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Marginal division of the neostriatum: A subcortical memory center

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Journal of Biomedical Science

Abstract

The marginal division (MrD) is a pan-shaped subdivision in the caudal margin of the neostriatum newly discovered in the brains of the rat, cat, monkey and humans. A variety of intensely expressed neuropeptides and monoamines and their receptors were identified in the fibers, terminals and neuronal somata in the MrD with immunohistochemical and patch clamp methods. The MrD was shown to be involved in learning and memory by double-blind studies of Y-maze learning and long-term potentiation in rats. c-Fos expression and tract-tracing techniques with immunoelectronmicroscopy indicated that the MrD is a new component of the limbic system and is a key linking area between the limbic system and the basal nucleus of Meynert. Functional magnetic resonance image (fMRI) studies illustrated that the MrD and the prefrontal cortex are involved in digital working memory in the human brain. A cerebral hemorrhage case report confirmed the findings with fMRI. In conclusion, based on the position of the MrD, its advanced development in higher mammalian brains, abundant blood supply and diverse connections with other memory-related structures, MrD is likely to be an important subcortical center of learning and memory.

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References

  1. Aracava Y, Deshpands S, Swanson K, Rapoport H, Wonnacott S, Lunt G, Albuquerque EX. Nicotinic acetylcholine receptors in cultured neurons from the hippocampus and brain stem of the rat characterized by single channel recording. FEBS Lett 222:63–70;1987.

    Google Scholar 

  2. Bao XM, Shu SY. Distribution of neurotensin and somatostatin immunoreactivity in the marginal division of the rat striatum. Chin J Histochem Cytochem 6:1–5;1997.

    Google Scholar 

  3. Bao XM, Shu SY. Distribution of substance P-, Leu-enkephalin-, cholecystokinin-immunoreactivity in the marginal division of the rat striatum. Chin J Neuroanat 13:343–350;1997.

    Google Scholar 

  4. Bao XM, Shu SY, Li SX, Xu ZW. The afferent projections of the marginal division in the rat striatum: WGA-HRP retrograde and anterograde transport study. Chin J Neuroanat 9:93–96;1993.

    Google Scholar 

  5. Bao XM, Shu SY, Niu DB, Xu ZW. Distribution of substance P, Leu-enkephalin, neuropeptide Y, and NADPH-d reactivity in the marginal division of cat striatum. Chin J Neurosci 14:213–217;1998.

    Google Scholar 

  6. Bao XM, Shu SY, Wang J. Distribution of the limbic system-associated membrane protein in the marginal division of rat. Chin J Neuroanat 17:117–120;2001.

    Google Scholar 

  7. Bao XM, Shu SY, Zhang YZ, Zhou GD. Expression of c-fos oncogene protein in the brain following kainic acid injection into the marginal division of the rat striatum. Chin J Neuroanat 13:343–350;1997.

    Google Scholar 

  8. Bechtereva NP, Genkin AA, Moiseeva NI, Smirnov VM. Electrographic evidence of participation of deep structures of the human brain in certain mental processes. Electroencephalogr Clin Neurophysiol 25(suppl):153;1967.

    Google Scholar 

  9. Biggan SL, Beninger RJ, Cockhill J, Jhamandas K, Boegman RJ. Quisqualate lesions of rat NBM: Selective effects on working memory in a double Y-maze. Brain Res Bull 26:613–616;1991.

    Google Scholar 

  10. Bliss TV, Collingridge GL. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361:31–39;1993.

    Google Scholar 

  11. Bliss TVP, Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:331–356;1973.

    Google Scholar 

  12. Brooks VB: The Neural Basis of Motor Control. New York, Oxford University Press, 1986.

    Google Scholar 

  13. Carpenter MB, Sutin J: Human Neuroanatomy, ed 8, revised. Baltimore, Waverly, 1983.

    Google Scholar 

  14. Chudler EH, Dong WK. The role of the basal ganglia in nociception and pain. Pain 60:3–38;1995.

    Google Scholar 

  15. Chudler EH, Sugiyama K, Dong WK. Nociceptive responses in the neostriatum and globus pallidus of the anesthetized rat. J Neurophysiol 69:1890–1903;1993.

    Google Scholar 

  16. Conner-Kerr TA, Simmons DR, Peterson GM, Terrian DM. Evidence for the corelease of dynorphin and glutamate from rat hippocampal mossy fiber terminals. J Neurochem 61:627–636;1993.

    Google Scholar 

  17. Conrad CD, Lupien SJ, Thanasoulis LC, McEwen BS. The effects of type I and type II corticosteroid receptor agonists on exploratory behavior and spatial memory in the Y-maze. Brain Res 759:76–83;1997.

    Google Scholar 

  18. Costa JC, Tomaz C. Posttraining administration of substance P and its N-terminal fragment block the amnestic effects of diazepam. Neurobiol Learn Mem 69:65–70;1998.

    Google Scholar 

  19. D'Esposito M, Postle BR, Jonides J, Smith EE. The neural substrate and temporal dynamics of interference effects in working memory as revealed by event-related functional MRI. Proc Natl Acad Sci USA 96:7514–7519;1999.

    Google Scholar 

  20. Gore P, Alheid GF, Shammah-Lagnado SJ, Beltramino CA, Yang M, Marksteiner J, et al. Peripallidal portions of the extended amygdala in the rat: The supracapsular and marginal zones. Abstr Soc Neurosci 22:2049;1996.

    Google Scholar 

  21. Grimm R, Tischmeyer W. Complex patterns of immediate early gene induction in rat brain following brightness discrimination training and pseudotraining. Behav Brain Res 84:109–166;1997.

    Google Scholar 

  22. Gulya K, Kovascs, Ksa P. Partial depletion of endogenous zinc level by (D-Pen2, D-Pen5) enkephalin in the rat brain. Life Sci 48:57–62;1991.

    Google Scholar 

  23. Han ZS. Hippocampal formation. In: Wan XC, Yang TZ, Xu CT, eds. Modern Neurobiology. Beijing, Beijing Medical University and China Xiehe Medical University, 459–476;1999.

    Google Scholar 

  24. Heimer L, Alheid GF. Piecing together the puzzle of basal forebrain anatomy. In: Napier TC, Kalivas PW, Hanin I, eds. The Basal Forebrain. New York, Plenum, 1–42;1991.

    Google Scholar 

  25. Heimer L, Zahm DS, Alheid GF. Basal ganglia. In: Paxinos G, ed. The Rat Nervous System. New York, Academic, 579–628;1995.

    Google Scholar 

  26. Ikegami S, Inokuchi K. Antisense DNA against calcineurin facilitates memory in contextual fear conditioning by lowering the threshold for hippocampal long-term potentiation induction. Neuroscience 98:637–646;2000.

    Google Scholar 

  27. Ishizuk N, Weber J, Amaral DG. Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol 295:580–623;1990.

    Google Scholar 

  28. Kalivas PW, Barness CD: Limbic Motor Circuits and Neuropsychiatry. Boca Raton, CRC, 1993.

    Google Scholar 

  29. Lashley KS. In search of the engram. Symp Soc Exp Biol 4:454–482;1950.

    Google Scholar 

  30. Lavoie B, Parent A. Pedunculopontine nucleus in the squirrel monkey: Projections to the basal ganglia as revealed by anterograde tract-tracing methods. J Comp Neurol 344:210–310;1994.

    Google Scholar 

  31. Li YY, Shu SY, Bao XM, Wu WL. Distribution and fiber connection of calcitonin gene-related peptide immunoreactivity in the marginal division of the rat striatum. J First Mil Med Univ 19:201–204;1999.

    Google Scholar 

  32. Li YY, Shu SY, Bao XM, Wu WL. The connection among the marginal division of striatum, amygdaliod nucleus and bed nucleus of the stria terminalis in the rat brain as revealed by immunohistochemistry. Chin J Neuroanat 16:265–268;2000.

    Google Scholar 

  33. Li YY, Shu SY, Bao XM, Wu WL. Distribution of substance P in rat striatum and its linkage with other brain structures: An immunohistochemical study. J Fourth Mil Med Univ 21:890–893;2000.

    Google Scholar 

  34. Lidsky TI, Levine MS, Kreinick CJ, Schwartzbaum JS. Retrograde effects of amygdaloid stimulation on conditioned suppression (CER) in rats. J Comp Physiol Psychol 73:135–49;1970.

    Google Scholar 

  35. Mancini M, Ricci A, Amenta F. Age-related changes in sulfide-silver staining in the rat neostriatum: A quantitative histochemical study. Neurobiol Aging 14:501–504;1992.

    Google Scholar 

  36. Nicolle MM, Bizon JL, Gallagher M. In vitro autoradiography of ionotropic glutamate receptors in hippocampus and striatum of aged Long-Evans rats: Relationship to spatial learning. Neuroscience 74:741–756;1996.

    Google Scholar 

  37. Panagis G, Nomikos GG, Milliaressis E, Chergui K, Kastellakis A, Svensson TH, Spyraki C. Ventral pallidum self-stimulation induces stimulus dependent increase in c-fos expression in reward-related brain regions. Neuroscience 77:175–186;1997.

    Google Scholar 

  38. Ramirez OA, Carrer HF. Correlation between threshold to induce long-term potentiation in the hippocampus and performance in a shuttle box avoidance response in rats. Neurosci Lett 104:152–156;1989.

    Google Scholar 

  39. Riedel G, Wetzel W, Reymann KG. Computer-assisted shock-reinforced Y-maze training: A method for studying spatial alternation behavior. Neuroreport 5:2061–2064;1994.

    Google Scholar 

  40. Sagar SM, Sharp FR, Curran T. Expression of c-fos protein in brain: Metabolic mapping at the cellular level. Science 240:1328–1331;1988.

    Google Scholar 

  41. Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11;1957.

    Google Scholar 

  42. Sgambato V, Abo V, Rogard M, Besson MJ, Denian JM. Effect of electrical stimulation of the cerebral cortex on the expression of the Fos protein in the basal ganglia. Neuroscience 8:93–112;1997.

    Google Scholar 

  43. Shammah-Lagnado SJ, Alheid GF, Heimer L. Afferent connections of the interstitial nucleus of the posterior limb of the anterior commissure and adjacent amygdalostriatal transition area in the rat. Neuroscience 94:1097–1123;1999.

    Google Scholar 

  44. Shu SY, Bao R, Bao XM, Zheng ZC, Nui DB. Synaptic connections between the projection from the marginal division of the striatum to the Meynert's basal nucleus and its relationship to learning and memory behavior of the rat. Chin J Histochem Cytochem 7:1–11;1998.

    Google Scholar 

  45. Shu SY, Bao XM. Ultrastructural characteristics of substance P-immunoreactive terminals in marginal division of rat striatum. Chin Med J 104:887–896;1991.

    Google Scholar 

  46. Shu SY, Bao XM, Li SX. The immunohistochemistry of marginal division and oncogene expression in rat brain following kainic acid stimulation in the basal nucleus of Meynert and marginal division of the rat striatum. Histochem Cytochem 29:1028–1029;1996.

    Google Scholar 

  47. Shu SY, Bao XM, Li SX, Niu DB, Xu ZW, Li YY. A new subdivision of mammalian neostriatum with functional implications to learning and memory. J Neurosci Res 58:242–253;1999.

    Google Scholar 

  48. Shu SY, Bao XM, Li SX, Xu ZW. Immunohistochemical characteristics of afferent projection neurons in the marginal division of the rat striatum. Chin J Anat 16:509–511;1993.

    Google Scholar 

  49. Shu SY, Bao XM, Peterson GM. Ultrastructure of the marginal division in the rat striatum. Chin Med J 105:102–109;1992.

    Google Scholar 

  50. Shu SY, Bao XM, Wang J, Wu YM. Hippocampal long-term potentiation attenuated by the lesion in a new area of the rat striatum. J Neurosci Res, submitted.

  51. Shu SY, Bao XM, Zhang C, Li SX, Chan WY, Yew D. A new subdivision, marginal division, in the neostriatum of the monkey brain. Neurochem Res 25:231–237;2000.

    Google Scholar 

  52. Shu SY, McGinty JF, Peterson GM. High density zinc-containing and dynorphin B- and substance P-immunoreactive terminals in the marginal division of the rat striatum. Brain Res Bull 24:201–205;1990.

    Google Scholar 

  53. Shu SY, Penny GR, Peterson GM. The ‘marginal division’: A new subdivision in the neostriatum of the rat. J Chem Neuroanat 1:147–163;1988.

    Google Scholar 

  54. Shu SY, Wang LN, Wu YM, Bao XM, Wang ZF, Wen ZP. Hemorrhage in the medial areas of bilateral putamens causing deficiency of memory and calculation: Report of one case. J First Mil Med Univ 22:38–40;2002.

    Google Scholar 

  55. Shu SY, Wu YM, Bao XM, Wen ZB, Huang FH, Li SX, Fu QZ, Ning Q. A new area in the human brain with function of learning and memory: A structural and functional study. Mol Psychiatry, in press.

  56. Sorensen JC, Slomianka L, Christensen J, Zimmer J. Zinc-containing telencephalic connections to the rat striatum: A combined Fluoro-Gold tracing and histochemical study. Exp Brain Res 105:370–382;1995.

    Google Scholar 

  57. Squire LR, Zola MS. The medial temporal lobe memory system. Science 253:1380–1386;1991.

    Google Scholar 

  58. Talley EM, Rosin DL, Lee A, Guyenet PG, Lynch KR. Distribution of alpha 2A-adrenergic receptor-like immunoreactivity in the rat central nervous system. J Comp Neurol 372:111–134;1996.

    Google Scholar 

  59. Wang H, Shu SY, Bao XM. Expression of NMDA2B receptor mRNA in the marginal division of rat striatum. J First Mil Med Univ 21:574–576;2001.

    Google Scholar 

  60. Wang H, Shu SY, Bao XM, Yang WK. Expression of immediate-early c-fos and c-jun in the marginal division of striatum during learning and memory. J First Mil Med Univ 22:9–12;2002.

    Google Scholar 

  61. Zou F, Gao TM, Chen PX. Properties of acetylcholine receptor channel in hippocampal neurons. Acad J SUMS 15:86–90;1994.

    Google Scholar 

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  1. Institute for Neuroscience of the First Military Medical University Zhu-jiang Hospital, 253 Gong-ye Road, 510280, Guangzhou, China

    Si Yun Shu MD

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Shu, S.Y. Marginal division of the neostriatum: A subcortical memory center. J Biomed Sci 10, 14–29 (2003). https://doi.org/10.1007/BF02255993

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  • DOI: https://doi.org/10.1007/BF02255993

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