Altered dendritic distribution of dopamine D2 receptors and reduction in mitochondrial number in parvalbumin-containing interneurons in the medial prefrontal cortex of cannabinoid-1 (CB1) receptor knockout mice

Journal of Comparative Neurology

Volumn 520, Issue 17, 2012, Pages 4013-4031

  Fitzgerald, Megan L ^a   Chan, June ^a   Mackie, Kenneth ^b   Lupica, Carl R ^c   Pickel, Virginia M ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b INDIANA UNIVERSITY   (United States)

^c NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

Antipsychotic; Electron microscopy; Fast firing; Marijuana; Prelimbic; Trafficking

Indexed keywords

CANNABINOID 1 RECEPTOR; DOPAMINE 2 RECEPTOR; PARVALBUMIN;

ANIMAL TISSUE; ANTIBODY LABELING; ANTIBODY SPECIFICITY; ARTICLE; BRAIN MAPPING; BRAIN MITOCHONDRION; CONTROLLED STUDY; DENDRITE; IMMUNOELECTRON MICROSCOPY; IMMUNOREACTIVITY; INTERNEURON; MALE; MOUSE; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTOGENESIS;

ANIMALS; DENDRITES; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; PARVALBUMINS; PREFRONTAL CORTEX; RECEPTOR, CANNABINOID, CB1; RECEPTORS, DOPAMINE D2;

EID: 84867132216     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23141     Document Type: Article

References (60)

1. Alcántara S, Ferrer I, Soriano E. 1993. Postnatal development of parvalbumin and calbindin D28K immunoreactivities in the cerebral cortex of the rat. Anat Embryol 188: 63-73.
2. Amat J, Baratta MV, Paul E, Bland ST, Watkins LR, Maier SF. 2005. Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 8: 365-371.
3. Bartlett SE, Enquist J, Hopf FW, Lee JH, Gladher F, Kharazia V, Waldhoer M, Mailliard WS, Armstrong R, Bonci A, Whistler JL. 2005. Dopamine responsiveness is regulated by targeted sorting of D2 receptors. Proc Natl Acad Sci USA 102: 11521-11526.
4. Billups B, Forsythe ID. 2002. Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses. J Neurosci 22: 5840-5847.
5. Bodor AL, Katona I, Nyíri G, Mackie K, Ledent C, Hájos N, Freund TF. 2005. Endocannabinoid signaling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types. J Neurosci 25: 6845-6856.
6. Brana C, Aubert I, Charron G, Pellevoisin C, Bloch B. 1997. Ontogeny of the striatal neurons expressing the D2 dopamine receptor in humans: an in situ hybridization and receptor-binding study. Brain Res Mol Brain Res 48: 389-400.
7. Celio MR, Heizmann CW. 1981. Calcium-binding protein parvalbumin as a neuronal marker. Nature 293: 300-302.
8. Cellerino A, Siciliano R, Domenici L, Maffei L. 1992. Parvalbumin immunoreactivity: a reliable marker for the effects of monocular deprivation in the rat visual cortex. Neuroscience 51: 749-753.
9. Chan J, Aoki C, Pickel VM. 1990. Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. J Neurosci Methods 33: 113-127.
10. Chang DTW, Honick AS, Reynolds IJ. 2006. Mitochondrial trafficking to synapses in cultured primary cortical neurons. J Neurosci 26: 7035-7045.
11. Chard PS, Bleakman D, Christakos S, Fullmer CS, Miller RJ. 1993. Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones. J Physiol 472: 341-357.
12. Chattopadhyaya B, Di Cristo G, Wu CZ, Knott G, Kuhlman S, Fu Y, Palmiter RD, Huang ZJ. 2007. GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron 54: 889-903.
13. Chen J, Paredes W, Lowinson JH, Gardner EL. 1990. Delta 9-tetrahydrocannabinol enhances presynaptic dopamine efflux in medial prefrontal cortex. Eur J Pharmacol 190: 259-262.
14. Chiu CQ, Puente N, Grandes P, Castillo PE. 2010. Dopaminergic modulation of endocannabinoid-mediated plasticity at GABAergic synapses in the prefrontal cortex. J Neurosci 30: 7236-7248.
15. Dal Toso R, Sommer B, Ewert M, Herb A, Pritchett DB, Bach A, Shivers BD, Seeburg PH. 1989. The dopamine D2 receptor: two molecular forms generated by alternative splicing. EMBO J 8: 4025-4034.
16. Dalley JW, Cardinal RN, Robbins TW. 2004. Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci Biobehav Rev 28: 771-784.
17. Fitzgerald ML, Lupica CR, Pickel VM. 2011. Decreased parvalbumin immunoreactivity in the cortex and striatum of mice lacking the CB1 receptor. Synapse 65: 827-831.
18. French ED. 1997. delta9-Tetrahydrocannabinol excites rat VTA dopamine neurons through activation of cannabinoid CB1 but not opioid receptors. Neurosci Lett 226: 159-162.
19. Fung SJ, Webster MJ, Sivagnanasundaram S, Duncan C, Elashoff M, Weickert CS. 2010. Expression of interneuron markers in the dorsolateral prefrontal cortex of the developing human and in schizophrenia. Am J Psychiatry 167: 1479-1488.
20. Giros B, Sokoloff P, Martres MP, Riou JF, Emorine LJ, Schwartz JC. 1989. Alternative splicing directs the expression of two D2 dopamine receptor isoforms. Nature 342: 923-926.
21. Heng L, Beverley JA, Steiner H, Tseng KY. 2011. Differential developmental trajectories for CB1 cannabinoid receptor expression in limbic/associative and sensorimotor cortical areas. Synapse 65: 278-286.
22. Hill EL, Gallopin T, Ferezou I, Cauli B, Rossier J, Schweitzer P, Lambolez B. 2007. Functional CB1 receptors are broadly expressed in neocortical GABAergic and glutamatergic neurons. J Neurophysiol 97: 2580-2589.
23. Hill MN, McLughlin RJ, Pan B, Fitzgerald ML, Roberts CJ, Lee T, Karatsoreos IN, Mackie K, Viau V, Pickel VM, McEwen BS, Liu Q, Gorzalka BB, Hillard CJ. 2011. Recruitment of prefrontal cortical endocannabinoid signaling by glucocorticoids contributes to termination of the stress response. J Neurosci 31: 10506-10515.
24. Karson MA, Tang A-H, Milner TA, Alger BE. 2009. Synaptic cross talk between perisomatic-targeting interneuron classes expressing cholecystokinin and parvalbumin in hippocampus. J Neurosci 29: 4140-4154.
25. Katona I, Sperlagh B, Sik A, Kafalvi A, Vizi E, Mackie K, Freund T. 1999. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19: 4544-4558.
26. Katona I, Urbán GM, Wallace M, Ledent C, Jung KM, Piomelli D, Mackie K, Freund TF. 2006. Molecular composition of the endocannabinoid system at glutamatergic synapses. J Neurosci 26: 5628-5637.
27. Kearn C, Blake-Palmer K, Daniel E, Mackie K, Glass M. 2005. Concurrent stimulation of cannabinoid CB1 and dopamine D2 receptors enhances heterodimer formation: a mechanism for receptor cross-talk? Mol Pharmacol 67: 1697-1704.
28. Keating DJ. 2008. Mitochondrial dysfunction, oxidative stress, regulation of exocytosis and their relevance to neurodegenerative diseases. J Neurochem 104: 298-305.
29. Kita H, Kosaka T, Heizmann CW. 1990. Parvalbumin-immunoreactive neurons in the rat neostriatum: a light and electron microscopic study. Brain Res 36: 1-15.
30. Lafourcade M, Elezgarai I, Mato S, Bakiri Y, Grandes P, Manzoni OJ. 2007. Molecular components and functions of the endocannabinoid system in mouse prefrontal cortex. PLoS ONE 2: e709.
31. Lane DA, Chan J, Fitzgerald ML, Kearn CS, Mackie K, Pickel VM. 2012. Quinpirole elicits differential in vivo changes in the pre- and postsynaptic distributions of dopamine D2 receptors in mouse striatum: relation to cannabinoid-1 (CB1) receptor targeting. Mol Psychopharmacol [Epub ahead of print].
32. Le Moine C, Gaspar P. 1998. Subpopulations of cortical GABAergic interneurons differ by their expression of D1 and D2 dopamine receptor subtypes. Mol Brain Res 58: 231-236.
33. Li Z, Okamoto K-I, Hayashi Y, Sheng M. 2004. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119: 873-887.
34. Li X, Hoffman AF, Peng X-Q, Lupica CR, Gardner EL, Xi Z-X. 2009. Attenuation of basal and cocaine-enhanced locomotion and nucleus accumbens dopamine in cannabinoid CB1-receptor-knockout mice. Psychopharmacology 204: 1-11.
35. Lupica CR, Riegel AC, Hoffman AF. 2004. Marijuana and cannabinoid regulation of brain reward circuits. Br J Pharmacol 143: 227-234.
36. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. 2004. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5: 793-807.
37. Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, Cannich A, Azad SC, Cascio MG, Gutiérrez SO, van der Stelt M, López-Rodriguez ML, Casanova E, Schütz G, Zieglgänsberger W, Di Marzo V, Behl C, Lutz B. 2003. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302: 84-88.
38. Mátyás F, Urbán GM, Watanabe M, Mackie K, Zimmer A, Freund TF, Katona I. 2008. Identification of the sites of 2-arachidonoylglycerol synthesis and action imply retrograde endocannabinoid signaling at both GABAergic and glutamatergic synapses in the ventral tegmental area. Neuropharmacology 54: 95-107.
39. Miller EK, Cohen JD. 2001. An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24: 167-202.
40. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG. 1998. Dopamine receptors: from structure to function. Physiol Rev 78: 189-225.
41. Paxinos G, Franklin KBJ. 2001. The mouse brain in stereotaxic coordinates. San Diego, CA: Academic Press.
42. Peters A, Palay SL, Webster HD. 1991. The fine structure of the nervous system. New York: Oxford University Press.
43. Pickel VM, Chan J, Kearn CS, Mackie K. 2006. Targeting dopamine D2 and cannabinoid-1 (CB1) receptors in rat nucleus accumbens. J Comp Neurol 495: 299-313.
44. Porter LL, Rizzo E, Hornung JP. 1999. Dopamine affects parvalbumin expression during cortical development in vitro. J Neurosci 19: 8990-9003.
45. Prabakaran S, Swatton JE, Ryan MM, Huffaker SJ, Huang JT-J, Griffin JL, Wayland M, Freeman T, Dudbridge F, Lilley KS, Karp NA, Hester S, Tkachev D, Mimmack ML, Yolken RH, Webster MJ, Torrey EF, Bahn S. 2004. Mitochondrial dysfunction in schizophrenia: evidence for compromised brain metabolism and oxidative stress. Mol Psychiatry 9: 684-697, 643.
46. Santana N, Mengod G, Artigas F. 2009. Quantitative analysis of the expression of dopamine D1 and D2 receptors in pyramidal and GABAergic neurons of the rat prefrontal cortex. Cereb Cortex 19: 849-860.
47. Schambra B, Duncan G, Breese G, Fornaretto M, Caron M, Fremeau R. 1994. Ontogeny of D-1A and D-2 dopamine-receptor subtypes in rat brain using in-situ hybridization and receptor-binding. Neuroscience 62: 65-85.
48. Schmidt H, Arendt O, Brown EB, Schwaller B, Eilers J. 2007. Parvalbumin is freely mobile in axons, somata and nuclei of cerebellar Purkinje neurones. J Neurochem 100: 727-735.
49. Sesack SR, Hawrylak VA, Melchitzky DS, Lewis DA. 1998. Dopamine innervation of a subclass of local circuit neurons in monkey prefrontal cortex: ultrastructural analysis of tyrosine hydroxylase and parvalbumin immunoreactive structures. Cereb Cortex 8: 614-622.
50. Soria G, Mendizábal V, Touriño C, Robledo P, Ledent C, Parmentier M, Maldonado R, Valverde O. 2005. Lack of CB1 cannabinoid receptor impairs cocaine self-administration. Neuropsychopharmacology 30: 1670-1680.
51. Spencer KM, Nestor PG, Niznikiewicz MA, Salisbury DF, Shenton ME, McCarley RW. 2003. Abnormal neural synchrony in schizophrenia. J Neurosci 23: 7407-7411.
52. Tseng KY, O'Donnell P. 2004. Dopamine-glutamate interactions controlling prefrontal cortical pyramidal cell excitability involve multiple signaling mechanisms. J Neurosci 24: 5131-5139.
53. Tseng K-Y, O'Donnell P. 2007. Dopamine modulation of prefrontal cortical interneurons changes during adolescence. Cereb Cortex 17: 1235-1240.
54. Ulrich-Lai YM, Herman JP. 2009. Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 10: 397-409.
55. Usiello A, Baik JH, Rougé-Pont F, Picetti R, Dierich A, LeMeur M, Piazza PV, Borrelli E. 2000. Distinct functions of the two isoforms of dopamine D2 receptors. Nature 408: 199-203.
56. Wang Y, Goldman-Rakic PS. 2004. D2 receptor regulation of synaptic burst firing in prefrontal cortical pyramidal neurons. Proc Natl Acad Sci U S A 101: 5093-5098.
57. Wang H, Pickel VM. 2002. Dopamine D2 receptors are present in prefrontal cortical afferents and their targets in patches of the rat caudate-putamen nucleus. J Comp Neurol 442: 392-404.
58. Wang X, Schwarz TL. 2009. The mechanism of Ca2+ -dependent regulation of kinesin-mediated mitochondrial motility. Cell 136: 163-174.
59. Zaitsev AV, Gonzalez-Burgos G, Povysheva NV, Kroner S, Lewis DA, Krimer LS. 2005. Localization of calcium-binding proteins in physiologically and morphologically characterized interneurons of monkey dorsolateral prefrontal cortex. Cereb Cortex 15: 1178-1186.
60. Zimmer A, Zimmer AM, Hohmann AG, Herkenham M, Bonner TI. 1999. Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc Natl Acad Sci U S A 96: 5780-5785.