Activation of dopaminergic D2/D3 receptors modulates dorsoventral connectivity in the hippocampus and reverses the impairment of working memory after nerve injury

Journal of Neuroscience

Volumn 34, Issue 17, 2014, Pages 5861-5873

  Cardoso Cruz, Helder ^a,b   Dourado, Margarida ^a,b   Monteiro, Clara ^a,b   Matos, Mariana R ^a,b   Galhardo, Vasco ^a,b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

Author keywords

Awake animal physiology; Dopamine; Hippocampus; Neuropathy; Pain; Working memory

Indexed keywords

DOPAMINE 2 RECEPTOR; DOPAMINE 3 RECEPTOR; MESSENGER RNA; QUINPIROLE;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN ELECTROPHYSIOLOGY; CHRONIC PAIN; COGNITIVE DEFECT; CONNECTOME; CONTROLLED STUDY; DORSAL ROOT; ELECTRODE IMPLANT; GENE EXPRESSION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; INFRARED SPECTROSCOPY; MALE; MAZE TEST; MEASUREMENT ERROR; NERVE CELL PLASTICITY; NERVE INJURY; NERVE LESION; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPIKE WAVE; TASK PERFORMANCE; VENTRAL ROOT; WORKING MEMORY;

AWAKE ANIMAL PHYSIOLOGY; DOPAMINE; HIPPOCAMPUS; NEUROPATHY; PAIN; WORKING MEMORY;

ANIMALS; BEHAVIOR, ANIMAL; DOPAMINE AGONISTS; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY DISORDERS; MEMORY, SHORT-TERM; NERVE NET; NEURALGIA; PERIPHERAL NERVE INJURIES; QUINPIROLE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE D2; RECEPTORS, DOPAMINE D3; SPATIAL BEHAVIOR;

EID: 84899483174     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0021-14.2014     Document Type: Article

References (76)

1. Aguiar P, Mendonça L, Galhardo V (2007) OpenControl: a free opensource software for video tracking and automated control of behavioral mazes. J Neurosci Methods 166:66-72. CrossRef Medline
2. Altier N, Stewart J (1999) The role of dopamine in the nucleus accumbens in analgesia. Life Sci 65:2269-2287. CrossRef Medline
3. Amano T, Wada E, Yamada D, Zushida K, Maeno H, Noda M, Wada K, Sekiguchi M (2008) Heightened amygdala long-term potentiation in neurotensin receptor type-1 knockout mice. Neuropsychopharmacology 33:3135-3145. CrossRef Medline
4. Arnsten AF, Cai JX, Steere JC, Goldman-Rakic PS (1995) Dopamine D2 receptor mechanisms contribute to age-related cognitive decline: the effects of quinpirole on memory and motor performance in monkeys. J Neurosci 15:3429-3439. Medline
5. Baccalá LA, Sameshima K (2001) Partial directed coherence: a new concept in neural structure determination. Biol Cybern 84:463-474. CrossRef Medline
6. Bannerman DM, Yee BK, Good MA, Heupel MJ, Iversen SD, Rawlins JN (1999) Double dissociation of function within the hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behav Neurosci 113:1170-1188. CrossRef Medline
7. Baudonnat M, Huber A, David V, Walton ME (2013) Heads for learning, tails for memory: reward, reinforcement and a role of dopamine in determining behavioral relevance across multiple timescales. Front Neurosci 7:175. CrossRef Medline
8. Berens P (2009) CircStat: a MATLAB toolbox for circular statistics. Journal of Statistical Software 31:1.
9. Bruinink A, Bischoff S (1993) Dopamine D2 receptors are unevenly distributed in the rat hippocampus and are modulated differently than in striatum. Eur J Pharmacol 245:157-164. CrossRef Medline
10. Cai JX, Arnsten AF (1997) Dose-dependent effects of the dopamine D1 receptor agonists A77636 or SKF81297 on spatial working memory in aged monkeys. J Pharmacol Exp Ther 283:183-189. Medline
11. Calabresi P, Saiardi A, Pisani A, Baik JH, Centonze D, Mercuri NB, Bernardi G, Borrelli E (1997) Abnormal synaptic plasticity in the striatum of mice lacking dopamine D2 receptors. J Neurosci 17:4536-4544. Medline
12. Cardoso-Cruz H, Lima D, Galhardo V (2011a) Instability of spatial encoding by CA1 hippocampal place cells after peripheral nerve injury. Eur J Neurosci 33:2255-2264. CrossRef Medline
13. Cardoso-Cruz H, Sameshima K, Lima D, Galhardo V (2011b) Dynamics of circadian thalamocortical flow of information during a peripheral neuropathic pain condition. Front Integr Neurosci 5:43. CrossRef Medline
14. Cardoso-Cruz H, Lima D, Galhardo V (2013a) Impaired spatial memory performance in a rat model of neuropathic pain is associated with reduced hippocampus-prefrontal cortex connectivity. J Neurosci 33:2465-2480. CrossRef Medline
15. Cardoso-Cruz H, Sousa M, Vieira JB, Lima D, Galhardo V (2013b) Prefrontal cortex and mediodorsal thalamus reduced connectivity is associated with spatial working memory impairment in rats with inflammatory pain. Pain 154:2397-2406. CrossRef Medline
16. Castner SA, Williams GV, Goldman-Rakic PS (2000) Reversal of antipsychoticinduced working memory deficits by short-term dopamine D1 receptor stimulation. Science 287:2020-2022. CrossRef Medline
17. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63. CrossRef Medline
18. Coffeen U, Ortega-Legaspi JM, de Gortari P, Simón-Arceo K, Jaimes O, Amaya MI, Pellicer F (2010) Inflammatory nociception diminishes dopamine release and increases dopamine D2 receptor mRNA in the rat's insular cortex. Mol Pain 6:75. CrossRef Medline
19. Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI (2009) Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462:353-357. CrossRef Medline
20. Decosterd I, Woolf CJ (2000) Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87:149-158. CrossRef Medline
21. Dong HW, Swanson LW, Chen L, Fanselow MS, Toga AW (2009) Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc Natl Acad Sci U S A 106:11794-11799. CrossRef Medline
22. Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7-19. CrossRef Medline
23. Fisher NI (1993) Statistical analysis of circular data: Cambridge UP.
24. Frey U, Hartmann S, Matthies H (1989) Domperidone, an inhibitor of the D2-receptor, blocks a late phase of an electrically induced long-term potentiation in the CA1-region in rats. Biomed Biochim Acta 48:473-476. Medline
25. Frey U, Schroeder H, MatthiesH (1990) Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the CA1 region of rat hippocampal slices. Brain Res 522:69-75. CrossRef Medline
26. Frey U, Matthies H, Reymann KG, MatthiesH (1991) The effect of dopaminergic D1 receptor blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro. Neurosci Lett 129: 111-114. CrossRef Medline
27. Fujishiro H, Umegaki H, Suzuki Y, Oohara-Kurotani S, Yamaguchi Y, Iguchi A (2005) Dopamine D2 receptor plays a role in memory function: implications of dopamine-acetylcholine interaction in the ventral hippocampus. Psychopharmacology (Berl) 182:253-261. CrossRef
28. Gasbarri A, Introini-Collison IB, Packard MG, Pacitti C, McGaugh JL (1993) Interaction of cholinergic-dopaminergic systems in the regulation of memory storage in aversively motivated learning tasks. Brain Res 627:72-78. CrossRef Medline
29. Gasbarri A, Verney C, Innocenzi R, Campana E, Pacitti C (1994) Mesolimbic dopaminergic neurons innervating the hippocampal formation in the rat: a combined retrograde tracing and immunohistochemical study. Brain Res 668:71-79. CrossRef Medline
30. Gasbarri A, Sulli A, Innocenzi R, Pacitti C, Brioni JD (1996) Spatial memory impairment induced by lesion of the mesohippocampal dopaminergic system in the rat. Neuroscience 74:1037-1044. CrossRef Medline
31. Gasbarri A, Sulli A, Packard MG (1997) The dopaminergic mesencephalic projections to the hippocampal formation in the rat. Prog Neuropsychopharmacol Biol Psychiatry 21:1-22. CrossRef Medline
32. Ghanbarian E, Motamedi F (2013) Ventral tegmental area inactivation suppresses the expression of CA1 long term potentiation in anesthetized rat. PLoS ONE 8:e58844. CrossRef Medline
33. Granado N, Ortiz O, Suárez LM, Martin ED, Ceña V, Solís JM, Moratalla R (2008) D1 but not D5 dopamine receptors are critical for LTP, spatial learning, and LTP-Induced arc and zif268 expression in the hippocampus. Cereb Cortex 18:1-12. CrossRef Medline
34. Greengard P, Allen PB, Nairn AC (1999) Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade. Neuron 23:435-447. CrossRef Medline
35. Horvitz JC, Williams G, Joy R (2001) Time-dependent actions of D2 family agonist quinpirole on spontaneous behavior in the rat: dissociation between sniffing and locomotion. Psychopharmacology (Berl) 154:350-355. CrossRef Medline
36. Huang JJ, Yen CT, Liu TL, Tsao HW, Hsu JW, Tsai ML (2013) Effects of dopamine D2 agonist quinpirole on neuronal activity of anterior cingulate cortex and striatum in rats. Psychopharmacology (Berl) 227:459-466. CrossRef Medline
37. Jones MW, Wilson MA (2005) Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm. Hippocampus 15: 867-873. CrossRef Medline
38. Kjelstrup KG, Tuvnes FA, Steffenach HA, Murison R, Moser EI, Moser MB (2002) Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci U S A 99:10825-10830. CrossRef Medline
39. Lisman J, Grace AA, Duzel E (2011) A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP. Trends Neurosci 34: 536-547. CrossRef Medline
40. Luo AH, Tahsili-Fahadan P, Wise RA, Lupica CR, Aston-Jones G (2011) Linking context with reward: a functional circuit from hippocampal CA3 to ventral tegmental area. Science 333:353-357. CrossRef Medline
41. Manahan-Vaughan D, Kulla A (2003) Regulation of depotentiation and long-term potentiation in the dentate gyrus of freely moving rats by dopamine D2-like receptors. Cereb Cortex 13:123-135. CrossRef Medline
42. Martig AK, Mizumori SJ (2011) Ventral tegmental area disruption selectively affects CA1/CA2 but not CA3 place fields during a differential reward working memory task. Hippocampus 21:172-184. CrossRef Medline
43. Meador-Woodruff JH, Mansour A, Healy DJ, Kuehn R, Zhou QY, Bunzow JR, Akil H, Civelli O, Watson SJ Jr (1991) Comparison of the distributions of D1 and D2 dopamine receptor mRNAs in rat brain. Neuropsychopharmacology 5:231-242. Medline
44. Moriarty O, McGuire BE, Finn DP (2011) The effect of pain on cognitive function: a review of clinical and preclinical research. Prog Neurobiol 93:385-404. CrossRef Medline
45. Moser MB, Moser EI (1998) Functional differentiation in the hippocampus. Hippocampus 8:608-619. CrossRef Medline
46. Neve KA, Seamans JK, Trantham-Davidson H (2004) Dopamine receptor signaling. J Recept Signal Transduct Res 24:165-205. CrossRef Medline
47. O'Carroll CM, Martin SJ, Sandin J, Frenguelli B, Morris RG (2006) Dopaminergic modulation of the persistence of one-trial hippocampusdependent memory. Learn Mem 13:760-769. CrossRef Medline
48. Onton J, Delorme A, Makeig S (2005) Frontal midline EEG dynamics during working memory. Neuroimage 27:341-356. CrossRef Medline
49. Packard MG, White NM (1991) Dissociation of hippocampus and caudate nucleus memory systems by posttraining intracerebral injection of dopamine agonists. Behav Neurosci 105:295-306. CrossRef Medline
50. Pais-Vieira M, Mendes-Pinto MM, Lima D, Galhardo V (2009) Cognitive impairment of prefrontal-dependent decision-making in rats after the onset of chronic pain. Neuroscience 161:671-679. CrossRef Medline
51. Pais-Vieira M, Aguiar P, Lima D, Galhardo V (2012) Inflammatory pain disrupts the orbitofrontal neuronal activity and risk-assessment performance in a rodent decision-making task. Pain 153:1625-1635. CrossRef Medline
52. Patel J, Fujisawa S, Berényi A, Royer S, Buzsáki G (2012) Traveling theta waves along the entire septotemporal axis of the hippocampus. Neuron 75:410-417. CrossRef Medline
53. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. San Diego: Academic.
54. Penley SC, Hinman JR, Long LL, Markus EJ, Escabí MA, Chrobak JJ (2013) Novel space alters theta and gamma synchrony across the longitudinal axis of the hippocampus. Front Syst Neurosci 7:20. CrossRef Medline
55. Pennartz CM, Ito R, Verschure PF, Battaglia FP, Robbins TW (2011) The hippocampal-striatal axis in learning, prediction and goal-directed behavior. Trends Neurosci 34:548-559. CrossRef Medline
56. Rainer G, Miller EK (2000) Effects of visual experience on the representation of objects in the prefrontal cortex. Neuron 27:179-189. CrossRef Medline
57. Royer S, Sirota A, Patel J, Buzsáki G (2010) Distinct representations and theta dynamics in dorsal and ventral hippocampus. J Neurosci 30:1777-1787. CrossRef Medline
58. Saadé NE, Atweh SF, Bahuth NB, Jabbur SJ (1997) Augmentation of nociceptive reflexes and chronic deafferentation pain by chemical lesions of either dopaminergic terminals or midbrain dopaminergic neurons. Brain Res 751:1-12. CrossRef Medline
59. Sabolek HR, Penley SC, Hinman JR, Bunce JG, Markus EJ, Escabi M, Chrobak JJ (2009) Theta and gamma coherence along the septotemporal axis of the hippocampus. J Neurophysiol 101:1192-1200. CrossRef Medline
60. Sameshima K, Baccalá LA (1999) Using partial directed coherence to describe neuronal ensemble interactions. J Neurosci Methods 94:93-103. CrossRef Medline
61. Sarkis D, Souteyrand JP, Albe-Fessard D (1984) Self-stimulation in the ventral tegmental area suppresses self-mutilation in rats with forelimb deafferentiation. Neurosci Lett 44:199-204. CrossRef Medline
62. Schmidt B, Hinman JR, Jacobson TK, Szkudlarek E, Argraves M, Escabí MA, Markus EJ (2013) Dissociation between dorsal and ventral hippocampal theta oscillations during decision-making. J Neurosci 33:6212-6224. CrossRef Medline
63. Sotres-Bayón F, Torres-López E, López-Avila A, del Angel R, Pellicer F (2001) Lesion and electrical stimulation of the ventral tegmental area modify persistent nociceptive behavior in the rat. Brain Res 898:342-349. CrossRef Medline
64. Swanson LW, CowanWM (1977) An autoradiographic study of the organi zation of the efferent connections of the hippocampal formation in the rat. J Comp Neurol 172:49-84. CrossRef Medline
65. Takahashi H, Kato M, Takano H, Arakawa R, Okumura M, Otsuka T, Kodaka F, Hayashi M, Okubo Y, Ito H, Suhara T (2008) Differential contributions of prefrontal and hippocampal dopamine D(1) and D(2) receptors in human cognitive functions. J Neurosci 28:12032-12038. CrossRef Medline
66. Tesche CD, Karhu J (2000) Theta oscillations index human hippocampal activation during a working memory task. Proc Natl Acad Sci U S A 97: 919-924. CrossRef Medline
67. Thompson CL, Pathak SD, Jeromin A, Ng LL, MacPherson CR, Mortrud MT, Cusick A, Riley ZL, Sunkin SM, Bernard A, Puchalski RB, Gage FH, Jones AR, Bajic VB, Hawrylycz MJ, Lein ES (2008) Genomic anatomy of the hippocampus. Neuron 60:1010-1021. CrossRef Medline
68. Verney C, Baulac M, Berger B, Alvarez C, Vigny A, Helle KB (1985) Morphological evidence for a dopaminergic terminal field in the hippocampal formation of young and adult rat. Neuroscience 14:1039-1052. CrossRef Medline
69. Weiner DM, Levey AI, Sunahara RK, Niznik HB, O'Dowd BF, Seeman P, Brann MR (1991) D1 and D2 dopamine receptor mRNA in rat brain. Proc Natl Acad Sci U S A 88:1859-1863. CrossRef Medline
70. Wilkerson A, Levin ED (1999) Ventral hippocampal dopamine D1 and D2 systems and spatial working memory in rats. Neuroscience 89:743-749. CrossRef Medline
71. Witter MP, Amaral DG (2004) Hippocampal formation. In: The rat nervous system, Ed 3 (Paxinos G, ed), pp 635-704. London: Elsevier.
72. Wood PB (2006) Mesolimbic dopaminergic mechanisms and pain control. Pain 120:230-234. CrossRef Medline
73. Wood PB, Patterson JC 2nd, Sunderland JJ, Tainter KH, Glabus MF, Lilien DL (2007a) Reduced presynaptic dopamine activity in fibromyalgia syndrome demonstrated with positron emission tomography: a pilot study. J Pain 8:51-58. CrossRef Medline
74. Wood PB, Schweinhardt P, Jaeger E, Dagher A, Hakyemez H, Rabiner EA, Bushnell MC, Chizh BA (2007b) Fibromyalgia patients show an abnormal dopamine response to pain. Eur J Neurosci 25:3576-3582. CrossRef Medline
75. Wood PB, Glabus MF, Simpson R, Patterson JC 2nd (2009) Changes in gray matter density in fibromyalgia: correlation with dopamine metabolism. J Pain 10:609-618. CrossRef Medline
76. ZimmermannM (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16:109-110. CrossRef Medline