapse-specific plasticity and compartmentalized signaling in cerebellar stellate cells. Nat Neurosci 9(6):798–806PubMedCrossRefGoogle Scholar
  151. Solomon PR, Moore JW (1975) Latent inhibition and stimulus generalization of the classically conditioned nictitating membrane response in rabbits (Oryctolagus cuniculus) following dorsal hippocampal ablation. J Comp Physiol Psychol 89(10):1192–1203PubMedCrossRefGoogle Scholar
  152. Solomon PR, Vander Schaaf ER (1986) Hippocampus and trace conditioning of the rabbit’s classically conditioned nictitating membrane response. Behav Neurosci 100(5):729–744PubMedPubMedCentralCrossRefGoogle Scholar
  153. Solomon PR, Solomon SD, Schaaf EV, Perry HE (1983) Altered activity in the hippocampus is more detrimental to classical conditioning than removing the structure. Science 220(4594):329–331PubMedCrossRefGoogle Scholar
  154. Squire LR, Alvarez P (1995) Retrograde amnesia and memory consolidation: a neurobiological perspective. Curr Opin Neurobiol 5(2):169–177PubMedPubMedCentralCrossRefGoogle Scholar
  155. Squire LR, Kandel ER (2009) Memory from mind to molecules. 2nd edn Aufl. Roberts & Company,ColoradoGoogle Scholar
  156. Squire LR, Zola-Morgan S (1991) The medial temporal lobe memory system. Science 253(5026):1380–1386PubMedCrossRefGoogle Scholar
  157. 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(2):103–115PubMedCrossRefGoogle Scholar
  158. Steinmetz JE, Rosen DJ, Chapman PF, Lavond DG, Thompson RF (1986) Classical conditioning of the rabbit eyelid response with a mossy-fiber stimulation CS: I. Pontine nuclei and middle cerebellar peduncle stimulation. Behav Neurosci 100(6):878–887PubMedCrossRefGoogle Scholar
  159. 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 USA 84(10):3531–3535PubMedPubMedCentralCrossRefGoogle Scholar
  160. Steinmetz JE, Lavond DG, Thompson RF (1989) Classical conditioning in rabbits using pontine nucleus stimulation as a conditioned stimulus and inferior olive stimulation as an unconditioned stimulus. Synapse 3(3):225–233PubMedCrossRefGoogle Scholar
  161. Steinmetz JE, Logue SF, Steinmetz SS (1992) Rabbit classically conditioned eyelid responses do not reappear after interpositus nucleus lesion and extensive post-lesion training. Behav Brain Res 51(1):103–114PubMedCrossRefGoogle Scholar
  162. Steinmetz AB, Harmon TC, Freeman JH (2013) Visual cortical contributions to associative cerebellar learning. Neurobiol Learn Mem 104:103–109PubMedPubMedCentralCrossRefGoogle Scholar
  163. Suter EE, Weiss C, Disterhoft JF (2013) Perirhinal and postrhinal, but not lateral entorhinal, cortices are essential for acquisition of trace eyeblink conditioning. Learn Mem 20(2):80–84PubMedPubMedCentralCrossRefGoogle Scholar
  164. Sutherland RJ, Rudy JW (1989) Configural association theory: the role of the hippocampal formation in learning, memory, and amnesia. Psychobiology 17(2):129–144Google Scholar
  165. Svensson P, Bengtsson F, Hesslow G (2006) Cerebellar inhibition of inferior olivary transmission in the decerebrate ferret. Exp Brain Res 168(1–2):241–253PubMedCrossRefGoogle Scholar
  166. Swenson RS, Castro AJ (1983) The afferent connections of the inferior olivary complex in rats. An anterograde study using autoradiographic and axonal degeneration techniques. Neuroscience 8(2):259–275PubMedCrossRefGoogle Scholar
  167. Takehara K, Kawahara S, Takatsuki K, Kirino Y (2002) Time-limited role of the hippocampus in the memory for trace eyeblink conditioning in mice. Brain Res 951(2):183–190PubMedCrossRefGoogle Scholar
  168. Takehara K, Kawahara S, Kirino Y (2003) Time-dependent reorganization of the brain components underlying memory retention in trace eyeblink conditioning. J Neurosci 23(30):9897–9905PubMedGoogle Scholar
  169. Takehara-Nishiuchi Kaori, McNaughton Bruce L (2008) Spontaneous changes of neocortical code for associative memory during consolidation. Science 322(5903):960–963PubMedCrossRefGoogle Scholar
  170. Takehara-Nishiuchi K, Kawahara S, Kirino Y (2005) NMDA receptor-dependent processes in the medial prefrontal cortex are important for acquisition and the early stage of consolidation during trace, but not delay eyeblink conditioning. Learn Mem 12(6):606–614PubMedPubMedCentralCrossRefGoogle Scholar
  171. Takehara-Nishiuchi K, Nakao K, Kawahara S, Matsuki N, Kirino Y (2006) Systems consolidation requires postlearning activation of NMDA receptors in the medial prefrontal cortex in trace eyeblink conditioning. J Neurosci 26(19):5049–5058PubMedCrossRefGoogle Scholar
  172. Tanninen SE, Morrissey MD, Takehara-Nishiuchi K (2013) Unilateral lateral entorhinal inactivation impairs memory expression in trace eyeblink conditioning. PLoS ONE 8(12):e84543PubMedPubMedCentralCrossRefGoogle Scholar
  173. Tanninen SE, Yu X, Giritharan T, Tran L, Bakir R, Volle J, Morrissey MD, Takehara-Nishiuchi K (2015) Cholinergic, but not NMDA, receptors in the lateral entorhinal cortex mediate acquisition in trace eyeblink conditioning. Hippocampus 25(11):36–45CrossRefGoogle Scholar
  174. Teyler TJ, DiScenna P (1986) The hippocampal memory indexing theory. Behav Neurosci 100(2):147–154PubMedCrossRefGoogle Scholar
  175. Tseng W, Guan R, Disterhoft JF, Weiss C (2004) Trace eyeblink conditioning is hippocampally dependent in mice. Hippocampus 14(1):58–65PubMedCrossRefGoogle Scholar
  176. Uylings HB, Groenewegen HJ, Kolb B (2003) Do rats have a prefrontal cortex? Behav Brain Res 146(1–2):3–17PubMedCrossRefGoogle Scholar
  177. Van Cauter T, Poucet B, Save E (2008) Unstable CA1 place cell representation in rats with entorhinal cortex lesions. Eur J Neurosci 27(8):1933–1946PubMedCrossRefGoogle Scholar
  178. Vazdarjanova A, Guzowski JF (2004) Differences in hippocampal neuronal population responses to modifications of an environmental context: evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J Neurosci 24(29):6489–6496PubMedCrossRefGoogle Scholar
  179. Vinogradova OS (2001) Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11(5):578–598PubMedCrossRefGoogle Scholar
  180. Walker AG, Steinmetz JE (2008) Hippocampal lesions in rats differentially affect long- and short-trace eyeblink conditioning. Physiol Behav 93(3):570–578PubMedCrossRefGoogle Scholar
  181. Weeks AC, Connor S, Hinchcliff R, LeBoutillier JC, Thompson RF, Petit TL (2007) Eye-blink conditioning is associated with changes in synaptic ultrastructure in the rabbit interpositus nuclei. Learn Mem 14(6):385–389PubMedPubMedCentralCrossRefGoogle Scholar
  182. Weible AP, McEchron MD, Disterhoft JF (2000) Cortical involvement in acquisition and extinction of trace eyeblink conditioning. Behav Neurosci 114(6):1058–1067PubMedCrossRefGoogle Scholar
  183. Weible AP, Weiss C, Disterhoft JF (2003) Activity profiles of single neurons in caudal anterior cingulate cortex during trace eyeblink conditioning in the rabbit. J Neurophysiol 90(2):599–612PubMedCrossRefGoogle Scholar
  184. Weible AP, O’Reilly JA, Weiss C, Disterhoft JF (2006) Comparisons of dorsal and ventral hippocampus cornu ammonis region 1 pyramidal neuron activity during trace eye-blink conditioning in the rabbit. Neuroscience 141(3):1123–1137PubMedCrossRefGoogle Scholar
  185. Weible AP, Weiss C, Disterhoft JF (2007) Connections of the caudal anterior cingulate cortex in rabbit: neural circuitry participating in the acquisition of trace eyeblink conditioning. Neuroscience 145(1):288–302PubMedCrossRefGoogle Scholar
  186. Weikart CL, Berger TW (1986) Hippocampal lesions disrupt classical learning of cross-modality reversal learning of the rabbit nictitating response membrane. Behav Brain Res 22(1):85–89PubMedCrossRefGoogle Scholar
  187. Weiss C, Disterhoft JF (1996) Eyeblink conditioning, motor control, and the analysis of limbic-cerebellar interactions. Behav Brain Sci 19(3):479–481CrossRefGoogle Scholar
  188. Weiss C, Houk JC, Gibson AR (1990) Inhibition of sensory responses of cat inferior olive neurons produced by stimulation of red nucleus. J Neurophysiol 64(4):1170–1185PubMedCrossRefGoogle Scholar
  189. Weiss C, Kronforst-Collins MA, Disterhoft JF (1996) Activity of hippocampal pyramidal neurons during trace eyeblink conditioning. Hippocampus 6(2):192–209PubMedCrossRefGoogle Scholar
  190. Weiss C, Bouwmeester H, Power JM, Disterhoft JF (1999) Hippocampal lesions prevent trace eyeblink conditioning in the freely moving rat. Behav Brain Res 99(2):123–132PubMedCrossRefGoogle Scholar
  191. Welsh JP, Harvey JA (1998) Acute inactivation of the inferior olive blocks associative learning. Eur J Neurosci 10(11):3321–3332PubMedCrossRefGoogle Scholar
  192. Welsh JP, Yamaguchi H, Zeng XH, Kojo M, Nakada Y, Takagi A, Sugimori M, Llinas RR (2005) Normal motor learning during pharmacological prevention of Purkinje cell long-term depression. Proc Natl Acad Sci USA 102(47):17166–17171PubMedPubMedCentralCrossRefGoogle Scholar
  193. Wickelgren WA (1979) Chunking and consolidation: a theoretical synthesis of semantic networks, configuring in conditioning, S-R versus cognitive learning, normal forgetting, the amnesic syndrome, and the hippocampal arousal system. Psychol Rev 86(1):44–60PubMedCrossRefGoogle Scholar
  194. Wiesendanger R, Wiesendanger M (1982) The corticopontine system in the rat. II. The projection pattern. J Comp Neurol 208(3):227–238PubMedCrossRefGoogle Scholar
  195. Winocur G, Moscovitch M, Bontempi B (2010) Memory formation and long-term retention in humans and animals: convergence towards a transformation account of hippocampal-neocortical interactions. Neuropsychologia 48(8):2339–2356PubMedPubMedCentralCrossRefGoogle Scholar
  196. Woodruff-Pak DS, Disterhoft JF (2008) Where is the trace in trace conditioning? Trends Neurosci 31(2):105–112PubMedCrossRefGoogle Scholar
  197. Woodruff-Pak DS, Lavond DG, Thompson RF (1985) Trace conditioning: abolished by cerebellar nuclear lesions but not lateral cerebellar cortex aspirations. Brain Res 348(2):249–260PubMedCrossRefGoogle Scholar
  198. Woodruff-Pak DS, Green JT, Levin SI, Meisler MH (2006) Inactivation of sodium channel Scn8A (Na-sub(v)1.6) in Purkinje neurons impairs learning in Morris water maze and delay but not trace eyeblink classical conditioning. Behav Neurosci 120(2):229–240PubMedCrossRefGoogle Scholar
  199. Yeo CH, Hardiman MJ, Glickstein M (1985a) Classical conditioning of the nictitating membrane response of the rabbit. I. Lesions of the cerebellar nuclei. Exp Brain Res 60(1):87–98PubMedCrossRefGoogle Scholar
  200. Yeo CH, Hardiman MJ, Glickstein M (1985b) Classical conditioning of the nictitating membrane response of the rabbit. II. Lesions of the cerebellar cortex. Exp Brain Res 60(1):99–113PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Psychology, Cell and Systems Biology, Neuroscience ProgramUniversity of TorontoTorontoCanada

Personalised recommendations