The human medial amygdala: Structure, diversity, and complexity of dendritic spines

Journal of Anatomy

Volumn 227, Issue 4, 2015, Pages 440-459

  Dall'Oglio, Aline ^a   Dutra, Ana Carolina L ^a   Moreira, Jorge E ^b   Rasia Filho, Alberto A ^a  

^a UNIVERSIDADE FEDERAL DE CIÊNCIAS DA SAÚDE DE PORTO ALEGRE   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

3D reconstruction; DiI dye; Extended amygdala; Golgi method; Neuronal morphology; Spine shape; Ultrastructure

Indexed keywords

CARBOCYANINE; FLUORESCENT DYE;

ADULT; AGED; ARTICLE; AUTOPSY; CAUSE OF DEATH; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITIC SPINE; GOLGI STAIN; HUMAN; HUMAN CELL; HUMAN TISSUE; IMAGE PROCESSING; IMMUNOFLUORESCENCE; MALE; MEDIAL AMYGDALA; MIDDLE AGED; POTENTIAL DIFFERENCE; PRIORITY JOURNAL; SYNAPSE; THREE DIMENSIONAL IMAGING; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; AMYGDALA; ANATOMY AND HISTOLOGY; AXON; CADAVER; DENDRITE;

AGED; AMYGDALA; AXONS; CADAVER; DENDRITES; DENDRITIC SPINES; HUMANS; MALE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MIDDLE AGED;

EID: 84941188666     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/joa.12358     Document Type: Article

References (111)

1. Anderson K, Bones B, Robinson B, et al. (2009) The morphology of supragranular pyramidal neurons in the human insular cortex: a quantitative Golgi study. Cereb Cortex 19, 2131-2144.
2. Araque A, Parpura V, Sanzgiri RP, et al. (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 22, 208-215.
3. Arellano JI, Benavides-Piccione R, DeFelipe J, et al. (2007a) Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies. Front Neurosci 1, 131-143.
4. Arellano JI, Espinosa A, Fairén A, et al. (2007b) Non-synaptic dendritic spines in neocortex. Neuroscience 145, 464-469.
5. Benavides-Piccione R, Ballesteros-Yáñes I, DeFelipe J, et al. (2002) Cortical area and species differences in dendritic spine morphology. J Neurocytol 31, 337-346.
6. Benzing WC, Mufson EJ, Jennes L, et al. (1992) Distribution of neurotensin immunoreactivity within the human amygdaloid complex: a comparison with acetylcholinesterase- and Nissl-stained tissue sections. J Comp Neurol 317, 283-297.
7. Bian X (2013) Physiological and morphological characterization of GABAergic neurons in the medial amygdala. Brain Res 1509, 8-19.
8. Bian X, Yanagawa Y, Chen WR, et al. (2008) Cortical-like functional organization of the pherormone-processing circuits in the medial amygdala. J Neurophysiol 99, 77-86.
9. Bianchi S, Stimpson CD, Bauernfeind AL, et al. (2013) Dendritic morphology of pyramidal neurons in the chimpanzee neocortex: regional specializations and comparison to humans. Cereb Cortex 23, 2429-2436.
10. Blood AJ, Zatorre RJ (2001) Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion. Proc Natl Acad Sci USA 98, 11818-11823.
11. Boersma MCH, Dresselhaus EC, De Biase LM, et al. (2011) A requirement for nuclear factor-kB in developmental and plasticity-associated synaptogenesis. J Neurosci 31, 5414-5425.
12. Bolam JP (1992) Experimental Neuroanatomy: A Practical Approach. New York: Oxford University Press.
13. Bourne JN, Harris KM (2007) Dendritic spines. In: eLS. http://www.els.net. doi: 10.1002/9780470015902.a0000093.pub2. Chichester: John Wiley & Sons Ltd.
14. Bourne JN, Harris KM (2008) Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31, 47-67.
15. Brodal A (1981) Neurological Anatomy. New York: Oxford University Press.
16. Brusco J, Dall'Oglio A, Rocha LB, et al. (2010) Descriptive findings on the morphology of dendritic spines in the rat medial amygdala. Neurosci Lett 483, 152-156.
17. Brusco J, Merlo S, Ikeda ÉT, et al. (2014) Inhibitory and multisynaptic spines, and hemispherical synaptic specialization in the posterodorsal medial amygdala of male and female rats. J Comp Neurol 522, 2075-2088.
18. Chen S, Sabatini BL (2012) Signaling in dendritic spines and spine microdomains. Curr Opin Neurobiol 22, 389-396.
19. Chen X, Leischner U, Rochefort NL, et al. (2011) Functional mapping of single spines in cortical neurons in vivo. Nature 475, 501-507.
20. Cooke BM, Stokas MR, Woolley CS (2007) Morphological sex differences and laterality in the prepubertal medial amygdala. J Comp Neurol 501, 904-915.
21. Dall'Oglio A, Gehlen G, Achaval M, et al. (2008) Dendritic branching features of posterodorsal medial amygdala neurons of adult male and female rats: further data based on the Golgi method. Neurosci Lett 430, 151-156.
22. Dall'Oglio A, Ferme D, Brusco J, et al. (2010) The 'single-section' Golgi method adapted for formalin-fixed human brain and light microscopy. J Neurosci Methods 189, 51-55.
23. Dall'Oglio A, Xavier LL, Hilbig A, et al. (2013) Cellular components of the human medial amygdaloid nucleus. J Comp Neurol 521, 589-611.
24. DeArmond SJ, Fusco MM, Dewey MM (1989) Structure of the Human Brain. New York: Oxford University Press.
25. Dityatev A, Rusakov DA (2011) Molecular signals of plasticity at the tetrapartite synapse. Curr Opin Neurobiol 21, 1-7.
26. Drakew A, Müller M, Gähwiler BH, et al. (1996) Spine loss in experimental epilepsy: quantitative light and electron microscopic analysis of intracellularly stained CA3 pyramidal cells in hippocampal slice cultures. Neuroscience 70, 31-45.
27. Everitt B (1995) Limbic lobe and olfactory pathways. In: Gray's Anatomy. (eds Berry MM, Bannister LH, Standring SM), pp. 1115-1141, London: Churchill Livingstone.
28. Feldman ML (1984) Morphology of the neocortical pyramidal neuron. In: Cerebral Cortex, Vol. 2. (eds Jones EG, Peters A), pp. 107-121, New York: Plenum Press.
29. Fiala JC, Harris KM (1999) Dendrite structure. In: Dendrites. (eds Stuart G, Sprutson N, Häusser M), pp. 1-34, New York: Oxford University Press.
30. Fiala JC, Spacek J, Harris KM (2002) Dendritic spine pathology: cause or consequence of neurological disorders? Brain Res Rev 39, 29-54.
31. Fortin DA, Srivastava T, Soderling TRS (2012) Structural modulation of dendritic spines during synaptic plasticity. Neuroscientist 18, 326-341.
32. Freese JL, Amaral DG (2009) Neuroanatomy of the primate amygdala. In: The Human Amygdala. (eds Whalen PJ, Phelps EA), pp. 3-42, New York: The Guilford Press.
33. Frick A, Johnston D (2005) Plasticity of dendritic excitability. J Neurobiol 64, 100-115.
34. Gabbott PL, Somogyi J (1984) The 'single' section Golgi-impregnation procedure: methodological description. J Neurosci Methods 11, 221-230.
35. Gamer M, Zurowski B, Büchel C (2010) Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans. Proc Natl Acad Sci USA 107, 9400-9405.
36. García-López P, García-Marín V, Freire M (2007) The discovery of dendritic spines by Cajal in 1888 and its relevance in the present neuroscience. Prog Neurobiol 83, 110-130.
37. García-López P, García-Marín V, Freire M (2010) Dendritic spines and development: towards a unifying model of spinogenesis - a present day review of Cajal's histological slides and drawings. Neural Plast 769207, doi: 10.1155/2010/769207.
38. Garey LJ, Ong WY, Patel TS, et al. (2014) Reduced dendritic spine density on cerebral cortical neurons in schizophrenia. J Neurol Neurosurg Psychiatry 65, 446-453.
39. Giaume C, Liu X (2012) From a glial syncytium to a more restricted and specific glial networking. J Physiol 106, 34-39.
40. Gloor P (1997) The Temporal Lobe and Limbic System. New York: Oxford University Press.
41. Goldstein JM, Seidman LJ, Horton NJ, et al. (2001) Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cereb Cortex 11, 490-497.
42. González-Burgos I, Rivera-Cervantes MCR, Velázquez-Zamora DA, et al. (2012) Selective estrogen receptor modulators regulate dendritic spine plasticity in the hippocampus of male rats. Neural Plast 2012:309494. doi: 10.1155/2012/309494.
43. González-Ramírez MM, Velázquez-Zamora DA, Olvera-Cortés ME, et al. (2014) Changes in the plastic properties of hippocampal dendritic spines underlie the attenuation of place learning in healthy aged rats. Neurobiol Learn Mem 109, 94-103.
44. Gulledge AT, Carnevale NT, Stuart GJ (2012) Electrical advantages of dendritic spines. PLoS One 7, e36007.
45. Hall EA (1972) The amygdala of the cat: a Golgi study. Z Zellforsch Mikrosk Anat 134, 439-458.
46. Harnett MT, Makara JK, Spruston N, et al. (2012) Synaptic amplification by dendritic spines enhances input cooperativity. Nature 491, 599-605.
47. Harris KM, Jensen FE, Tsao B (1992) Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci 12, 2685-2705.
48. Heimer L, Van Hoesen GW, Trimble M, et al. (2008) Anatomy of Neuropsychiatry - The New Anatomy of the Basal Forebrain and Its Implications for Neuropsychiatric Illness. San Diego, CA: Academic Press.
49. Holtmaat A, Svoboda K (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 10, 647-658.
50. Horiguchi K, Kouki T, Fujiwara K, et al. (2011) The extracellular matrix component laminin promotes gap junction formation in the rat anterior pituitary gland. J Endocrinol 208, 225-232.
51. Izzo PN, Graybiel AM, Bolam JP (1987) Characterization of substance P- and [Met]enkephalin-immunoreactive neurons in the caudate nucleus of cat and ferret by a single section Golgi procedure. Neuroscience 20, 577-587.
52. Jacobs B, Driscoll L, Schall M (1997) Life-span dendritic and spine changes in areas 10 and 18 of human cortex: a quantitative Golgi study. J Comp Neurol 386, 661-680.
53. Jacobs B, Schall M, Prather M, et al. (2001) Regional dendritic and spine variation in human cerebral cortex: a quantitative Golgi study. Cereb Cortex 11, 558-571.
54. Janak PH, Tye KM (2015) From circuits to behavior in the amygdala. Nature 517, 284-292.
55. Kasai H, Fukuda M, Watanabe S, et al. (2010) Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci 33, 121-129.
56. Kilpatrick LA, Zald DH, Pardo JV, et al. (2006) Sex-related differences in amygdala functional connectivity during resting conditions. NeuroImage 30, 452-461.
57. Kim BG, Dai H-N, McAtee M, et al. (2007) Labeling of dendritic spines with the carbocyanine dye DiI for confocal microscopic imaging in lightly fixed cortical slices. J Neurosci Methods 162, 237-243.
58. Kirov SA, Sorra KE, Harris KM (1999) Slices have more synapses than perfusion-fixed hippocampus from young and mature rats. J Neurosci 19, 2876-2886.
59. Kuwajima M, Spacek J, Harris KM (2013) Beyond counts and shapes: studying pathology of dendritic spines in the context of the surrounding neuropil through serial section electron microscopy. Neuroscience 251, 75-89.
60. Lauer M, Senitz D (2006) Dendritic excrescences seem to characterize hippocampal CA3 pyramidal neurons in humans. J Neural Transm 113, 1469-1475.
61. Lee KFH, Soares C, Béïque JC (2012) Examining form and function of dendritic spines. Neural Plast 2012:704103. doi:10.1155/2012/704103.
62. Lepousez G, Nissant A, Bryant AK, et al. (2014) Olfactory learning promotes input-specific synaptic plasticity in adult-born neurons. Proc Natl Acad Sci USA 111, 13984-13989.
63. Liberzon I, Phan KL, Decker LR, et al. (2003) Extended amygdala and emotional salience: a PET activation study of positive and negative affect. Neurospsychopharmacology 28, 726-733.
64. Lippman J, Dunaevsky A (2005) Dendritic spine morphogenesis and plasticity. J Neurobiol 64, 47-57.
65. Lu D, He L, Xiang W, et al. (2013) Somal and dendritic development of human CA3 pyramidal neurons from midgestation to middle childhood: a quantitative Golgi study. Anat Rec 296, 123-132.
66. Mai JK, Paxinos G, Voss T (2008) Atlas of the Human Brain. New York: Academic Press.
67. Mancuso JJ, Chen Y, Li X, et al. (2012) Methods of dendritic spine detection: from Golgi to high-resolution optical imaging. Neuroscience 251, 129-140.
68. Martin LJ, Powers RE, Dellovade TL, et al. (1991) The bed nucleus-amygdala continuum in human and monkey. J Comp Neurol 309, 445-485.
69. Matus A (2000) Actin-based plasticity in dendritic spines. Science 290, 754-758.
70. McDonald J, Mascagni F, Augustine JR (1995) Neuropeptide Y and somatostatin-like immunoreactivity in neurons of the monkey amygdala. Neuroscience 66, 959-982.
71. Medvedev N, Popov V, Henneberger C, et al. (2014) Glia selectively approach synapses on thin dendritic spines. Philos Trans R Soc Lond B Biol Sci 369, 20140047.
72. Meek J, Kirchberg G, Grant K, et al. (2004) Dye coupling without gap junctions suggests excitatory connections of γ-aminobutiric acidergic neurons. J Comp Neurol 468, 151-164.
73. Mishchenko Y, Hu T, Spacek J, et al. (2010) Ultrastructural analysis of hippocampal neuropil from the connectomics perspective. PLoS One 67, 1009-1020.
74. Morales J, Benavides-Piccione R, Dar M, et al. (2014) Random positions of dendritic spines in human cerebral cortex. J Neurosci 34, 10078-10084.
75. Niimi K, Horie S, Yokosuka M, et al. (2012) Heterogeneous electrophysiological and morphological properties of neurons in the mouse medial amygdala in vitro. Brain Res 1480, 41-52.
76. Nimchinsky EA, Gilissen E, Allman JM, et al. (1999) A neuronal morphologic type unique to humans and great apes. Proc Natl Acad Sci USA 96, 5268-5273.
77. Oikonomou KD, Singh MB, Sterjanaj EV, et al. (2014) Spiny neurons of amygdala, striatum, and cortex use dendritic plateau potentials to detect network UP states. Front Neurosci 8, 292.
78. de Olmos JS (2004) Amygdala. In: The Human Nervous System. (eds Paxinos G, Mai J), pp. 739-868, San Diego, CA: Elsevier.
79. Ossewaarde L, van Wingen GA, Rijpkema M, et al. (2013) Menstrual cycle-related changes in amygdala morphology are associated with changes in stress sensitivity. Hum Brain Mapp 34, 1187-1193.
80. Pannese E (1980) Caratteri strutturali utili per l'identificazione delle cellule gliali del sistema nervoso central. Istocitopatologia 2, 129-136.
81. Pannese E (1994) Neurocitology: Fine Structure of Neurons, Nerve Processes, and Neuroglial Cells. New York: Thieme.
82. Peters A, Jones EG (1984) Classification of cortical neurons. In: Cerebral Cortex. Functional Properties of Cortical Cells, Vol. 2. (eds Jones EG, Peters A), pp. 107-121, New York: Plenum Press.
83. Peters A, Palay SL, Webster H (1991) The Fine Structure of the Nervous System. New York: Oxford University Press.
84. Pitkänen A, Amaral DG (1994) The distribution of GABAergic cells, fibers, and terminals in the monkey amygdaloid complex: an immunohistochemical and in situ hybridization study. J Neurosci 74, 2200-2224.
85. Rasia-Filho AA, Fabian C, Rigoti K, et al. (2004) Influence of sex, estrous cycle and motherhood in dendritic spine density in the rat medial amygdala revealed by the Golgi method. Neuroscience 126, 839-847.
86. Rasia-Filho AA, Brusco J, Rocha LB, et al. (2010) Dendritic spines observed by extracellular DiI dye and immunolabeling under confocal microscopy. Nat Protoc/Protoc Exch. http://www.nature.com/protocolexchange/protocols/1890
87. Rasia-Filho AA, Dalpian F, Menezes IC, et al. (2012) Dendritic spines of the medial amygdala: plasticity, density, shape, and subcellular modulation by sex steroids. Histol Histopathol 27, 985-1011.
88. Rochefort NL, Konnerth A (2012) Dendritic spines: from structure to in vivo function. EMBO Rep 13, 699-708.
89. Sätzler K, Söhl LF, Bollmann JH, et al. (2002) Three-dimensional reconstruction of a Calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. J Neurosci 22, 10567-10579.
90. Schumann CM, Amaral DG (2005) Stereological estimation of the number of neurons in the human amygdaloid complex. J Comp Neurol 491, 320-329.
91. Segal M (2010) Dendritic spines, synaptic plasticity and neuronal survival: activity shapes dendritic spines to enhance neuronal viability. Eur J Neurosci 31, 2178-2184.
92. Sims KS, Williams RS (1990) The human amygdaloid complex: a cytologic and histochemical atlas using Nissl, myelin, acetylcholinesterase and nicotinamide adenine dinucleotide phosphate diaphorase staining. Neuroscience 2, 449-472.
93. Sorvari H (1997) Neurons containing calcium-binding proteins in the human amygdaloid complex. Ph.D. Thesis, University of Kuopio, Finland.
94. Sorvari H, Soininen H, Pitkänen A (1996a) Calretinin-immunoreactive cells and fibers in the human amygdaloid complex. J Comp Neurol 369, 188-208.
95. Sorvari H, Soininen H, Pitkänen A (1996b) Calbindin-D28K-immunoreactive cells and fibres in the human amygdaloid complex. Neuroscience 75, 421-443.
96. Spacek J, Harris KM (2004) Trans-endocytosis via spinules in adult rat hippocampus. J Neurosci 24, 4233-4241.
97. Spruston N, Häusser M, Stuart G (2013) Information processing in dendrites and spines. In: Fundamental Neuroscience. (eds Squire LR, Berg D, Bloom FE, et al.), pp. 231-260, Waltham: Elsevier.
98. Stewart MG, Popov VI, Kraev IV, et al. (2014) Structure and complexity of the synapse and dendritic spine. In: The Synapse. (eds Pickel V, Segal M), pp. 1-20, Kidlington: Academic Press.
99. Sun Q, Srinivas KV, Sotayo A, et al. (2014) Dendritic Na+ spikes enable cortical input to drive action potential output from hippocampal CA2 pyramidal neurons. eLIFE 3, e04551.
100. Tao-Cheng J-H, Dosemeci A, Gallant PE, et al. (2009) Rapid turnover of spinules at synaptic terminals. Neuroscience 160, 42-50.
101. Tarrant SB, Routtenberg A (1977) The synaptic spinule in the dendritic spine: electron microscopic study of the hippocampal dentate gyrus. Tissue Cell 9, 461-473.
102. Tonnesen J, Katona G, Rózsa B, et al. (2014) Spine neck plasticity regulates compartmentalization of synapses. Nat Neurosci 17, 678-685.
103. Torres-Platas SG, Hercher C, Davoli MA, et al. (2011) Astrocytic hypertrophy in anterior cingulate white matter of depressed suicides. Neuropsychopharmacology 36, 2650-2658.
104. Uematsu A, Matsui M, Tanaka C, et al. (2012) Developmental trajectories of amygdala and hippocampus from infancy to early adulthood in healthy individuals. PLoS One 7, e46970.
105. Vargas-Barroso V, Larriva-Sahd J (2013) A cytological and experimental study of the neuropil and primary olfactory afferences to the piriform cortex. Anat Rec 296, 1297-1316.
106. Verzi DW, Noris OY (2009) A compartmental model for activity-dependent dendritic spine branching. Bull Math Biol 71, 1048-1072.
107. Yilmazer-Hanke DM (2012) Amygdala. In: The Human Nervous System. (eds Paxinos G, Mai J), pp. 759-834, San Diego, CA: Elsevier.
108. Yuste R (2011) Dendritic spine and distributed circuits. Neuron 71, 772-781.
109. Yuste R (2013) Electrical compartmentalization in dendritic spines. Annu Rev Neurosci 36, 429-449.
110. Zald DH, Pardo JV (1997) Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. Proc Natl Acad Sci USA 94, 4119-4124.
111. van der Zee EA (2015) Synapses, spines and kinases in mammalian learning and memory, and the impact of aging. Neurosci Biobehav Rev. 50, 77-85.