Functional disconnection of the substantia nigra pars compacta from the pedunculopontine nucleus impairs learning of a conditioned avoidance task

Neurobiology of Learning and Memory

Volumn 94, Issue 2, 2010, Pages 229-239

  Bortolanza, Mariza ^a   Wietzikoski, Evellyn C ^a   Boschen, Suelen L ^a   Dombrowski, Patricia A ^a   Latimer, Mary ^a,b   MacLaren, Duncan A A ^a,c   Winn, Philip ^a,c   Cunha, Claudio Da ^a  

^a FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

^c UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

Active avoidance; Basal ganglia; Dopamine; Parkinson

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; IBOTENIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN DAMAGE; BRAIN FUNCTION; COGNITIVE DEFECT; CONTROLLED STUDY; FOOTSHOCK; LEARNING DISORDER; MALE; NEUROPATHOLOGY; NONHUMAN; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; RAT; REACTION TIME; SUBSTANTIA NIGRA;

EID: 77955562814     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2010.05.011     Document Type: Article

References (95)

1. Aguilar M.A., Mari-Sanmillan M.I., Morant-Deusa J.J., Minarro J. Different inhibition of conditioned avoidance response by clozapine and DA D-1 and D-2 antagonists in male mice. Behavioral Neuroscience 2000, 114:389-400.
2. Alderson H.L., Brown V.J., Latimer M.P., Brasted P.J., Robertson A.H., Winn P. Excitotoxic lesions of the pedunculopontine tegmental nucleus in rats: An examination of the perception of reward strength measured by responding on a progressive ratio schedule of reinforcement. Neuroscience 2002, 112:417-425.
3. Alderson H.L., Latimer M.P., Blaha C.D., Phillips A.G., Winn P. An examination of d-amphetamine self-administration in pedunculopontine tegmental nucleus-lesioned rats. Neuroscience 2004, 125:349-358.
4. Alderson H.L., Winn P. The pedunculopontine and reinforcement 2005, Springer, New York.
5. Alexander G.E., Delong M.R., Strick P.L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience 1986, 9:357-381.
6. Aravamuthan B.R., Bergstrom D.A., French R.A., Taylor J.J., Parr-Brownlie L.C., Walters J.R. Altered neuronal activity relationships between the pedunculopontine nucleus and motor cortex in a rodent model of Parkinson's disease. Experimental Neurology 2008, 213:268-280.
7. Balleine B.W., Liljeholm M., Ostlund S.B. The integrative function of the basal ganglia in instrumental conditioning. Behavioural Brain Research 2009, 199:43-52.
8. Beninato M., Spencer R.F. A cholinergic projection to the rat substantia-nigra from the pedunculopontine tegmental nucleus. Brain Research 1987, 412:169-174.
9. Beninato M., Spencer R.F. The cholinergic innervation of the rat substantia nigra - A light and electron-microscopic immunohistochemical study. Experimental Brain Research 1988, 72:178-184.
10. Brischoux F., Chakraborty S., Brierley D.I., Ungless M.A. Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:4893-4899.
11. Calabresi P., Picconi B., Tozzi A., Di Filippo M. Dopamine-mediated regulation of corticostriatal synaptic plasticity. Trends in Neurosciences 2007, 30:211-219.
12. Calabresi P., Pisani A., Mercuri N.B., Bernardi G. Long-term potentiation in the striatum is unmasked by removing the voltage-dependent magnesium block of NMDA receptor channels. European Journal of Neuroscience 1992, 4:929-935.
13. Carbon M., Marie R.M. Functional imaging of cognition in Parkinson's disease. Current Opinion in Neurology 2003, 16:475-480.
14. Carlson J.D., Pearlstein R.D., Buchholz J., Iacono R.P., Maeda G. Regional metabolic changes in the pedunculopontine nucleus of unilateral 6-hydroxydopamine Parkinson's model rats. Brain Research 1999, 828:12-19.
15. Clarke P.B.S., Hommer D.W., Pert A., Skirboll L.R. Innervation of substantia nigra neurons by cholinergic afferents from pedunculopontine nucleus in the rat - neuroanatomical and electrophysiological evidence. Neuroscience 1987, 23:1011-1019.
16. Cohen M.X., Frank M.J. Neurocomputational models of basal ganglia function in learning, memory and choice. Behavioural Brain Research 2009, 199:141-156.
17. Corrigall W.A., Coen K.M., Zhang J., Adamson K.L. GABA mechanisms in the pedunculopontine tegmental nucleus influence particular aspects of nicotine self-administration selectively in the rat. Psychopharmacology 2001, 158:189-197.
18. Corrigall W.A., Coen K.M., Zhang J., Adamson K.L. Pharmacological manipulations of the pedunculopontine tegmental nucleus in the rat reduce self-administration of both nicotine and cocaine. Psychopharmacology 2002, 160:198-205.
19. Da Cunha C., Gevaerd M.S., Vital M., Miyoshi E., Andreatini R., Silveira R., et al. Memory disruption in rats with nigral lesions induced by MPTP: A model for early Parkinson's disease amnesia. Behavioural Brain Research 2001, 124:9-18.
20. Da Cunha C., Wietzikoski E.C., Dombrowski P., Santos L.M., Bortolanza M., Boschen S.L., et al. Learning processing in the basal ganglia: A mosaic of broken mirrors. Behavioural Brain Research 2009, 199:156-169.
21. Da Cunha C., Wietzikoski E.C., Ferro M.M., Martinez G.R., Vital M., Hipolide D., et al. Hemiparkinsonian rats rotate toward the side with the weaker dopaminergic neurotransmission. Behavioural Brain Research 2008, 189:364-372.
22. Da Cunha C., Wietzikoski S., Wietzikoski E.C., Miyoshi E., Ferro M.M., Anselmo-Franci J.A., et al. Evidence for the substantia nigra pars compacta as an essential component of a memory system independent of the hippocampal memory system. Neurobiology of Learning and Memory 2003, 79:236-242.
23. Da Cunha C., Wietzikoski S., Wietzikoski E.C., Silva M.H.C., Chandler J., Ferro M.M., et al. Pre-training to find a hidden platform in the Morris water maze can compensate for a deficit to find a cued platform in a rat model of Parkinson's disease. Neurobiology of Learning and Memory 2007, 87:451-463.
24. Del Guante M.A.D., Rivas M., Prado-Alcala R.A., Quirarte G.L. Amnesia produced by pre-training infusion of serotonin into the substantia nigra. Neuroreport 2004, 15:2527-2529.
25. Di Giovanni G., Shi W.X. Effects of scopolamine on dopamine neurons in the substantia nigra: Role of the pedunculopontine tegmental nucleus. Synapse 2009, 63:673-680.
26. Dubois B., Pillon B. Cognitive deficits in Parkinson's disease. Journal of Neurology 1997, 244:2-8.
27. Faure A., Haberland U., Conde F., El Massioui N. Lesion to the nigrostriatal dopamine system disrupts stimulus-response habit formation. Journal of Neuroscience 2005, 25:2771-2780.
28. Fernandez-Ruiz J., Wang J., Aigner T.G., Mishkin M. Visual habit formation in monkeys with neurotoxic lesions of the ventrocaudal neostriatum. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:4196-4201.
29. Ferro M.M., Bellissimo M.I., Anselmo-Franci J.A., Angellucci M.E.M., Canteras N.S., Da Cunha C. Comparison of bilaterally 6-OHDA- and MPTP-lesioned rats as models of the early phase of Parkinson's disease: Histological, neurochemical, motor and memory alterations. Journal of Neuroscience Methods 2005, 148:78-87.
30. Fujimoto K., Ikeguchi K., Yoshida M. Impaired acquisition, preserved retention and retrieval of avoidance-behavior after destruction of pedunculopontine nucleus areas in the rat. Neuroscience Research 1992, 13:43-51.
31. Fujimoto K., Yoshida M., Ikeguchi K., Niijima K. Impairment of active-avoidance produced after destruction of pedunculopontine nucleus areas in the rat. Neuroscience Research 1989, 6:321-328.
32. Futami T., Takakusaki K., Kitai S.T. Glutamatergic and cholinergic inputs from the pedunculopontine tegmental nucleus to dopamine neurons in the substantia-nigra pars compacta. Neuroscience Research 1995, 21:331-342.
33. Gevaerd M.S., Miyoshi E., Silveira R., Canteras N.S., Takahashi R.N., Da Cunha C. L-dopa restores striatal dopamine level but fails m to reverse MPTP-induced memory deficits in rats. International Journal of Neuropsycopharmacology 2001, 4:361-370.
34. Gevaerd M.S., Takahashi R.N., Silveira R., Da Cunha C. Caffeine reverses the memory disruption induced by intra-nigral MPTP-injection in rats. Brain Research Bulletin 2001, 55:101-106.
35. Gomez-Gallego M., Fernandez-Villalba E., Fernandez-Barreiro A., Herrero M.T. Changes in the neuronal activity in the pedunculopontine nucleus in chronic MPTP-treated primates: An in situ hybridization study of cytochrome oxidase subunit I, choline acetyl transferase and substance P mRNA expression. Journal of Neural Transmission 2007, 114:319-326.
36. Góngora-Alfaro J.L., Hernandez-Lopez S., Martinez-Fong D., Flores G., Aceves J. Circling behavior elicited by cholinergic transmission in the substantia nigra pars compacta: Involvement of nicotinic and muscarinic receptors. Neuroscience 1996, 71:729-734.
37. Gould E., Woolf N.J., Butcher L.L. Cholinergic projections to the substantia nigra from the pedunculopontine and laterodorsal tegmental nuclei. Neuroscience 1989, 28:611-623.
38. Grahn J.A., Parkinson J.A., Owen A.M. The role of the basal ganglia in learning and memory: Neuropsychological studies. Behavioural Brain Research 2009, 199:53-60.
39. Grahn J.A., Parkinson J.A., Owen A.M. The role of the basal ganglia in learning and memory: Neuropsychological studies. Behavioural Brain Research 2009, 199:53-60.
40. Harik S.I., Schmidley J.W., Iacofano L.A., Blue P., Arora P.K., Sayre L.M. On the mechanisms underlying 1-methyl-4phenyl-1,2,3,6-tetrahydropiridine neurotoxicity: The effect of perinigral infusion of 1-methyl-4-phenyl-1,2,3,6-tetrahydropiridine, its metabolite and their analogs in rat. Journal of Pharmacology and Experimental Therapeutics 1987, 241:669-676.
41. Hood K.L., Postle B.R., Corkin S. An evaluation of the concurrent discrimination task as a measure of habit learning: Performance of amnesic subjects. Neuropsychologia 1999, 37:1375-1386.
42. Ikeda H., Akiyama G., Matsuzaki S., Sato M., Moribe S., Koshikawa N., et al. Role of GABA(A) receptors in the pedunculopontine tegmental nucleus in rat turning behavior. International Journal of Neuropsychopharmacology 2004, 7:S289.
43. Inglis W.L., Dunbar J.S., Winn P. Outflow from the nucleus accumbens to the pedunculopontine tegmental nucleus: A dissociation between locomotor activity and the acquisition of responding for conditioned reinforcement stimulated by amphetamine. Neuroscience 1994, 62:51-64.
44. Inglis W.L., Olmstead M.C., Robbins T.W. Pedunculopontine tegmental nucleus lesions impair stimulus-reward learning in autoshaping and conditioned reinforcement paradigms. Behavioral Neuroscience 2000, 114:285-294.
45. Izquierdo I., Bevilaqua L.R., Rossato J.I., Bonini J.S., Da Silva W.C., Medina J.H., et al. The connection between the hippocampal and the striatal memory systems of the brain: A review of recent findings. Neurotoxicity Research 2006, 10:113-121.
46. Jhou T.C., Fields H.L., Baxter M.G., Saper C.B., Holland P.C. The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses. Neuron 2009, 61:786-800.
47. Joshua M., Adler A., Mitelman R., Vaadia E., Bergman H. Midbrain dopaminergic neurons and striatal cholinergic interneurons encode the difference between reward and aversive events at different epochs of probabilistic classical condition in trials. Journal of Neuroscience 2008, 28:11673-11684.
48. Juri C., Chana P. Levodopa for Parkinson's disease. What have we learned?. Revista Medica De Chile 2006, 134:893-901.
49. Keating G.L., Winn P. Examination of the role of the pedunculopontine tegmental nucleus in radial maze tasks with or without a delay. Neuroscience 2002, 112:687-696.
50. Kessler J., Markowitsch H.J., Sigg G. Memory related role of the posterior cholinergic system. International Journal of Neuroscience 1986, 30:101-119.
51. Kimura M. Role of basal ganglia in behavioral learning. Neuroscience Research 1995, 22:353-358.
52. Knowlton B.J., Squire L.R., Paulsen J.S., Swerdlow N.R., Swenson M., Butters N. Dissociations within nondeclarative memory in Huntington's disease. Neuropsychology 1996, 10:538-548.
53. Kobayashi Y., Okada K.C. Reward prediction error computation in the pedunculopontine tegmental nucleus neurons. Reward and Decision Making in Corticobasal Ganglia Networks 2007, 1104:310-323.
54. Kumar P., Kaundal R.K., More S., Sharma S.S. Beneficial effects of pioglitazone on cognitive impairment in MPTP model of Parkinson's disease. Behavioural Brain Research 2009, 197:398-403.
55. Matsumoto M., Hikosaka O. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 2009, 459:838-842.
56. Matsumoto M., Hikosaka O. Representation of negative motivational value in the primate lateral habenula. Nature Neuroscience 2009, 12:77-84.
57. Mazzone P., Lozano A., Stanzione P., Galati S., Scarnati E., Peppe A., et al. Implantation of human pedunculopontine nucleus: A safe and clinically relevant target in Parkinson's disease. Neuroreport 2005, 16:1877-1881.
58. Mena-Segovia P., Winn P., Bolam J.P. Cholinergic modulation of midbrain dopaminergic systems. Brain Research Reviews 2008, 58:265-271.
59. Miyoshi E., Wietzikoski S., Camplessei M., Silveira R., Takahashi R.N., Da Cunha C. Impaired learning in a spatial working memory version and in a cued version of the water maze in rats with MPTP-induced mesencephalic dopaminergic lesions. Brain Research Bulletin 2002, 58:41-47.
60. Morris G., Schmidt R., Bergman H. Striatal action-learning based on dopamine concentration. Experimental Brain Research 2010, 200:307-317.
61. Ogren S.O., Archer T. Effects of typical and atypical antipsychotic-drugs on 2-way active-avoidance - relationship to da receptor blocking profile. Psychopharmacology 1994, 114:383-391.
62. Okada K., Toyama K., Inoue Y., Isa T., Kobayashi Y. Different pedunculopontine tegmental neurons signal predicted and actual task rewards. Journal of Neuroscience 2009, 29:4858-4870.
63. Olmstead M.C., Franklin K.B.J. Lesions of the pedunculopontine tegmental nucleus block drug-induced reinforcement but not amphetamine-induced locomotion. Brain Research 1994, 638:29-35.
64. Olmstead M.C., Robbins T.W., Everitt B.J. Basal forebrain cholinergic lesions enhance conditioned approach responses to stimuli predictive of food. Behavioral Neuroscience 1998, 112:611-629.
65. Orieux G., Francois C., Feger J., Yelnik J., Vila M., Ruberg M., et al. Metabolic activity of excitatory parafascicular and pedunculopontine inputs to the subthalamic nucleus in a rat model of Parkinson's disease. Neuroscience 2000, 97:79-88.
66. Packard M.G., McGaugh J.L. Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: Further evidence for multiple memory systems. Behavioural Neuroscience 1992, 106:439-446.
67. Packard M.G., McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiology of Learning and Memory 1996, 65:65-72.
68. Pan W.X., Hyland B.I. Pedunculopontine tegmental nucleus controls conditioned responses of midbrain dopamine neurons in behaving rats. Journal of Neuroscience 2005, 25:4725-4732.
69. Parkinson J.A., Robbins T.W., Everitt B.J. Dissociable roles of the central and basolateral amygdala in appetitive emotional learning. European Journal of Neuroscience 2000, 12:405-413.
70. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2005, Academic Press, Ltd, San Diego, CA, USA.
71. Pierantozzi M., Palmieri M.G., Galati S., Stanzione P., Peppe A., Tropepi D., et al. Pedunculopontine nucleus deep brain stimulation changes spinal cord excitability in Parkinson's disease patients. Journal of Neural Transmission 2008, 115:731-735.
72. Redgrave P., Gurney K., Reynolds J. What is reinforced by phasic dopamine signals?. Brain Research Reviews 2008, 58:322-339.
73. Roncacci S., Troisi E., Carlesimo G.A., Nocentini U., Caltagirone C. Implicit memory in Parkinsonian patients: Evidence for deficient skill learning. European Neurology 1996, 36:154-159.
74. Saavedra J.M., Brownstein M.J., Kizer J.S., Palkovits M. Biogenic amines and related enzymes in the circumventricular organs of the rat. Brain Research 1976, 107:412-417.
75. Salmon D.P., Butters N. Neurobiology of skill and habit learning. Current Opinion in Neurobiology 1995, 5:184-190.
76. Satorra-Marin N., Coll-Andreau M., Portell-Cortes I., Aldavert-Vera L., Morgado-Bernal I. Impairment of two-way active avoidance after pedunculopontine tegmental nucleus lesions: Effects of conditioned stimulus duration. Behavioural Brain Research 2001, 118:1-9.
77. Scarnati E., Campana E., Pacitti C. Pedunculopontine-evoked excitation of substantia nigra neurons in the rat. Brain Research 1984, 304:351-361.
78. Scarnati E., Proia A., Campana E., Pacitti C. A microiontophoretic study on the nature of the putative synaptic neurotransmitter involved in the pedunculopontine-substantia nigra pars compacta excitatory pathway of the rat. Experimental Brain Research 1986, 62:470-478.
79. Schultz W. Multiple dopamine functions at different time courses. Annual Review of Neuroscience 2007, 30:259-288.
80. Schulz, D., & Canbeyli, R. (1999). Freezing behavior in BNST-lesioned Wistar rats. In J. F. McGinty (Ed.), Advancing from the ventral striatum to the extended amygdala - Implications for neuropsychiatry and drug abuse: In honor of Lennart Heimer (pp. 728-731).
81. Sesack S.R., Grace A.A. Cortico-basal ganglia reward network: Microcircuitry. Neuropsychopharmacology 2010, 35:27-47.
82. Sparks P.D., Ledoux J.E. Septal-lesions potentiate freezing behavior to contextual but not to phasic conditioned-stimuli in rats. Behavioral Neuroscience 1995, 109:184-188.
83. Stefani A., Lozano A.M., Peppe A., Stanzione P., Galati S., Tropepi D., et al. Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson's disease. Brain 2007, 130:1596-1607.
84. Taylor C.L., Kozak R., Latimer M.P., Winn P. Effects of changing reward on performance of the delayed spatial win-shift radial maze task in pedunculopontine tegmental nucleus lesioned rats. Behavioural Brain Research 2004, 153:431-438.
85. Timar J., Knoll B., Jona G., Knoll J. Inhibition of acquisition of conditioned avoidance responses by substantia nigra lesion. Naunyn-Schmiedebergs Archives of Pharmacology 1974, 284:R83.
86. Treit D., Menard J. Dissociations among the anxiolytic effects of septal, hippocampal, and amygdaloid lesions. Behavioral Neuroscience 1997, 111:653-658.
87. Versteeg D.H., Van Der Gugten J., De Jong W., Palkovits M. Regional concentrations of noradrenaline and dopamine in rat brain. Brain Research 1976, 113:563-574.
88. Wang A.L., Liou Y.M., Pawlak C.R., Ho Y.J. Involvement of NMDA receptors in both MPTP-induced neuroinflammation and deficits in episodic-like memory in Wistar rats. Behavioural Brain Research 2010, 208:38-46.
89. White N.M. Some highlights of research on the effects of caudate nucleus lesions over the past 200 years. Behavioural Brain Research 2009, 199:3-23.
90. Wickens J.R. Synaptic plasticity in the basal ganglia. Behavioural Brain Research 2009, 199:119-128.
91. Wilson D.I.G., MacLaren D.A.A., Winn P. Bar pressing for food: differential consequences of lesions to the anterior versus posterior pedunculopontine. European Journal of Neuroscience 2009, 30:504-513.
92. Woolf N.J., Butcher L.L. Cholinergic systems in the rat-brain. 3. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Research Bulletin 1986, 16:603-637.
93. Yin H.H., Knowlton B.J. The role of the basal ganglia in habit formation. Nature Reviews Neuroscience 2006, 7:464-476.
94. Zokoll M.A., Klump G.M., Langemann U. Auditory memory for temporal characteristics of sound. Journal of Comparative Physiology a-Neuroethology Sensory Neural and Behavioral Physiology 2008, 194:457-467.
95. Zuddas A., Corsini G.U., Schinelli S., Johannessen J.N., Diporzio U., Kopin I.J. MPTP treatment combined with ethanol or acetaldehyde selectively destroys dopaminergic-neurons in mouse substantia nigra. Brain Research 1989, 501:1-10.