Hippocampal CA1/subiculum-prefrontal cortical pathways induce plastic changes of nociceptive responses in cingulate and prelimbic areas

BMC Neuroscience

Volumn 11, Issue , 2010, Pages

  Nakamura, Hiroyuki ^a   Katayama, Yoko ^a   Kawakami, Yoriko ^a  

^a TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN FOS;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN ELECTROPHYSIOLOGY; BRAIN NERVE CELL; CELLULAR DISTRIBUTION; CINGULATE GYRUS; CONTROLLED STUDY; EVOKED CORTICAL RESPONSE; HIPPOCAMPUS; LIMBIC CORTEX; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NOCICEPTION; NONHUMAN; PREFRONTAL CORTEX; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; SUBICULUM; AFFECT; ANIMAL; EXTRACELLULAR SPACE; HIPPOCAMPAL CA1 REGION; LIMBIC SYSTEM; MEMORY; NERVE TRACT; PAIN; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGICAL ASPECT; STIMULATION; WISTAR RAT;

AFFECT; ANIMALS; CA1 REGION, HIPPOCAMPAL; EXTRACELLULAR SPACE; GYRUS CINGULI; HIPPOCAMPUS; LIMBIC SYSTEM; MALE; MEMORY; NEURAL PATHWAYS; NEURONAL PLASTICITY; PAIN; PHYSICAL STIMULATION; PREFRONTAL CORTEX; RATS; RATS, WISTAR;

EID: 77955524050     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-11-100     Document Type: Article

References (40)

1. Rainville P, Duncan G, Price D, Carrier B, Bushnell M. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 1997, 277(5328):968-971. 10.1126/science.277.5328.968, 9252330.
2. Sawamoto N, Honda M, Okada T, Hanakawa T, Kanda M, Fukuyama H, Konishi J, Shibasaki H. Expectation of pain enhances responses to nonpainful somatosensory stimulation in the anterior cingulate cortex and parietal operculum/posterior insula: an event-related functional magnetic resonance imaging study. J Neurosci 2000, 20(19):7438-7445.
3. Singer T, Seymour B, O'Doherty J, Kaube H, Dolan R, Frith C. Empathy for pain involves the affective but not sensory components of pain. Science 2004, 303(5661):1157-1162. 10.1126/science.1093535, 14976305.
4. Gao Y, Ren W, Zhang Y, Zhao Z. Contributions of the anterior cingulate cortex and amygdala to pain- and fear-conditioned place avoidance in rats. Pain 2004, 110(1-2):343-353. 10.1016/j.pain.2004.04.030, 15275785.
5. Vogt BAVL. Anterior cingulate cortex and the medial pain system. Neurobiology of cingulated cortex and limbic thalamus 1993, 313-344. Boston: Birkhauser, Vogt BA, Gabriel M.
6. Jung M, Baeg E, Kim M, Kim Y, Kim J. Plasticity and memory in the prefrontal cortex. Rev Neurosci 2008, 19(1):29-46.
7. Hirsch J, Crepel F. Use-dependent changes in synaptic efficacy in rat prefrontal neurons in vitro. J Physiol 1990, 427:31-49. 1189918, 2213602.
8. Jay T, Burette F, Laroche S. NMDA receptor-dependent long-term potentiation in the hippocampal afferent fiber system to the prefrontal cortex in the rat. Eur J Neurosci 1995, 7(2):247-250. 10.1111/j.1460-9568.1995.tb01060.x, 7757261.
9. Wei F, Xu Z, Qu Z, Milbrandt J, Zhuo M. Role of EGR1 in hippocampal synaptic enhancement induced by tetanic stimulation and amputation. J Cell Biol 2000, 149(7):1325-1334. 10.1083/jcb.149.7.1325, 2175137, 10871275.
10. Khanna S, Sinclair J. Noxious stimuli produce prolonged changes in the CA1 region of the rat hippocampus. Pain 1989, 39(3):337-343. 10.1016/0304-3959(89)90047-X, 2616183.
11. Bingel U, Quante M, Knab R, Bromm B, Weiller C, Büchel C. Subcortical structures involved in pain processing: evidence from single-trial fMRI. Pain 2002, 99(1-2):313-321. 10.1016/S0304-3959(02)00157-4, 12237210.
12. Ploghaus A, Narain C, Beckmann C, Clare S, Bantick S, Wise R, Matthews P, Rawlins J, Tracey I. Exacerbation of pain by anxiety is associated with activity in a hippocampal network. J Neurosci 2001, 21(24):9896-9903.
13. Swanson L. A direct projection from Ammon's horn to prefrontal cortex in the rat. Brain Res 1981, 217(1):150-154. 10.1016/0006-8993(81)90192-X, 7260612.
14. Jay T, Witter M. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. J Comp Neurol 1991, 313(4):574-586. 10.1002/cne.903130404, 1783682.
15. Ferino F, Thierry A, Glowinski J. Anatomical and electrophysiological evidence for a direct projection from Ammon's horn to the medial prefrontal cortex in the rat. Exp Brain Res 1987, 65(2):421-426. 10.1007/BF00236315, 3556468.
16. Carr D, Sesack S. Hippocampal afferents to the rat prefrontal cortex: synaptic targets and relation to dopamine terminals. J Comp Neurol 1996, 369(1):1-15. 10.1002/(SICI)1096-9861(19960520)369:1<1::AID-CNE1>3.0.CO;2-7, 8723699.
17. Laroche S, Jay T, Thierry A. Long-term potentiation in the prefrontal cortex following stimulation of the hippocampal CA1/subicular region. Neurosci Lett 1990, 114(2):184-190. 10.1016/0304-3940(90)90069-L, 2395531.
18. Tierney P, Dégenètais E, Thierry A, Glowinski J, Gioanni Y. Influence of the hippocampus on interneurons of the rat prefrontal cortex. Eur J Neurosci 2004, 20(2):514-524. 10.1111/j.1460-9568.2004.03501.x, 15233760.
19. Jay T, Glowinski J, Thierry A. Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat. Brain Res 1989, 505(2):337-340. 10.1016/0006-8993(89)91464-9, 2598054.
20. Takita M, Izaki Y, Jay T, Kaneko H, Suzuki S. Induction of stable long-term depression in vivo in the hippocampal-prefrontal cortex pathway. Eur J Neurosci 1999, 11(11):4145-4148. 10.1046/j.1460-9568.1999.00870.x, 10583503.
21. Finch DM. Hippocampal, suibcular and entorhinal afferents and synaptic integration in rodent cingulate cortex. Neurobiology of cingulate cortex and limbic thalamus 1993, Boston: Birkhauser, Vogt BA, Gabriel M.
22. Thierry A, Gioanni Y, Dégénétais E, Glowinski J. Hippocampo-prefrontal cortex pathway: anatomical and electrophysiological characteristics. Hippocampus 2000, 10(4):411-419. 10.1002/1098-1063(2000)10:4<411::AID-HIPO7>3.0.CO;2-A, 10985280.
23. Wang G, Cai J. Reversible disconnection of the hippocampal-prelimbic cortical circuit impairs spatial learning but not passive avoidance learning in rats. Neurobiol Learn Mem 2008, 90(2):365-373. 10.1016/j.nlm.2008.05.009, 18614383.
24. Nagata T, Suzuki H, Zhang R, Ozaki M, Kawakami Y. Mechanical stimulation activates small fiber mediated nociceptive responses in the nucleus gigantocellularis. Exp Brain Res 2003, 149(4):505-511.
25. Jay T, Burette F, Laroche S. Plasticity of the hippocampal-prefrontal cortex synapses. J Physiol Paris 1996, 90(56):361-366. 10.1016/S0928-4257(97)87920-X, 9089514.
26. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. 1998, San Diego.: Academic Press, 4.
27. Zhang R, Tomida M, Katayama Y, Kawakami Y. Response durations encode nociceptive stimulus intensity in the rat medial prefrontal cortex. Neuroscience 2004, 125(3):777-785. 10.1016/j.neuroscience.2004.01.055, 15099691.
28. Dégenètais E, Thierry A, Glowinski J, Gioanni Y. Synaptic influence of hippocampus on pyramidal cells of the rat prefrontal cortex: an in vivo intracellular recording study. Cereb Cortex 2003, 13(7):782-792. 10.1093/cercor/13.7.782, 12816894.
29. Zhuo M. Cortical excitation and chronic pain. Trends Neurosci 2008, 31:199-207. 10.1016/j.tins.2008.01.003, 18329111.
30. Zhao MG, Toyoda H, Lee Y, Wu L, Ko S, Zhang X, Jia Y, Shum F, Xu H, Li B, et al. Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 2005, 47(6):859-872. 10.1016/j.neuron.2005.08.014, 16157280.
31. Cho K, Kemp N, Noel J, Aggleton JP, Brown MW, Bashir ZI. A new form of long-term depression in the perirhinal cortex. Nature Neuroscience 2000, 3(2):150-156. 10.1038/72093, 10649570.
32. Toyoda H, Zhao M, Zhuo M. Roles of NMDA receptor NR2A and NR2B subtypes for long-term depression in the anterior cingulate cortex. Eur J Neurosci 2005, 22(2):485-494. 10.1111/j.1460-9568.2005.04236.x, 16045501.
33. Blond O, Crépel F, Otani S. Long-term potentiation in rat prefrontal slices facilitated by phased application of dopamine. Eur J Pharmacol 2002, 438(1-2):115-116. 10.1016/S0014-2999(02)01291-8, 11906719.
34. Gonzalez-Islas C, Hablitz J. Dopamine enhances EPSCs in layer II-III pyramidal neurons in rat prefrontal cortex. J Neurosci 2003, 23(3):867-875.
35. Gao C, Wolf M. Dopamine receptors regulate NMDA receptor surface expression in prefrontal cortex neurons. J Neurochem 2008, 106(6):2489-2501. 10.1111/j.1471-4159.2008.05597.x, 2692210, 18673451.
36. Cheong M, Yun S, Mook-Jung I, Kang Y, Jung M. Induction of homosynaptic long-term depression in entorhinal cortex. Brain Res 2002, 954(2):308-310. 10.1016/S0006-8993(02)03516-3, 12414114.
37. Manahan-Vaughan D. Group 1 and 2 metabotropic glutamate receptors play differential roles in hippocampal long-term depression and long-term potentiation in freely moving rats. J Neurosci 1997, 17(9):3303-3311.
38. Izaki Y, Takita M, Akema T. Compatibility of bidirectional synaptic plasticity on hippocampo-prefrontal cortex pathway in rats. Neurosci Lett 2003, 345(1):69-71. 10.1016/S0304-3940(03)00492-0, 12809991.
39. Wei F, Zhuo M. Potentiation of sensory responses in the anterior cingulate cortex following digit amputation in the anaesthetised rat. J Physiol 2001, 532(Pt 3):823-833. 10.1111/j.1469-7793.2001.0823e.x, 2278568, 11313449.
40. Laroche S, Davis S, Jay T. Plasticity at hippocampal to prefrontal cortex synapses: dual roles in working memory and consolidation. Hippocampus 2000, 10(4):438-446. 10.1002/1098-1063(2000)10:4<438::AID-HIPO10>3.0.CO;2-3, 10985283.