Behavior modification after inactivation of cerebellar dentate nuclei

Behavioral Neuroscience

Volumn 126, Issue 4, 2012, Pages 551-562

  Peterson, Todd C ^a   Villatoro, Lee ^a   Arneson, Tom ^a   Ahuja, Brittany ^a   Voss, Stephanie ^a   Swain, Rodney A ^a  

^a UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

Behavioral modification; Cerebellothalamocortical pathway; Cerebellum; Dentate nuclei; Effort based decision making

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR MODIFICATION; CEREBELLUM; CONTROLLED STUDY; DECISION MAKING; DENTATE NUCLEUS; HIGH DENSITY REINFORCEMENT; LOW DENSITY REINFORCEMENT; MALE; MAZE TEST; MENTAL TASK; NEUROMODULATION; NEUROPSYCHOLOGY; NONHUMAN; PALATABILITY; RAT; REINFORCEMENT; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL BEHAVIOR; CEREBELLUM NUCLEUS; DRUG EFFECT; FOOD DEPRIVATION; LONG EVANS RAT; MOTOR ACTIVITY; PERCEPTIVE DISCRIMINATION; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; REACTION TIME; REWARD; ROTAROD TEST;

BUPIVACAINE; LOCAL ANESTHETIC AGENT;

ANALYSIS OF VARIANCE; ANESTHETICS, LOCAL; ANIMALS; BEHAVIOR, ANIMAL; BUPIVACAINE; CEREBELLAR NUCLEI; DISCRIMINATION (PSYCHOLOGY); FOOD DEPRIVATION; MALE; MOTOR ACTIVITY; PSYCHOMOTOR PERFORMANCE; RATS; RATS, LONG-EVANS; REACTION TIME; REWARD; ROTAROD PERFORMANCE TEST;

EID: 84871904564     PISSN: 07357044     EISSN: 19390084     Source Type: Journal    
DOI: 10.1037/a0028701     Document Type: Article

References (74)

1. Alam, M. N., & Mallick, B. N. (1990). Differential acute influence of medial and lateral preoptic areas on sleep-wakefulness in freely moving rats. Brain Research, 20, 242-248. doi:10.1016/0006-8993(90)90870-H.
2. Allen, G., Buxton, R. B., Wong, E. C., & Courchesne, E. (1997). Attentional activation of the cerebellum independent of motor movement. Science, 275, 1940-1943. doi:10.1126/science.275.5308.1940.
3. Alling, K., & Poling, A. (1995). The effects of differing response-force requirements on fixed ratio responding of rats. Journal of the Experimental Analysis of Behavior, 63, 331-346. doi:10.1901/jeab.1995.63-331.
4. Andersen, R. A., & Cui, H. (2009). Inention, action planning, and decision making in parietal-frontal circuits. Neuron, 63, 568-583. doi:10.1016/j.neuron.2009.08.028.
5. Aparicio, C. F. (2001). Overmatching in rats: The barrier choice paradigm. Journal of the Experimental Analysis of Behavior, 75, 93-106. doi:10.1901/jeab.2001.75-93.
6. Assadi, S. M., Yucel, M., & Pantelis, C. (2009). Dopamine modulates neural networks involved in effort-based decision-making. Neuroscience and Behavior Reviews, 33, 383-393. doi:10.1016/j.neubiorev.2008.10.010.
7. Bauer, D. J., Kerr, A. L., & Swain, R. A. (2011). Cerebellar dentate nuclei lesions reduce motivation in appetitive operant conditioning and open field exploration. Neurobiology of Learning and Memory, 95, 166-175. doi:10.1016/j.nlm.2010.12.009.
8. Bauer, D. J., Nardi, S. A., Boehlen, M. E., Villatoro, L. O., & Swain, R. A. (2008, November). Alteration of dendritic spine morphology in prefrontal cortex following cerebellar dentate nuclei lesions in rat. Poster presented at the annual conference of the Society for Neuroscience, Washington, D. C.
9. Baxter, M. G., Parker, A. Lindner, C. C., Izquierdo, A. D., & Murray, E. A. (2000). Control of response selection by reinforcer value requires interaction of amygdale and orbital prefrontal cortex. The Journal of Neuroscience, 20, 4311-4319.
10. Boeijinga, P. H., Mulder, A. B., Pennartz, C. M., Manshanden, I., & Lopes da Silva, F. H. (1993). Responses of the nucleus accumbens following fornix/fimbria stimulation in the rat. Identification and long-term potentiation of mono- and polysynaptic pathways. Neuroscience, 53, 1049-1058. doi:10.1016/0306-4522(93)90488-2.
11. Caston, J., Chianale, C., Delhaye-Bouchard, N., & Mariani, J. (1998). Role of the cerebellum in exploration behavior. Brain Research, 808, 232-237. doi:10.1016/S0006-8993(98)00847-6.
12. Caterall, W. A., & Mackie, K. (1996). Local anesthetics. In J. G. Hardman, L. E. Limbard, P. B. Molinoff, R. W. Rudden, A. Gillman (Eds), Goodman and Gillman's the pharmalogical basis of experimental therapeutics (9th ed., pp. 321-347). New York, NY: McGraw-Hill.
13. Chambers, W. W., & Sprague, J. M. (1955). Functional localization in the cerebellum I: Organization in longitudinal cortio-nuclear zones and their contribution to the control of posture, both extrapyramidal and pyramidal. Journal of Comparative Neurobiology, 103, 105-130. doi:10.1002/cne.901030107.
14. Christian, K. M., & Thompson, R. F. (2003). Neural substrates of eyeblink conditioning: Acquisition and retention. Learning & Memory, 10, 427-455. doi:10.1101/lm.59603.
15. Chung, S. H. (1965). Effects of effort on response rate. Journal of the Experimental Analysis of Behavior, 8, 1-7. doi:10.1901/jeab.1965.8-1.
16. D'Agata, V., Drago, F., Serapide, F., & Cicirata, F. (1993). Effects of cerebellectomy on motivation-related behavior: A time-course study. Physiology & Behavior, 53, 173-176. doi:10.1016/0031-9384(93)90027-D.
17. Denk, F., Walton, M. E., Jennings, K. A., Sharp, T., Rushworth, M. F. S., & Bannerman, D. M. (2005). Differential involvement of serotonin and dopamine systems in cost-benefit decisions about delay or effort. Psychopharmacology, 179, 587-596. doi:10.1007/s00213-004-2059-4.
18. Eron, J. N., Cohen, B., Raphan, T., & Yakushin, S. B. (2008). Differential coding of head rotation by lateral-vertical canal convergent central vestibular neurons. Progressive Brain Research, 171, 313-318. doi:10.1016/S0079-6123(08)00645-6.
19. Floresco, S. B., & Ghods-Sharifi, S. (2007). Amygdala-prefrontal cortical circuitry regulates effort-based decision making. Cerebral Cortex, 17, 251-260. doi:10.1093/cercor/bhj143.
20. Floresco, S. B., St. Onge, J. R., Ghods-Sharifi, S., & Winstanley, C. A. (2008). Cortico-limbic-striatal circuits subserving different forms of cost-benefit decision making. Cognitive, Affective, & Behavioral Neuroscience, 8, 375-389. doi:10.3758/CABN.8.4.375.
21. Fujita, Y., Rosenberg, J., & Segundo, J. P. (1968). Activity of cells in the lateral vestibular nucleus as a function of head position. Journal of Physiology, 196, 1-18.
22. Hauber, W., & Sommer, S. (2009). Prefrontostriatal circuitry regulates effort-related decision making. Cerebral Cortex. doi:10.1093.
23. Hendley, E. D., Conti, L. H., Wessel, D. J., Horton, E. S., & Musty, R. E. (1987). Behavioral and metabolic effects of sucrose-supplemented feeding in hyperactive rats. American Journal of Physiology, 253, R434-R443.
24. Hodos, W., & Kalman, G. (1963). Effects of increment size and reinforce volume on progressive ratio performance. Journal of the Experimental Analysis of Behavior, 6, 387-392. doi:10.1901/jeab.1963.6-387.
25. Hodos, W. (1961). Progressive ratio as a measure of reward strength. Science, 134, 943-944. doi:10.1126/science.134.3483.943.
26. Ichinohe, N., Mori, F., & Shoumura, K. (2000). A di-synaptic projection from the lateral cerebellar nucleus to the laterodorsal part of the striatum via the central lateral nucleus of the thalamus in the rat. Brain Research, 880, 191-197. doi:10.1016/S0006-8993(00)02744-X.
27. Imamizu, H., Kuroda, T., Miyauchi, S., Yoshioka, T., & Kowato, M. (2003). Modular organization of internal models of tools in the human cerebellum. PNAS Proceedings of the National Academy of Sciences of the USA, 100, 5461-5466. doi:10.1073/pnas.0835746100.
28. Ito, M. (1982). Cerebellar control of the vestibule-ocular reflex: Around the flocculus hypothesis. Annual Review of Neuroscience, 5, 275-297. doi:10.1146/annurev.ne.05.030182.001423.
29. Joyal, C. C., Strazielle, C., & Lalonde, R. (2001). Effects of dentate nucleus lesions on spatial and postural sensorimotor learning in rats. Behavioural Brain Research, 122, 131-137. doi:10.1016/S0166-4328(00)00390-9.
30. Kasper, J., Schor, R. H., & Wilson, V. J. (1988). Response of vestibular neurons to head rotations in vertical planes. II. Response to neck stim-ulation and vestibular-neck interaction. Journal of Neurophysiology, 60, 1765-1768.
31. Kelly, R. M., & Strick, P. L. (2003). Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. The Journal of Neuroscience, 23, 8432-8444.
32. Kendall, M. G. (1973). Hiawatha designs an experiment. Journal of Applied Behavior Analysis, 6, 331-332. doi:10.1901/jaba.1973.6-331.
33. Kim, S. G., Ugurbil, K., & Strick, P. L. (1994). Activation of cerebellar nucleus during cognitive processing. Science, 265, 949-951. doi:10.1126/science.8052851.
34. Kitazawa, S., Kimura, T., & Yin, P. B. (1998). Cerebellar complex spikes encode both destinations and errors in arm movements. Nature, 392, 494-497. doi:10.1038/33141.
35. Kitazawa, S., & Yin, P. B. (2002). Prism adaptation with delayed visual error signals in the monkey. Experimental Brain Research, 144, 258-261. doi:10.1007/s00221-002-1089-6.
36. Kraeling, D. (1961). Analysis of amount of reward as a variable in learning. Journal of Comparative and Physiological Psychology, 54, 560-565. doi:10.1037/h0040833.
37. Krupa, D. J., & Thompson, R. F. (1997). Reversible inactivation of the cerebellar interpositus nucleus completely prevents acquisition of the classically conditioned eye-blink response. Learning & Memory, 3, 545-556. doi:10.1101/lm.3.6.545.
38. Kwapis, J. L., Jarome, T. J., Lonergan, M. E., & Helmstetter, F. J. (2009). Protein kinase mzeta maintains fear memory in the amygdala but not in the hippocampus. Behavioral Neuroscience, 123, 844-850. doi:10.1037/a0016343.
39. Lavond, D. G., Hembree, T. L., & Thompson, R. F. (1985). Effect of kainic acid lesions of the cerebellar interpositus nucleus on eyelid conditioning in the rabbit. Brain Research, 326, 179-182. doi:10.1016/0006-8993(85)91400-3.
40. Lincoln, J. S., McCormick, D. A., & Thompson, R. F. (1982). Ipsilateral cerebellar lesions prevent learning of the classically conditioned nictitating membrane/eyelid response. Brain Research, 242, 190-193. doi:10.1016/0006-8993(82)90510-8.
41. Martin, T. A., Keating, J. G., Goodkin, H. P., Bastian, A. J., & Thach, W. T. (1996). Throwing while looking through prisms: Focal olivocerebellar lesions impair adaptation. Brain: A Journal of Neurology, 119, 1183-1198. doi:10.1093/brain/119.4.1183.
42. Maxwell, S. E., & Delaney, H. D. (2004). Designing experiments and analyzing data: A model comparison perspective (2nd ed.). Mahwah, NJ: Lawrence Erlbaum Associates.
43. McCormick, D. A., Lavond, D. G., Clark, G. A. Kettner, R. E. Rising, C. E., & Thompson, R. F. (1981). The engram found? Role of the cerebellum in classical conditioning of nictitating membrane and eyelid responses. Bulletin of the Psychonomic Society, 18, 103-105.
44. McCormick, D. A., Steinmetz, J. E., & Thompson, R. F. (1985). Lesions of the inferior olivary complex cause extinction of the classically conditioned eyeblink response. Brain Research, 359, 120-130. doi:10.1016/0006-8993(85)91419-2.
45. McCormick, D. A., & Thompson, R. F. (1984). Cerebellum: Essential involvement in the classically conditioned eyelid response. Science, 223, 296-299. doi:10.1126/science.6701513.
46. Middleton, F. A., & Strick, P. L. (1994). Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. Science, 266, 458-461. doi:10.1126/science.7939688.
47. Middleton, F. A., & Strick, P. L. (1997). Cerebellar output channels. Neurobiology, 41, 61-82.
48. Middleton, F. A., & Strick, P. L. (2000). Basal ganglia and cerebellar loops: Motor and cognitive circuits. Brain Research Reviews, 31, 236-250. doi:10.1016/S0165-0173(99)00040-5.
49. Middleton, F. A., & Strick, P. L. (2001). Cerebellar projections to the prefrontal cortex of the primate. The Journal of Neuroscience, 21, 700-712.
50. Mowrer, O. H., & Jones, H. (1943). Extinction and behavioral variability as a function of effortfulness of a task. Journal of Experimental Psychology, 33, 369-386. doi:10.1037/h0056182.
51. Noblett, K. L., & Swain, R. A. (2003). Pretraining enhances recovery from visuospatial deficit following cerebellar dentate nucleus lesion. Behavioral Neuroscience, 117, 785-798. doi:10.1037/0735-7044.117.4.785.
52. Paxinos, G., & Watson, C. (1998). The rat brain in stereotaxic coordinates (4th ed.). New York, NY: Academic Press.
53. Richardson, J. V., & Baron, A. (2008). Avoidance of timeout from response-independent food: Effects of delivery rate and quality. Journal of the Experimental Analysis of Behavior, 89, 169-181. doi:10.1901/jeab.2008.89-169.
54. Roesch, M. R., Singh, T., Brown, P. L., Mullins, S. E., & Schoenbaum, G. (2009). Ventral striatal neurons encode the value of the chosen action in rats deciding between differently delayed or sized rewards. The Journal of Neuroscience, 29, 13365-13376. doi:10.1523/JNEUROSCI.2572-09.2009.
55. Rosen, A. J. (1966). Incentive-shift performance as a function of magnitude and number of sucrose rewards. Journal of Comparative and Physiological Psychology, 62, 487-490. doi:10.1037/h0023950.
56. Salamone, J. D., Cousins, M. S., & Bucher, S. (1994). Anhedonia or anergia? Effects of halhaloperidol and nucleus accumbens dopamine depletion on instrumental response selection in a T-maze cost/benefit procedure. Behavioural Brain Research, 65, 221-229. doi:10.1016/0166-4328(94)90108-2.
57. Schmahmann, J. D. (1996). From movement to thought: Anatomic substrates of the cerebellar contribution to cognitive processing. Human Brain Mapping, 4, 174-198. doi:10.1002/(SICI)1097-0193(1996)4:3_174::AID-HBM3_3.0.CO;2-0.
58. Schmahmann, J. D. (1997). The cerebellum and cognition. San Diego, CA: Academic Press.
59. Sclafani, A., & Ackroff, K. (2003). Reinforcement value of sucrose measured by progressive ratio operant licking in the rat. Physiology & Behavior, 79, 663-670. doi:10.1016/S0031-9384(03)00143-4.
60. Sclafani, A., Touzani, K., & Bodnar, R. J. (2011). Dopamine and learned food preference. Physiology & Behavior, 104, 64-68. doi:10.1016/j.physbeh.2011.04.039.
61. Sears, L. L., & Steinmetz, J. E. (1991). Dorsal accessory inferior olive activity diminishes during acquisition of the rabbit classically conditioned eyelid response. Brain Research, 545, 114-122. doi:10.1016/0006-8993(91)91276-7.
62. Shinkman, P. G., Swain, R. A., & Thompson, R. F. (1996). Classical condition with electrical stimulation of cerebellum as both conditioned and unconditioned stimulus. Behavioral Neuroscience, 110, 914-921. doi:10.1037/0735-7044.110.5.914.
63. Sidman, M. (1960). Tactics of scientific research. New York, NY: Basic Books.
64. Skjoldager, P., Pierre, P. J., & Mittleman, G. (1993). Reinforcer magnitude and progressive ratio responding in the rat: Effects of increased effort, prefeeding, and extinction. Learning and Motivation, 24, 303-343. doi:10.1006/lmot.1993.1019.
65. Stafford, D., & Branch, M. N. (1998). Effects of step size and break-point criterion on progressive-ratio performance. Journal of the Experimental Analysis of Behavior, 70, 123-138. doi:10.1901/jeab.1998.70-123.
66. Swain, R. A., Shinkman, P. G., Thompson, J. K., Grethe, J. S., & Thompson, R. F. (1999). Essential neuronal pathways for reflex and conditioned response initiation in an intracerebellar stimulation paradigm and the impact of unconditioned stimulus preexposure on learning rate. Neurobiology of Learning and Memory, 71, 167-193. doi:10.1006/nlme.1998.3872.
67. Tehovnik, E. J., & Sommer, M. A. (1997). Effective spread and timecourse of neural inactivation caused by lidocaine injection in monkey cerebral cortex. Journal of Neuroscience Methods, 74, 17-26. doi:10.1016/S0165-0270(97)02229-2.
68. Thoma, P., Bellebaum, C., Koch, B., Schwarz, M., & Daum, I. (2008). The cerebellum is involved in reward-based reversal learning. The Cerebellum, 7, 433-443. doi:10.1007/s12311-008-0046-8.
69. Thompson, R. F. (1986). The neurobiology of learning and memory. Science, 233, 941-947. doi:10.1126/science.3738519.
70. Vitali, R., & Clarke, S. (2004). Improved rotorod performance and hyperactivity in mice deficient in a protein repair methlytransferase. Behavioural Brain Research, 153, 129-141. doi:10.1016/j.bbr.2003.11.007.
71. Walton, M. E., Bannerman, D. M., & Rushworth, M. F. S. (2002). The role of rat medial frontal cortex in effort-based decision making. The Journal of Neuroscience, 22, 10996-11003.
72. Walton, M. E., Bannerman, D. M., & Rushworth, M. F. S. (2003). Functional specialization within medial frontal cortex of the anterior cingulated for evaluating effort-related decisions. The Journal of Neuroscience, 23, 6475-6479.
73. Weeks, A. C. W., Connor, S. Hinchcliff, R., LeBoutillier, J. C. Thompson, R. F., & Petit, T. L. (2007). Eye-blink conditioning is associated with changes in synaptic ultrastructure in the rabbit interpositus nuclei. Learning & Memory, 14, 385-389. doi:10.1101/lm.348307.
74. Zainos, A., DeAnda, R., Chavez, L., & Garcia-Munoz, M. (1984). Turning behavior, barrel rolling, and sensory neglect induced by picrotoxin in the thalamus. Experimental Neurology, 83, 534-547. doi:10.1016/0014-4886(84)90121-3.