The Korean Journal of Physiology and Pharmacology

The Korean Society of Pharmacology (대한약리학회)
권호 표지
DOI QR코드

DOI QR Code

The Characteristics of Supramammillary Cells Projecting to the Hippocampus in Stress Response in the Rat

  • Choi, Woong-Ki (Acupuncture & Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University) ;
  • Wirtshafter, David (Department of Psychology, The University of Illinois at Chicago) ;
  • Park, Hyun-Jung (Acupuncture & Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University) ;
  • Lee, Mi-Sook (Acupuncture & Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University) ;
  • Her, Song (Division of Bio-Imaging, Chuncheon Center, Korea Basic Science Institute) ;
  • Shim, In-Sop (Acupuncture & Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University)
  • Received : 2011.09.30
  • Accepted : 2011.12.25
  • Published : 2012.02.29
Download PDF
⟨ Previous Next ⟩

Abstract

The hypothalamus-pituitary-adrenocortex (HPA) axis is the central mediator of the stress response. The supramammillary (SuM) region is relatively unique among the hypothalamic structures in that it sends a large, direct projection to the hippocampal formation. It has been shown that mild stress could activate the SuM cells that project to the hippocampus. However, the role of these cell populations in modulating the stress response is not known. The present study examined the effect of stress on different populations of SuM cells that project to the hippocampus by injecting the fluorescent retrograde tracer, fluorogold (FG), into the hippocampus and utilizing the immunohistochemistry of choline acetyltransferase (ChAT), corticotrophin releasing factor (CRF), serotonin (5-HT), glutamate decarboxylase (GAD), tyrosine hydroxylase (TH) and NADPH-d reactivity. Immobilization (IMO) stress (2 hr) produced an increase in the expression of ChAT- immunoreactivity, and tended to increase in CRF, 5-HT, GAD, TH-immunoreactivity and nitric oxide (NO)-reactivity in the SuM cells. Fifty-three percent of 5-HT, 31% of ChAT and 56% of CRF cells were double stained with retrograde cells from the hippocampus. By contrast, a few retrogradely labeled cells projecting to the hippocampus were immunoreactive for dopamine, ${\gamma}$-aminobutyric acid (GABA) and NO. These results suggest that the SuM region contains distinct cell populations that differentially respond to stress. In addition, the findings suggest that serotonergic, cholinergic and corticotropin releasing cells projecting to the hippocampus within the SuM nucleus may play an important role in modulating stress-related behaviors.

Keywords

References

  1. Hesketh S, Jessop DS, Hogg S, Harbuz MS. Differential actions of acute and chronic citalopram on the rodent hypothalamicpituitary- adrenal axis response to acute restraint stress. J Endocrinol. 2005;185:373-382. https://doi.org/10.1677/joe.1.06074
  2. Gonzalo-Ruiz A, Morte L, Flecha JM, Sanz JM. Neurotransmitter characteristics of neurons projecting to the supramammillary nucleus of the rat. Anat Embryol (Berl). 1999;200:377-392. https://doi.org/10.1007/s004290050287
  3. Wyss JM, Swanson LW, Cowan WM. Evidence for an input to the molecular layer and the stratum granulosum of the dentate gyrus from the supramammillary region of the hypothalamus. Anat Embryol (Berl). 1979;156:165-176. https://doi.org/10.1007/BF00300012
  4. Vertes RP. PHA-L analysis of projections from the supramammillary nucleus in the rat. J Comp Neurol. 1992;326:595-622. https://doi.org/10.1002/cne.903260408
  5. Wyss JM, Swanson LW, Cowan WM. A study of subcortical afferents to the hippocampal formation in the rat. Neuroscience. 1979;4:463-476. https://doi.org/10.1016/0306-4522(79)90124-6
  6. Vertes RP, McKenna JT. Collateral projections from the supramammillary nucleus to the medial septum and hippocampus. Synapse. 2000;38:281-293. https://doi.org/10.1002/1098-2396(20001201)38:3<281::AID-SYN7>3.0.CO;2-6
  7. Zamir N, Palkovits M, Brownstein M. Distribution of immunoreactive Met-enkephalin-Arg6-Gly7-Leu8 and Leu-enkephalin in discrete regions of the rat brain. Brain Res. 1985;326:1-8. https://doi.org/10.1016/0006-8993(85)91378-2
  8. Ruggiero DA, Giuliano R, Anwar M, Stornetta R, Reis DJ. Anatomical substrates of cholinergic-autonomic regulation in the rat. J Comp Neurol. 1990;292:1-53. https://doi.org/10.1002/cne.902920102
  9. Gonzalo-Ruiz A, Alonso A, Sanz JM, Llinás RR. A dopaminergic projection to the rat mammillary nuclei demonstrated by retrograde transport of wheat germ agglutinin-horseradish peroxidase and tyrosine hydroxylase immunohistochemistry. J Comp Neurol. 1992;321:300-311. https://doi.org/10.1002/cne.903210209
  10. Hayakawa T, Zyo K. Fine structure of the supramammillary nucleus of the rat: analysis of the ultrastructural character of dopaminergic neurons. J Comp Neurol. 1994;346:127-136. https://doi.org/10.1002/cne.903460109
  11. Leranth C, Kiss J. A population of supramammillary area calretinin neurons terminating on medial septal area cholinergic and lateral septal area calbindin-containing cells are aspartate/glutamatergic. J Neurosci. 1996;16:7699-7710.
  12. Borhegyi Z, Magloczky Z, Acsady L, Freund TF. The supramammillary nucleus innervates cholinergic and GABAergic neurons in the medial septum-diagonal band of Broca complex. Neuroscience. 1998;82:1053-1065.
  13. Mizumori SJ, McNaughton BL, Barnes CA. A comparison of supramammillary and medial septal influences on hippocampal field potentials and single-unit activity. J Neurophysiol. 1989; 61:15-31.
  14. Kocsis B, Vertes RP. Characterization of neurons of the supramammillary nucleus and mammillary body that discharge rhythmically with the hippocampal theta rhythm in the rat. J Neurosci. 1994;14:7040-7052.
  15. Ikemoto S, Witkin BM, Zangen A, Wise RA. Rewarding effects of AMPA administration into the supramammillary or posterior hypothalamic nuclei but not the ventral tegmental area. J Neurosci. 2004;24:5758-5765. https://doi.org/10.1523/JNEUROSCI.5367-04.2004
  16. Shahidi S, Motamedi F, Naghdi N. Effect of reversible inactivation of the supramammillary nucleus on spatial learning and memory in rats. Brain Res. 2004;1026:267-274. https://doi.org/10.1016/j.brainres.2004.08.030
  17. Swanson LW. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull. 1982;9:321-353. https://doi.org/10.1016/0361-9230(82)90145-9
  18. Pan WX, McNaughton N. The supramammillary area: its organization, functions and relationship to the hippocampus. Prog Neurobiol. 2004;74:127-166. https://doi.org/10.1016/j.pneurobio.2004.09.003
  19. Curran T, Morgan JI. Fos: an immediate-early transcription factor in neurons. J Neurobiol. 1995;26:403-412. https://doi.org/10.1002/neu.480260312
  20. Choi DC, Furay AR, Evanson NK, Ulrich-Lai YM, Nguyen MM, Ostrander MM, Herman JP. The role of the posterior medial bed nucleus of the stria terminalis in modulating hypothalamicpituitary- adrenocortical axis responsiveness to acute and chronic stress. Psychoneuroendocrinology. 2008;33:659-669. https://doi.org/10.1016/j.psyneuen.2008.02.006
  21. Wirtshafter D, Stratford TR, Shim I. Placement in a novel environment induces fos-like immunoreactivity in supramammillary cells projecting to the hippocampus and midbrain. Brain Res. 1998;789:331-334. https://doi.org/10.1016/S0006-8993(97)01555-2
  22. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 2nd ed. New York: Academic Press; 1986.
  23. Oh JK, Kim YS, Park HJ, Lim EM, Pyun KH, Shim I. Antidepressant effects of Soyo-san on Immobilization stress in ovariectomized female rats. Biol Pharm Bull. 2007;30:1422-1426. https://doi.org/10.1248/bpb.30.1422
  24. Donahue DA, Dougherty EJ, Meserve LA. Influence of a combination of two tetrachlorobiphenyl congeners (PCB 47; PCB 77) on thyroid status, choline acetyltransferase (ChAT) activity, and short- and long-term memory in 30-day-old Sprague-Dawley rats. Toxicology. 2004;203:99-107. https://doi.org/10.1016/j.tox.2004.06.011
  25. Wahba ZZ, Soliman KF. Effect of stress on choline acetyltransferase activity of the brain and the adrenal of the rat. Experientia. 1992;48:265-268. https://doi.org/10.1007/BF01930471
  26. Jiang F, Khanna S. Microinjection of carbachol in the supramammillary region suppresses CA1 pyramidal cell synaptic excitability. Hippocampus. 2006;16:891-905. https://doi.org/10.1002/hipo.20219
  27. Lee HC, Chang DE, Yeom M, Kim GH, Choi KD, Shim I, Lee HJ, Hahm DH. Gene expression profiling in hypothalamus of immobilization-stressed mouse using cDNA microarray. Brain Res Mol Brain Res. 2005;135:293-300. https://doi.org/10.1016/j.molbrainres.2004.11.016
  28. Djordjevic J, Vuckovic T, Jasnic N, Cvijic G. Effect of various stressors on the blood ACTH and corticosterone concentration in normotensive Wistar and spontaneously hypertensive Wistar-Kyoto rats. Gen Comp Endocrinol. 2007;153:217-220. https://doi.org/10.1016/j.ygcen.2007.02.004
  29. Cullinan WE, Helmreich DL, Watson SJ. Fos expression in forebrain afferents to the hypothalamic paraventricular nucleus following swim stress. J Comp Neurol. 1996;368:88-99. https://doi.org/10.1002/(SICI)1096-9861(19960422)368:1<88::AID-CNE6>3.0.CO;2-G
  30. McEwen BS. Corticosteroids and hippocampal plasticity. Ann N Y Acad Sci. 1994;746:134-142.
  31. Kellendonk C, Gass P, Kretz O, Schutz G, Tronche F. Corticosteroid receptors in the brain: gene targeting studies. Brain Res Bull. 2002;57:73-83. https://doi.org/10.1016/S0361-9230(01)00638-4
  32. Corodimas KP, LeDoux JE, Gold PW, Schulkin J. Corticosterone potentiation of conditioned fear in rats. Ann N Y Acad Sci. 1994;746:392-393.
  33. McEwen BS. Stress and hippocampal plasticity. Annu Rev Neurosci. 1999;22:105-122. https://doi.org/10.1146/annurev.neuro.22.1.105
  34. McEwen BS, Sapolsky RM. Stress and cognitive function. Curr Opin Neurobiol. 1995;5:205-216. https://doi.org/10.1016/0959-4388(95)80028-X
  35. de Groote L, Linthorst AC. Exposure to novelty and forced swimming evoke stressor-dependent changes in extracellular GABA in the rat hippocampus. Neuroscience. 2007;148:794-805. https://doi.org/10.1016/j.neuroscience.2007.06.030

Cited by

  1. Effect of chronic immobilization stress on the pancreatic structure and the possible protective role of testosterone administration in male albino rats : vol.35, pp.3, 2012, https://doi.org/10.1097/01.ehx.0000418064.05379.e2
  2. New insights into the regulation of synaptic plasticity from an unexpected place: Hippocampal area CA2 vol.19, pp.9, 2012, https://doi.org/10.1101/lm.025304.111
  3. CP-154,526 Modifies CREB Phosphorylation and Thioredoxin-1 Expression in the Dentate Gyrus following Morphine-Induced Conditioned Place Preference vol.10, pp.8, 2015, https://doi.org/10.1371/journal.pone.0136164
  4. Substance P induces plasticity and synaptic tagging/capture in rat hippocampal area CA2 vol.114, pp.41, 2017, https://doi.org/10.1073/pnas.1711267114
  5. The role of the supramammillary area of the hypothalamus in cognitive functions vol.22, pp.1, 2012, https://doi.org/10.1080/19768354.2018.1427627
  6. Anti-stress effects of human placenta extract: possible involvement of the oxidative stress system in rats vol.18, pp.None, 2012, https://doi.org/10.1186/s12906-018-2193-x
  7. Antidepressant effect and neural mechanism of Acer tegmentosum in repeated stress–induced ovariectomized female rats vol.24, pp.4, 2012, https://doi.org/10.1080/19768354.2020.1808063
  8. CA2: A Highly Connected Intrahippocampal Relay vol.43, pp.1, 2020, https://doi.org/10.1146/annurev-neuro-080719-100343
  9. Selective neuromodulation and mutual inhibition within the CA3–CA2 system can prioritize sequences for replay vol.30, pp.11, 2012, https://doi.org/10.1002/hipo.23256