Morphological characterization of electrophysiologically and immunohistochemically identified basal forebrain cholinergic and neuropeptide Y-containing neurons

详细信息    查看全文

• 作者：Alvaro Duque (1)
  James M. Tepper (2)
  Laszlo Detari (3)
  Giorgio A. Ascoli (4)
  Laszlo Zaborszky (2)
  
• 关键词：Dendritic morphometry ; Three ; dimensional reconstruction ; Axon collaterals ; Rat
• 刊名：Brain Structure and Function
• 出版年：2007
• 出版时间：July 2007
• 年：2007
• 卷：212
• 期：1
• 页码：55-73
• 全文大小：1434KB
• 参考文献：1. Allen YS, Adrian TE, Allen JM, Tatemoto K, Crow TJ, Bloom SR, Polak JM (1983) Neuropeptide Y distribution in the rat brain. Science 221:877-79 CrossRef
  2. Alonso A, Khateb A, Fort P, Jones BE, Muhlethaler M (1996) Differential oscillatory properties of cholinergic and noncholinergic nucleus basalis neurons in guinea pig brain slice. Eur J Neurosci 8:169-82 CrossRef
  3. Aoki C, Pickel VM (1989) Neuropeptide Y in the cerebral cortex and the caudate-putamen nuclei: ultrastructural basis for interactions with GABAergic and non-GABAergic neurons. J Neurosci 9:4333-354
  4. Arendt T, Zvegintseva HG, Leontovich TA (1986) Dendritic changes in the basal nucleus of Meynert and in the diagonal band nucleus in Alzheimer’s disease—a quantitative Golgi investigation. Neuroscience 19:1265-278 CrossRef
  5. Bartus RT, Flicker C, Dean RL, Fisher S, Pontecorvo M, Figueiredo J (1986) Behavioral and biochemical effects of nucleus basalis magnocellularis lesions: implications and possible relevance to understanding or treating Alzheimer’s disease. Prog Brain Res 70:345-61
  6. Bengtson CP, Osborne PB (2000) Electrophysiological properties of cholinergic and noncholinergic neurons in the ventral pallidal region of the nucleus basalis in rat brain slices. J Neurophysiol 83:2649-660
  7. Bialowas J, Frotscher M, (1987) Choline acetyltransferase-immunoreactive neurons and terminals in the rat septal complex: a combined light and electron microscopic study. J Comp Neurol 259:298-07 CrossRef
  8. Book AA, Wiley RG, Schweitzer JB (1994) 192 IgG-saporin: I. Specific lethality for cholinergic neurons in the basal forebrain of the rat. J Neuropathol Exp Neurol 53:95-02
  9. Brashear HR, Zaborszky L, Heimer L (1986) Distribution of GABAergic and cholinergic neurons in the rat diagonal band. Neuroscience 17:439-51 CrossRef
  10. Brauer K, Schober W, Werner L, Winkelmann E, Lungwitz W, Hajdu F (1988) Neurons in the basal forebrain complex of the rat: a Golgi study. J Hirnforsch 29:43-1
  11. Brauer K, Seeger G, Hartig W, Rossner S, Poethke R, Kacza J, Schliebs R, Bruckner G, Bigl V (1998) Electron microscopic evidence for a cholinergic innervation of GABAergic parvalbumin-immunoreactive neurons in the rat medial septum. J Neurosci Res 54:248-53 CrossRef
  12. Carnevale NT, Tsai KY, Claiborne BJ, Brown TH (1997) Comparative electrotonic analysis of three classes of rat hippocampal neurons. J Neurophysiol 78:703-20
  13. Chen G, van den Pol AN (1996) Multiple NPY receptors coexist in pre- and postsynaptic sites: inhibition of GABA release in isolated self-innervating SCN neurons. J Neurosci 16:7711-724
  14. Chronwall BM, DiMaggio DA, Massari VJ, Pickel VM, Ruggiero DA, O’Donohue TL (1985) The anatomy of neuropeptide-Y-containing neurons in rat brain. Neuroscience 15:1159-181 CrossRef
  15. Csillik B, Rakic P, Knyihar-Csillik E (1998) Peptidergic innervation and the nicotinic acetylcholine receptor in the primate basal nucleus. Eur J Neurosci 10:573-85 CrossRef
  16. Dani JA (2001) Overview of nicotinic receptors and their roles in the central nervous system. Biol Psychiatry 49:166-74 CrossRef
  17. Davies P, Maloney AJ (1976) Selective loss of central cholinergic neurons in Alzheimer’s disease [letter]. Lancet 2:1403 CrossRef
  18. de Quidt ME, Emson PC (1986a) Distribution of neuropeptide Y-like immunoreactivity in the rat central nervous system-II. Immunohistochemical analysis. Neuroscience 18:545-18 CrossRef
  19. de Quidt ME, Emson PC (1986b) Distribution of neuropeptide Y-like immunoreactivity in the rat central nervous system-I. Radioimmunoassay and chromatographic characterisation. Neuroscience 18:527-43 CrossRef
  20. Detari L (2000) Tonic and phasic influence of basal forebrain unit activity on the cortical EEG. Behav Brain Res 115:159-70 CrossRef
  21. Detari L, Vanderwolf CH (1987) Activity of identified cortically projecting and other basal forebrain neurones during large slow waves and cortical activation in anaesthetized rats. Brain Res 437:1- CrossRef
  22. Detari L, Rasmusson DD, Semba K (1999) The role of basal forebrain neurons in tonic and phasic activation of the cerebral cortex. Prog Neurobiol 58:249-77 CrossRef
  23. Dringenberg HC, Vanderwolf CH (1998) Involvement of direct and indirect pathways in electrocorticographic activation. Neurosci Biobehav Rev 22:243-57 CrossRef
  24. Duque A, Zaborszky L (2006) Juxtacellular labeling of individual neurons in vivo: from electrophysiology to synaptology. In: Zaborszky L, Wouterlood FG, Lanciego JL (eds) Neuroanatomical tract-tracing 3 molecules, neurons, and systems. Springer, New York, pp 197-36 CrossRef
  25. Duque A, Balatoni B, Detari L, Zaborszky L (2000) EEG correlation of the discharge properties of identified neurons in the basal forebrain. J Neurophysiol 84:1627-635
  26. Edvinsson L, Minthon L, Ekman R, Gustafson L (1993) Neuropeptides in cerebrospinal fluid of patients with Alzheimer’s disease and dementia with frontotemporal lobe degeneration. Dementia 4:167-71
  27. Fisher RS, Levine MS (1989) Transmitter cosynthesis by corticopetal basal forebrain neurons. Brain Res 491:163-68 CrossRef
  28. Geula C, Mesulam MM (1994) Cholinergic systems and related neuropathological predilection patterns in Alzheimer disease. In: Terry RD, Katzman R, Bick KL (eds) Alzheimer disease. Raven, New York, pp 263-91
  29. Gotti C, Fornasari D, Clementi F (1997) Human neuronal nicotinic receptors. Prog Neurobiol 53:199-37 CrossRef
  30. Gritti I, Manns ID, Mainville L, Jones BE (2003) Parvalbumin, calbindin, or calretinin in cortically projecting and GABAergic, cholinergic, or glutamatergic basal forebrain neurons of the rat. J Comp Neurol 458:11-1 CrossRef
  31. Hajszan T, Zaborszky L (2002) Direct catecholaminergic-cholinergic interactions in the basal forebrain. III. Adrenergic innervation of choline acetyltransferase-containing neurons in the rat. J Comp Neurol 449:141-57 CrossRef
  32. Heimer L, de Olmos J, Alheid GF, Zaborszky L (1991) “Perestroika-in the basal forebrain: opening the border between neurology and psychiatry. Prog Brain Res 87:109-65
  33. H?kfelt T (1991) Neuropeptides in perspective: the last ten years. Neuron 7:867-79 CrossRef
  34. Horikawa K, Armstrong WE (1988) A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. J Neurosci Methods 25:1-1 CrossRef
  35. Hur EE, Zaborszky L (2005) Vglut2 afferents to the medial prefrontal and primary somatosensory cortices: a combined retrograde tracing in situ hybridization. J Comp Neurol 483(3):351-3 CrossRef
  36. Jaeger D (2001) Accurate reconstruction of neuronal morphology. In: De Schutter E (ed) Computational neuroscience: realistic modeling for experimentalists. Lewis, Boca Raton, pp 159-78
  37. Jones BE, Muhlethaler M (1999) Cholinergic and GABAergic neurons of the basal forebrain: role in cortical activation. In: Lydic R, Baghdoyan HA (eds) Handbook of behavioral state control—cellular and molecular mechanisms. CRC, Boca Raton, pp 213-34
  38. Kaspirzhny AV, Gogan P, Horcholle-Bossavit G, Tyc-Dumont S (2002) Neuronal morphology data bases: morphological noise and assessment of data quality. Network 13:357-80 CrossRef
  39. Khateb A, Muhlethaler M, Alonso A, Serafin M, Mainville L, Jones BE (1992) Cholinergic nucleus basalis neurons display the capacity for rhythmic bursting activity mediated by low-threshold calcium spikes. Neuroscience 51:489-94 CrossRef
  40. Khateb A, Fort P, Williams S, Serafin M, Jones BE, Muhlethaler M (1997) Modulation of cholinergic nucleus basalis neurons by acetylcholine and N-methyl-d -aspartate. Neuroscience 81:47-5 CrossRef
  41. Khateb A, Fort P, Williams S, Serafin M, Muhlethaler M, Jones BE (1998) GABAergic input to cholinergic nucleus basalis neurons. Neuroscience 86:937-47 CrossRef
  42. K?hler C, Eriksson L, Davies S, Chan-Palay V (1986) Neuropeptide Y innervation of the hippocampal region in the rat and monkey brain. J Comp Neurol 244:384-00 CrossRef
  43. Krichmar JL, Nasuto SJ, Scorcioni R, Washington SD, Ascoli GA (2002) Effects of dendritic morphology on CA3 pyramidal cell electrophysiology: a simulation study. Brain Res 941:11-8 CrossRef
  44. Leontovich TA, Zhukova GP (1963) The specificity of the neuronal structure and topography of the reticular formation in the brain and spinal cord of carnivora. J Comp Neurol 121:347-79 CrossRef
  45. Li Y, Brewer D, Burke RE, Ascoli GA (2005) Developmental changes in spinal motoneuron dendrites in neonatal mice. J Comp Neurol 483:304-17 CrossRef
  46. Manns ID, Alonso A, Jones BE (2000) Discharge properties of juxtacellularly labeled and immunohistochemically identified cholinergic basal forebrain neurons recorded in association with the electroencephalogram in anesthetized rats. J Neurosci 20:1505-518
  47. Metcalf RH, Boegman RJ (1989) Release of acetylcholine from tissue slices of the rat nucleus basalis magnocellularis. J Neurochem 52:1143-148 CrossRef
  48. Metcalf RH, Boegman RJ, Riopelle RJ, Ludwin SK (1988) The release of endogenous acetylcholine from the medial septum/diagonal band of rat brain. Neurosci Lett 93:85-0 CrossRef
  49. Millhouse OE (1986) Pallidal neurons in the rat. J Comp Neurol 254:209-27 CrossRef
  50. Minthon L, Edvinsson L, Gustafson L (1996) Correlation between clinical characteristics and cerebrospinal fluid neuropeptide Y levels in dementia of the Alzheimer type and frontotemporal dementia. Alzheimer Dis Assoc Disord 10:197-03 CrossRef
  51. Momiyama T, Zaborszky L (2006) Somatostatin presynaptically inhibits both GABA and glutamate release onto rat basal forebrain cholinergic neurons. J Neurophysiol 96:686-94 CrossRef
  52. Mosca KF, Duque A, Detari L, Noszek A, Rommer E, Zaborszky L (2005) Postsynaptic target of electrophysiologically identified NPY axons in the rat basal forebrain. Program No. 936.1. SFN Abstracts. Washington DC, Online
  53. Nishimura LM, Boegman RJ (1990) N-methyl-d -aspartate-evoked release of acetylcholine from the medial septum/diagonal band of rat brain. Neurosci Lett 115:259-64 CrossRef
  54. Nunez A (1996) Unit activity of rat basal forebrain neurons: relationship to cortical activity. Neuroscience 72:757-66 CrossRef
  55. Pang K, Tepper JM, Zaborszky L (1998) Morphological and electrophysiological characteristics of noncholinergic basal forebrain neurons. J Comp Neurol 394:186-04 CrossRef
  56. Picciotto MR, Caldarone BJ, King SL, Zachariou V (2000) Nicotinic receptors in the brain. Links between molecular biology and behavior. Neuropsychopharmacology 22:451-65 CrossRef
  57. Pinault D (1994) Golgi-like labeling of a single neuron recorded extracellularly. Neurosci Lett 170:255-60 CrossRef
  58. Pinault D (1996) A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or neurobiotin. J Neurosci Methods 65:113-36 CrossRef
  59. Poirazi P, Brannon T, Mel BW (2003) Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell. Neuron 37:977-87 CrossRef
  60. Ramon-Moliner E (1962) An attempt at classifying nerve cells on the basis of their dendritic patterns. J Comp Neurol 119:211-27 CrossRef
  61. Ramon-Moliner E, Nauta WJ (1966) The isodendritic core of the brain stem. J Comp Neurol 126:311-36 CrossRef
  62. Reiner PB, Semba K, Fibiger HC, McGeer EG (1987) Physiological evidence for subpopulations of cortically projecting basal forebrain neurons in the anesthetized rat. Neuroscience 20:629-36 CrossRef
  63. Sarter M, Bruno JP (1999) Abnormal regulation of corticopetal cholinergic neurons and impaired information processing in neuropsychiatric disorders. Trends Neurosci 22:67-4 CrossRef
  64. Sarter M, Parikh V (2005) Choline transporters, cholinergic transmission and cognition. Nat Rev Neurosci 6:48-6 CrossRef
  65. Schaefer AT, Larkum ME, Sakmann B, Roth A (2003) Coincidence detection in pyramidal neurons is tuned by their dendritic branching pattern. J Neurophysiol 89:3143-154 CrossRef
  66. Scheibel ME, Scheibel AB (1961) On circuit patterns of the brain stem reticular core. Ann N Y Acad Sci 89:857-65 CrossRef
  67. Scorcioni RE, Ascoli GA (2001) Algorithmic extraction of morphological statistics from electronic archives of neuroanatomy. Lect Notes Comp Sci 2084:30-7 CrossRef
  68. Scorcioni R, Lazarewicz MT, Ascoli GA (2004) Quantitative morphometry of hippocampal pyramidal cells: differences between anatomical classes and reconstructing laboratories. J Comp Neurol 473:177-93 CrossRef
  69. Semba K, Reiner PB, McGeer EG, Fibiger HC (1987) Morphology of cortically projecting basal forebrain neurons in the rat as revealed by intracellular iontophoresis of horseradish peroxidase. Neuroscience 20:637-51 CrossRef
  70. Sim JA, Griffith WH (1996) Muscarinic inhibition of glutamatergic transmissions onto rat magnocellular basal forebrain neurons in a thin-slice preparation. Eur J Neurosci 8:880-91 CrossRef
  71. Smiley JF, Levey AI, Mesulam MM (1999a) m2 muscarinic receptor immunolocalization in cholinergic cells of the monkey basal forebrain and striatum. Neuroscience 90:803-14 CrossRef
  72. Smiley JF, Subramanian M, Mesulam MM (1999b) Monoaminergic-cholinergic interactions in the primate basal forebrain. Neuroscience 93:817-29 CrossRef
  73. Sun QQ, Akk G, Huguenard JR, Prince DA (2001) Differential regulation of GABA release and neuronal excitability mediated by neuropeptide Y1 and Y2 receptors in rat thalamic neurons. J Physiol 531:81-4 CrossRef
  74. Sun QQ, Baraban SC, Prince DA, Huguenard JR (2003) Target-specific neuropeptide Y-ergic synaptic inhibition and its network consequences within the mammalian thalamus. J Neurosci 23:9639-649
  75. Surkis A, Taylor B, Peskin CS, Leonard CS (1996) Quantitative morphology of physiologically identified and intracellularly labeled neurons from the guinea-pig laterodorsal tegmental nucleus in vitro. Neuroscience 74:375-92 CrossRef
  76. Toth A, Zaborszky L, Detari L (2005) EEG effect of basal forebrain neuropeptide Y administration in urethane anaesthetized rats. Brain Res Bull 66:37-2 CrossRef
  77. Valverde F (1961a) A new type of cell in the lateral reticular formation of the brain stem. J Comp Neurol 117:189-95 CrossRef
  78. Valverde F (1961b) Reticular formation of the pons and medulla oblongata. A Golgi study. J Comp Neurol 116:71-9 CrossRef
  79. Vetter P, Roth A, Hausser M (2001) Propagation of action potentials in dendrites depends on dendritic morphology. J Neurophysiol 85:926-37
  80. Vezzani A, Sperk G, Colmers WF (1999) Neuropeptide Y: emerging evidence for a functional role in seizure modulation. Trends Neurosci 22:25-0 CrossRef
  81. Vilaro MT, Palacios JM, Mengod G (1994) Multiplicity of muscarinic autoreceptor subtypes? Comparison of the distribution of cholinergic cells and cells containing mRNA for five subtypes of muscarinic receptors in the rat brain. Brain Res Mol Brain Res 21:30-6 CrossRef
  82. Voytko ML, Olton DS, Richardson RT, Gorman LK, Tobin JR, Price DL (1994) Basal forebrain lesions in monkeys disrupt attention but not learning and memory [published erratum appears in J Neurosci 1995 Mar;15(3 Pt 2):following table of contents]. J Neurosci 14:167-86
  83. Walker LC, Koliatsos VE, Kitt CA, Richardson RT, Rokaeus A, Price DL (1989a) Peptidergic neurons in the basal forebrain magnocellular complex of the rhesus monkey. J Comp Neurol 280:272-82 CrossRef
  84. Walker LC, Price DL, Young WS (1989b) GABAergic neurons in the primate basal forebrain magnocellular complex. Brain Res 499:188-92 CrossRef
  85. Whitehouse PJ, Price DL, Struble RG, Clark AW, Coyle JT, Delon MR (1982) Alzheimer’s disease and senile dementia: loss of neurons in the basal forebrain. Science 215:1237-239 CrossRef
  86. Wolak ML, DeJoseph MR, Cator AD, Mokashi AS, Brownfield MS, Urban JH (2003) Comparative distribution of neuropeptide Y Y1 and Y5 receptors in the rat brain by using immunohistochemistry. J Comp Neurol 464:285-11 CrossRef
  87. Wu M, Shanabrough M, Leranth C, Alreja M (2000) Cholinergic excitation of septohippocampal GABA but not cholinergic neurons: implications for learning and memory. J Neurosci 20:3900-908
  88. Yu MC, Luo CB, Long L, Yew DT (1993) An immunohistochemical study of neuropeptide Y positive sites in the developing human hippocampal formation. Brain Res Dev Brain Res 72:277-81 CrossRef
  89. Zaborszky L, Cullinan WE (1996) Direct catecholaminergic-cholinergic interactions in the basal forebrain. I. Dopamine-beta-hydroxylase- and tyrosine hydroxylase input to cholinergic neurons. J Comp Neurol 374:535-54 CrossRef
  90. Zaborszky L, Duque A (2000) Local synaptic connections of basal forebrain neurons. Behav Brain Res 115:143-58 CrossRef
  91. Zaborszky L, Duque A (2003) Sleep–wake mechanisms and basal forebrain circuitry. Front Biosci 8:d1146–d1169. [PubMed#:12957822] http://www.bioscience.org/
  92. Zaborszky L, Heimer L, Eckenstein F, Leranth C (1986) GABAergic input to cholinergic forebrain neurons: an ultrastructural study using retrograde tracing of HRP and double immunolabeling. J Comp Neurol 250:282-95 CrossRef
  93. Zaborszky L, Pang K, Somogyi J, Nadasdy Z, Kallo I (1999) The basal forebrain corticopetal system revisited. Ann N Y Acad Sci 877:339-67 CrossRef
  94. Zaborszky L, Csordas A, Duque A, Somogy J, Nadasdy Z (2002) Computational anatomical analysis of the basal forebrain corticopetal system. In: Ascoli G (ed) Computational neuroanatomy: principles and methods. Humana, Totowa, pp 171-97 CrossRef
  95. Zador AM, Agmon-Snir H, Segev I (1995) The morphoelectrotonic transform: a graphical approach to dendritic function. J Neurosci 15:1669-682
  
• 作者单位：Alvaro Duque (1)
  James M. Tepper (2)
  Laszlo Detari (3)
  Giorgio A. Ascoli (4)
  Laszlo Zaborszky (2)
  
  1. Department of Neurobiology, Yale University School of Medicine, New Haven, CT, 06510, USA
  2. Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, NJ, 07102, USA
  3. Department of Physiology and Neurobiology, Loránd E?tv?s University, Budapest, 1117, Hungary
  4. Krasnow Institute for Advanced Study and Psychology Department, George Mason University, Fairfax, VA, 22030, USA
  

文摘

The basal forebrain (BF) contains cholinergic as well as different types of non-cholinergic corticopetal neurons and interneurons, including neuropeptide Y (NPY) containing cells. BF corticopetal neurons constitute an extrathalamic route to the cortex and their activity is associated with an increase in cortical release of the neurotransmitter acetylcholine, concomitant with low voltage fast cortical EEG activity. It has been shown in previous studies (Duque et al. in J Neurophysiol 84:1627-635, 2000) that in anesthetized rats BF cholinergic neurons fire mostly during low voltage fast cortical EEG epochs, while increased NPY neuronal firing is accompanied by cortical slow waves. In this paper, electrophysiologically and neurochemically characterized cholinergic and NPY-containing neurons were 3D reconstructed from serial sections and morphometrically analyzed. Cholinergic and NPY-containing neurons, although having roughly the same dendritic surface areas and lengths, were found to differ in dendritic thickness and branching structure. They also have distinct patterns of dendritic endings. The subtle differences in dendritic arborization pattern may have an impact on how synaptic integration takes place in these functionally distinct neuronal populations. Cholinergic neurons exhibited cortically projecting axons and extensive local axon collaterals. Elaborate local axonal arbors confined to the BF also originated from NPY-containing neurons. The presence of local axon collaterals in both cholinergic and NPY neurons indicates that the BF is not a mere conduit for various brainstem inputs to the cortex, but a site where substantial local processing must take place.