Loss of asymmetric spine synapses in prefrontal cortex of motor-asymptomatic, dopamine-depleted, cognitively impaired MPTP-treated monkeys

International Journal of Neuropsychopharmacology

Volumn 16, Issue 4, 2013, Pages 905-912

  Elsworth, John D ^a   Leranth, Csaba ^a   Redmond, D Eugene ^a   Roth, Robert H ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Dendritic spine; dopamine; Parkinson's disease; prefrontal cortex; synapse

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; DOPAMINE;

ARTICLE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DENDRITIC SPINE; ENTORHINAL CORTEX; HAPLORHINI; MALE; MOTOR DYSFUNCTION; NEUROTRANSMISSION; NONHUMAN; PARKINSON DISEASE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SYNAPSE;

ANIMALS; CERCOPITHECUS AETHIOPS; COGNITION DISORDERS; DENDRITIC SPINES; DOPAMINE; MALE; PARKINSONIAN DISORDERS; PREFRONTAL CORTEX; SYNAPSES;

EID: 84875711161     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145712000892     Document Type: Article

References (47)

1. Alexander GE, DeLong MR, Strick PL (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience 9, 357-381.
2. Bean AJ, Roth RH (1991). Effects of haloperidol administration on in vivo extracellular dopamine in striatum and prefrontal cortex after partial dopamine lesions. Brain Research 549, 155-158.
3. Berger B, Gaspar P, Verney C (1991). Dopaminergic innervation of the cerebral cortex: unexpected differences between rodents and primates. Trends in Neurosciences 14, 21-27.
4. Blanpied TA, Ehlers MD (2004). Microanatomy of dendritic spines: emerging principles of synaptic pathology in psychiatric and neurological disease. Biological Psychiatry 55, 1121-1127.
5. Brozoski TJ, Brown RM, Rosvold HE, Goldman PS (1979). Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Science 205, 929-932.
6. Calabrese B, Wilson MS, Halpain S (2006). Development and regulation of dendritic spine synapses. Physiology (Bethesda) 21, 38-47.
7. Carlsson A, Waters N, Holm-Waters S, Tedroff J, et al. (2001). Interactions between monoamines, glutamate, and GABA in schizophrenia: new evidence. Annual Review of Pharmacology and Toxicology 41, 237-260.
8. Clinton SM, Sucharski IL, Finlay JM (2006). Desipramine attenuates working memory impairments induced by partial loss of catecholamines in the rat medial prefrontal cortex. Psychopharmacology 183, 404-412.
9. Day M, Wang Z, Ding J, An X, et al. (2006). Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nature Neuroscience 9, 251-259.
10. Dubois B, Pillon B (1997). Cognitive deficits in Parkinson's disease. Journal of Neurology 244, 2-8.
11. Elsworth JD, Hajszan T, Leranth C, Roth RH (2011). Loss of asymmetric spine synapses in dorsolateral prefrontal cortex of cognitively impaired phencyclidine-treated monkeys. International Journal of Neuropsychopharmacology, 14, 1411-1415.
12. Elsworth JD, Taylor JR, Sladek Jr. JR, Collier TJ, et al. (2000). Striatal dopaminergic correlates of stable Parkinsonism and degree of recovery in old-world primates one year after MPTP treatment. Neuroscience 95, 399-408.
13. Fernandez-Ruiz J, Doudet DJ, Aigner TG (1995). Long-term cognitive impairment in MPTP-treated rhesus monkeys. Neuroreport 7, 102-104.
14. Fox SH, Brotchie JM (2010). The MPTP-lesioned non-human primate models of Parkinson's disease. Past, present, and future. Progress in Brain Research 184, 133-157.
15. Fuster J (2008). The Prefrontal Cortex. London: Academic Press.
16. German DC, Dubach M, Askari S, Speciale SG, et al. (1988). 1-Methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-induced Parkinsonian syndrome in Macaca fascicularis: which midbrain dopaminergic neurons are lost? Neuroscience 24, 161-174.
17. Goldman-Rakic PS (1995). Cellular basis of working memory. Neuron 14, 477-485.
18. Goldman-Rakic PS, Brown RM (1981). Regional changes of monoamines in cerebral cortex and subcortical structures of aging rhesus monkeys. Neuroscience 6, 177-187.
19. Goldman-Rakic PS, Leranth C, Williams SM, Mons N, et al. (1989). Dopamine synaptic complex with pyramidal neurons in primate cerebral cortex. Proceedings of the National Academy of Sciences USA 86, 9015-9019.
20. Ingham CA, Hood SH, Taggart P, Arbuthnott GW (1998). Plasticity of synapses in the rat neostriatum after unilateral lesion of the nigrostriatal dopaminergic pathway. Journal of Neuroscience 18, 4732-4743.
21. Jay TM (2003). Dopamine: a potential substrate for synaptic plasticity and memory mechanisms. Progress in Neurobiology 69, 375-390.
22. Jentsch JD, Dazzi L, Chhatwal JP, Verrico CD, et al. (1998). Reduced prefrontal cortical dopamine, but not acetylcholine, release in vivo after repeated, intermittent phencyclidine administration to rats. Neuroscience Letters 258, 175-178.
23. Jentsch JD, Redmond Jr. DE, Elsworth JD, Taylor JR, et al. (1997a). Enduring cognitive deficits and cortical dopamine dysfunction in monkeys after long-term administration of phencyclidine. Science 277, 953-955.
24. Jentsch JD, Taylor JR, Elsworth JD, Redmond Jr. DE, et al. (1999). Altered frontal cortical dopaminergic transmission in monkeys after subchronic phencyclidine exposure: involvement in frontostriatal cognitive deficits. Neuroscience 90, 823-832.
25. Jentsch JD, Tran A, Le D, Youngren KD, et al. (1997b). Subchronic phencyclidine administration reduces mesoprefrontal dopamine utilization and impairs prefrontal cortical-dependent cognition in the rat. Neuropsychopharmacology 17, 92-99.
26. Lees AJ, Smith E (1983). Cognitive deficits in the early stages of Parkinson's disease. Brain 106, 257-270.
27. Leranth C, Hajszan T, Szigeti-Buck K, Bober J, et al. (2008). Bisphenol A prevents the synaptogenic response to estradiol in hippocampus and prefrontal cortex of ovariectomized nonhuman primates. Proceedings of the National Academy of Sciences USA 105, 14187-14191.
28. Lewis D, Sesack S (1997). Dopamine systems in the primate brain. In: Bloom FE, Bjorklund A, Hokfelt T (Eds.), The Primate Nervous System (pp. 263-375). Amsterdam: Elsevier.
29. Miller EK (2000). The prefrontal cortex and cognitive control. Nature Reviews Neuroscience 1, 59-65.
30. Morrow BA, Roth RH, Redmond DE, Elsworth JD (2011). Impact of methamphetamine on dopamine neurons in primates is dependent on age: implications for development of Parkinson's disease. Neuroscience 189, 277-285.
31. Peters A, Sethares C, Luebke JI (2008). Synapses are lost during aging in the primate prefrontal cortex. Neuroscience 152, 970-981.
32. Roberts AC, DeSalvia MA, Wilkinson LS, Collins P, et al. (1994). 6-Hydroxydopamine lesions of the prefrontal cortex in monkeys enhance performance on an analogue of the Wisconsin Card Sort Test: possible interactions with subcortical dopamine. Journal of Neuroscience 14, 2531-2544.
33. Scatton B, Javoy-Agid F, Rouquier L, Dubois B, et al. (1983). Reduction of cortical dopamine, noradrenaline, serotonin and their metabolites in Parkinson's disease. Brain Research 275, 321-328.
34. Schneider JS, Kovelowski CJ (1990). Chronic exposure to low doses of MPTP: I. Cognitive deficits in motor asymptomatic monkeys. Brain Research 519, 122-128.
35. Schultz W (2002). Getting formal with dopamine and reward. Neuron 36, 241-263.
36. Smiley JF, Williams SM, Szigeti K, Goldman-Rakic PS (1992). Light and electron microscopic characterization of dopamine-immunoreactive axons in human cerebral cortex. Journal of Comparative Neurology 321, 325-335.
37. Stam CJ, de Bruin JP, van Haelst AM, van der Gugten J, et al. (1989). Influence of the mesocortical dopaminergic system on activity, food hoarding, social-agonistic behavior, and spatial delayed alternation in male rats. Behavioral Neuroscience 103, 24-35.
38. Stern Y, Tetrud JW, Martin WR, Kutner SJ, et al. (1990). Cognitive change following MPTP exposure. Neurology 40, 261-264.
39. Taylor JR, Elsworth JD, Roth RH, Sladek Jr. JR, et al. (1990). Cognitive and motor deficits in the acquisition of an object retrieval/detour task in MPTP-treated monkeys. Brain 113, 617-637.
40. Taylor JR, Elsworth JD, Roth RH, Sladek Jr. JR, et al. (1994). Behavioral effects of MPTP administration in the Vervet monkey: a primate model of Parkinson's disease. In: Woodruff ML, Nonneman AJ (Eds.), Toxin-Induced Models of Neurological Disorders (pp. 139-174). New York: Plenum Press.
41. Taylor JR, Elsworth JD, Roth RH, Sladek Jr. JR, et al. (1997). Severe long-term 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-induced Parkinsonism in the Vervet monkey (Cercopithecus aethiops sabaeus). Neuroscience 81, 745-755.
42. Tseng KY, O'Donnell P (2004). Dopamine-glutamate interactions controlling prefrontal cortical pyramidal cell excitability involve multiple signaling mechanisms. Journal of Neuroscience 24, 5131-5139.
43. Venator DK, Lewis DA, Finlay JM (1999). Effects of partial dopamine loss in the medial prefrontal cortex on local baseline and stress-evoked extracellular dopamine concentrations. Neuroscience 93, 497-505.
44. Volk DW, Lewis DA (2010). Prefrontal cortical circuits in schizophrenia. Current Topics in Behavioral Neuroscience 4, 485-508.
45. Wang HD, Deutch AY (2008). Dopamine depletion of the prefrontal cortex induces dendritic spine loss: reversal by atypical antipsychotic drug treatment. Neuropsychopharmacology 33, 1276-1286.
46. Williams SM, Goldman-Rakic PS (1998). Widespread origin of the primate mesofrontal dopamine system. Cerebral Cortex 8, 321-345.
47. Zigmond MJ, Berger TW, Grace AA, Stricker EM (1989). Compensatory responses to nigrostriatal bundle injury. Studies with 6-hydroxydopamine in an animal model of Parkinsonism. Molecular and Chemical Neuropathology 10, 185-200.