Retrieval of contextual memories increases activity-regulated cytoskeleton-associated protein in the amygdala and hippocampus

Brain Structure and Function

Volumn 218, Issue 5, 2013, Pages 1177-1196

  Figge, David A ^a   Rahman, Ihteshamur ^a   Dougherty, Philip J ^a   Rademacher, David J ^a,b  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Activity regulated cytoskeleton associated protein; Amphetamine; Amygdala; Classical conditioning; Conditioned place preference; Hippocampus

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; CENTRAL NUCLEUS (AMYGDALA); CONTEXTUAL MEMORY; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; LATERAL AMYGDALA; LOCOMOTION; MALE; MEMORY; NONHUMAN; PLACE PREFERENCE; PRIMARY AUDITORY CORTEX; PRIORITY JOURNAL; RAT; RECALL; SYNAPSE;

AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; CYTOSKELETAL PROTEINS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MEMORY; MENTAL RECALL; MICROSCOPY, ELECTRON; NERVE TISSUE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84883143064     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-012-0453-y     Document Type: Article

References (95)

1. Beaulieu C, Somogyi P (1990) Targets and quantitative distribution of GABAergic synapses in the visual cortex of the cat. Eur J Neurosci 2(4):296-303
2. Bothwell S, Meredith GE, Phillips J, Staunton H, Doherty C, Grigorenko E, Glazier S, Deadwyler SA, O'Donovan CA, Farrell M (2001) Neural hypertrophy in the neocortex of patients with temporal lobe epilepsy. J Neurosci 21(13):4789-4800
3. Brinley-Reed M, Mascagni F, McDonald AJ (1995) Synaptology of prefrontal cortical projections to the basolateral amygdala: an electron microscopic study in the rat. Neurosci Lett 202(1-2):45-48
4. Calverley RK, Bedi KS, Jones DG (1988) Estimation of the numerical density of synapses in rat neocortex: comparison of the 'disector' with an 'unfolding' method. J Neurosci Methods 23(3):195-205
5. Carlsen J, Heimer L (1986) A correlated light and electron microscopic immunocytochemical study of cholinergic terminals and neurons in the rat amygdaloid body with special emphasis on the basolateral amygdaloid nucleus. J Comp Neurol 244(1):121-136
6. Daberkow DP, Riedy MD, Kesner RP, Keefe KA (2007) Arc mRNA induction in striatal efferent neurons associated with response learning. Eur J Neurosci 26(1):228-241
7. Day M, Wang Z, Ding J, An X, Ingham CA, Shering AF, Wokosin D, Ilijic E, Sun Z, Sampson AR, Mugnaini E, Deutch AY, Sesack SR, Arbuthnott GW, Surmeier DJ (2006) Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat Neurosci 9(2):251-259
8. De Groot DM (1988) Comparison of methods for the estimation of the thickness of ultrathin tissue sections. J Microsc 151(Pt 1):23-42
9. de Groot DM, Bierman EP (1986) A critical evaluation of methods for estimating the numerical density of synapses. J Neurosci Methods 18(1-2):79-101
10. Dragunow M, Peterson MR, Robertson HA (1987) Presence of c-fos-like immunoreactivity in the adult rat brain. Eur J Pharmacol 135(1):113-114
11. Dudai Y, Eisenberg M (2004) Rites of passage of the engram: reconsolidation and the lingering consolidation hypothesis. Neuron 44(1):93-100
12. Everitt BJ, Morris KA, O'Brien A, Robbins TW (1991) The basolateral amygdala-ventral striatal system and conditioned place preference: further evidence of limbic-striatal interactions underlying reward-related processes. Neuroscience 42(1):1-18
13. Ferbinteanu J, McDonald RJ (2001) Dorsal/ventral hippocampus, fornix, and conditioned place preference. Hippocampus 11(2):187-200
14. Fujimoto T, Tanaka H, Kumamaru E, Okamura K, Miki N (2004) Arc interacts with microtubules/microtubule-associated protein 2 and attenuates microtubule-associated protein 2 immunoreactivity in the dendrites. J Neurosci Res 76(1):51-63
15. Geinisman Y (2000) Structural synaptic modifications associated with hippocampal LTP and behavioral learning. Cereb Cortex 10(10):952-962
16. Geinisman Y, Berry RW, Disterhoft JF, Power JM, Van der Zee EA (2001) Associative learning elicits the formation of multiple-synapse boutons. J Neurosci 21(15):5568-5573
17. Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Møller A, Nielson K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A, West MJ (1988) The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96(10):857-881
18. Guzowski JF, McNaughton BL, Barnes CA, Worley PF (1999) Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 2(12):1120-1124
19. Guzowski JF, Lyford GL, Stevenson GD, Houston FP, McGaugh JL, Worley PF, Barnes CA (2000) Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 20(11):3993-4001
20. Guzowski JF, Setlow B, Wagner EK, McGaugh JL (2001) Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J Neurosci 21(14):5089-5098
21. Hearing MC, Schochet TL, See RE, McGinty JF (2010) Context-driven cocaine-seeking in abstinent rats increases activity-regulated gene expression in the basolateral amygdala and dorsal hippocampus differentially following short and long periods of abstinence. Neuroscience 170(2):570-579
22. Helmstetter FJ, Bellgowan PS (1994) Effects of muscimol applied to the basolateral amygdala on acquisition and expression of contextual fear conditioning in rats. Behav Neurosci 108(5):1005-1009
23. Hetzel A, Meredith GE, Rademacher DJ, Rosenkranz JA (2012) Effect of amphetamine place conditioning on excitatory synaptic events in the basolateral amygdala ex vivo. Neuroscience 206:7-16
24. Holland PC, Bouton ME (1999) Hippocampus and context in classical conditioning. Curr Opin Neurobiol 9(2):195-202
25. Honecker H, Coper H (1975) Kinetics and metabolism of amphetamine in the brain of rats of different ages. Naunyn Schmiedebergs Arch Pharmacol 291(2):111-121
26. Hsu EH, Schroeder JP, Packard MG (2002) The amygdala mediates memory consolidation for an amphetamine conditioned place preference. Behav Brain Res 129(1-2):93-100
27. Hung AC, Huang HM, Tsay HJ, Lin TN, Kuo JS, Sun SH (2000) ATP-stimulated c-fos and zif268 mRNA expression is inhibited by chemical hypoxia in a rat brain-derived type 2 astrocyte cell line, RBA-2. J Cell Biochem 77(2):323-332
28. Hunter A, Stewart MG (1993) Long-term increases in the numerical density of synapses in the chick lobus parolfactorius after passive avoidance training. Brain Res 605(2):251-255
29. Ingham CA, Hood SH, Taggart P, Arbuthnott GW (1998) Plasticity of synapses in the rat neostriatum after unilateral lesion of the nigrostriatal dopaminergic pathway. J Neurosci 18(12):4732-4743
30. Ito R, Robbins TW, McNaughton BL, Everitt BJ (2006) Selective excitotoxic lesions of the hippocampus and basolateral amygdala have dissociable effects on appetitive cue and place conditioning based on path integration in a novel Y-maze procedure. Eur J Neurosci 23(11):3071-3080
31. Jeffery KJ, Anderson MI, Hayman R, Chakraborty S (2004) A proposed architecture for the neural representation of spatial context. Neurosci Biobehav Rev 28(2):201-218
32. Kelly MP, Deadwyler SA (2002) Acquisition of a novel behavior induces higher levels of Arc mRNA than does overtrained performance. Neuroscience 110(4):617-626
33. Kelly MP, Deadwyler SA (2003) Experience-dependent regulation of the immediate-early gene arc differs across brain regions. J Neurosci 23(16):6443-6451
34. Kolb B, Teskey GC (2012) Age, experience, injury, and the changing brain. Dev Psychobiol 54(3):311-325
35. Kozell LB, Meshul CK (2001) The effects of acute or repeated cocaine administration on nerve terminal glutamate within the rat mesolimbic system. Neuroscience 106(1):16-25
36. Kozell LB, Meshul CK (2004) Nerve terminal glutamate immunoreactivity in the rat nucleus accumbens and ventral tegmental area after a short withdrawal from cocaine. Synapse 51(4):224-232
37. Kuo YM, Liang KC, Chen HH, Cherng CG, Lee HT, Lin Y, Huang AM, Liao RM, Yu L (2007) Cocaine- but not methamphetamine-associated memory requires de novo protein synthesis. Neurobiol Learn Mem 87(1):93-100
38. Lanahan A, Worley P (1998) Immediate-early genes and synaptic function. Neurobiol Learn Mem 70(1-2):37-43
39. Li R, Nishijo H, Wang Q, Uwano T, Tamura R, Ohtani O, Ono T (2001) Light and electron microscopic study of cholinergic and noradrenergic elements in the basolateral nucleus of the rat amygdala: evidence for interactions between the two systems. J Comp Neurol 439(4):411-425
40. Link W, Konietzko U, Kauselmann G, Krug M, Schwanke B, Frey U, Kuhl D (1995) Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc Natl Acad Sci USA 92(12):5734-5738
41. Lyford GL, Yamagata K, Kaufmann WE, Barnes CA, Sanders LK, Copeland NG, Gilbert DJ, Jenkins NA, Lanahan AA, Worley PF (1995) Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14(2):433-445
42. McCutcheon JE, Marinelli M (2009) Age matters. Eur J Neurosci 29(5):997-1014
43. McDonald AJ, Betette RL (2001) Parvalbumin-containing neurons in the rat basolateral amygdala: morphology and co-localization of Calbindin-D(28 k). Neuroscience 102(2):413-425
44. McDonald AJ, Mascagni F (2001) Colocalization of calcium-binding proteins and GABA in neurons of the rat basolateral amygdala. Neuroscience 105(3):681-693
45. Moga DE, Calhoun ME, Chowdhury A, Worley P, Morrison JH, Shapiro ML (2004) Activity-regulated cytoskeletal-associated protein is localized to recently activated excitatory synapses. Neuroscience 125(1):7-11
46. Mokin M, Lindahl JS, Keifer J (2006) Immediate-early gene-encoded protein Arc is associated with synaptic delivery of GluR4-containing AMPA receptors during in vitro classical conditioning. J Neurophysiol 95(1):215-224
47. Morshedi MM, Rademacher DJ, Meredith GE (2009) Increased synapses in the medial prefrontal cortex are associated with repeated amphetamine administration. Synapse 63(2):126-135
48. Mouton PR (2002) Principles and practices of unbiased stereology: an introduction for bioscientists. The Johns Hopkins University Press, Baltimore
49. Mueller D, Stewart J (2000) Cocaine-induced conditioned place preference: reinstatement by priming injections of cocaine after extinction. Behav Brain Res 115(1):39-47
50. Mueller D, Perdikaris D, Stewart J (2002) Persistence and drug-induced reinstatement of a morphine-induced conditioned place preference. Behav Brain Res 136(2):389-397
51. Muller J, Corodimas KP, Fridel Z, LeDoux JE (1997) Functional inactivation of the lateral and basal nuclei of the amygdala by muscimol infusion prevents fear conditioning to an explicit conditioned stimulus and to contextual stimuli. Behav Neurosci 111(4):683-691
52. Muller JF, Mascagni F, McDonald AJ (2005) Coupled networks of parvalbumin- immunoreactive interneurons in the rat basolateral amygdala. J Neurosci 25(32):7366-7376
53. Muller JF, Mascagni F, McDonald AJ (2007) Postsynaptic targets of somatostatin-containing interneurons in the rat basolateral amygdala. J Comp Neurol 500(3):513-529
54. Muller JF, Mascagni F, McDonald AJ (2009) Dopaminergic innervation of pyramidal cells in the rat basolateral amygdala. Brain Struct Funct 213(3):275-288
55. Nicholson DA, Geinisman Y (2009) Axospinous synaptic subtype-specific differences in structure, size, ionotropic receptor expression, and connectivity in apical dendritic regions of rat hippocampal CA1 pyramidal neurons. J Comp Neurol 512(3):399-418
56. Nikam SS, Tennekoon GI, Christy BA, Yoshino JE, Rutkowski JL (1995) The zinc finger transcription factor Zif268/Egr-1 is essential for Schwann cell expression of the p75 NGF receptor. Mol Cell Neurosci 6(4):337-348
57. O'Donnell P, Grace AA (1997) Cortical afferents modulate striatal gap junction permeability via nitric oxide. Neuroscience 76(1):1-5
58. Olmstead MC, Franklin KB (1997) The development of a conditioned place preference to morphine: effects of microinjections into various CNS sites. Behav Neurosci 111(6):1324-1334
59. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic Press, New York
60. Peters A, Palay SL, Webster HD (1991) The fine structure of the nervous system: neurons and their supporting cells. Oxford University Press, New York
61. Pinard R, Benfares J, Lanoir J (1991) Electron microscopic study of GABA-immunoreactive neuronal processes in the superficial gray layer of the rat superior colliculus: their relationships with degenerating retinal nerve endings. J Neurocytol 20(4):262-276
62. Pinard CR, Muller JF, Mascagni F, McDonald AJ (2008) Dopaminergic innervation of interneurons in the rat basolateral amygdala. Neuroscience 157(4):850-863
63. Pintchovski SA, Peebles CL, Kim HJ, Verdin E, Finkbeiner S (2009) The serum response factor and a putative novel transcription factor regulate expression of the immediate-early gene Arc/Arg3.1 in neurons. J Neurosci 29(5):1525-1537
64. Plath N, Ohana O, Dammermann B, Errington ML, Schmitz D, Gross C, Mao X, Engelsberg A, Mahlke C, Welzl H, Kobalz U, Strawrakakis A, Fernandez E, Waltereit R, Bick-Sander A, Therstappen E, Cooke SF, Blanquet V, Wurst W, Salmen B, Bösl MR, Lipp HP, Grant SG, Bliss TV, Wolfer DP, Kuhl D (2006) Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52(3):437-444
65. Rademacher DJ, Kovacs B, Shen F, Napier TC, Meredith GE (2006) The neural substrates of amphetamine conditioned place preference: implications for the formation of conditioned stimulus-reward associations. Eur J Neurosci 24(7):2089-2097
66. Rademacher DJ, Napier TC, Meredith GE (2007) Context modulates the expression of conditioned motor sensitization, cellular activation and synaptophysin immunoreactivity. Eur J Neurosci 26(9):2661-2668
67. Rademacher DJ, Rosenkranz JA, Morshedi MM, Sullivan EM, Meredith GE (2010) Amphetamine-associated contextual learning is accompanied by structural and functional plasticity in the basolateral amygdala. J Neurosci 30(13):4676-4686
68. Ramírez-Amaya V, Vazdarjanova A, Mikhael D, Rosi S, Worley PF, Barnes CA (2005) Spatial exploration-induced Arc mRNA and protein expression: evidence for selective, network-specific reactivation. J Neurosci 25(7):1761-1768
69. Robinson TE, Berridge KC (2000) The psychology and neurobiology of addiction: an incentive-sensitization view. Addiction 95(Suppl 2):S91-S117
70. Rudy JW, Sutherland RJ (1995) Configural association theory and the hippocampal formation: an appraisal and reconfiguration. Hippocampus 5(5):375-389
71. Sadler R, Herzig V, Schmidt WJ (2007) Repeated treatment with the NMDA antagonist MK-801 disrupts reconsolidation of memory for amphetamine-conditioned place preference. Behav Pharmacol 18(7):699-703
72. Schiltz CA, Kelley AE, Landry CF (2005) Contextual cues associated with nicotine administration increase arc mRNA expression in corticolimbic areas of the rat brain. Eur J Neurosci 21(6):1703-1711
73. Schroeder JP, Packard MG (2003) Systemic or intra-amygdala injections of glucose facilitate memory consolidation for extinction of drug-induced conditioned reward. Eur J Neurosci 17(7):1482-1488
74. Shen F, Meredith GE, Napier TC (2006) Amphetamine-induced place preference and conditioned motor sensitization requires activation of tyrosine kinase receptors in the hippocampus. J Neurosci 26(43):11041-11051
75. Shepherd JD, Bear MF (2011) New views of Arc, a master regulator of synaptic plasticity. Nat Neurosci 14(3):279-284
76. Small JV (1968) Measurement of section thickness, In: Fourth European regional conference on electron microscopy, Rome, Italy
77. Somogyi P, Soltész I (1986) Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidase-filled basket cells and clutch cells in the cat's visual cortex. Neuroscience 19(4):1051-1065
78. Sterio DC (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134(Pt 2):127-136
79. Steward O (1995) Targeting of mRNAs to subsynaptic microdomains in dendrites. Curr Opin Neurobiol 5(1):55-61
80. Steward O, Worley PF (2001) A cellular mechanism for targeting newly synthesized mRNAs to synaptic sites on dendrites. Proc Natl Acad Sci USA 98(13):7062-7068
81. Steward O, Wallace CS, Lyford GL, Worley PF (1998) Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21(4):741-751
82. Tan A, Moratalla R, Lyford GL, Worley P, Graybiel AM (2000) The activity-regulated cytoskeletal-associated protein arc is expressed in different striosome-matrix patterns following exposure to amphetamine and cocaine. J Neurochem 74(5):2074-2078
83. Teber I, Köhling R, Speckmann EJ, Barnekow A, Kremerskothen J (2004) Muscarinic acetylcholine receptor stimulation induces expression of the activity-regulated cytoskeleton-associated gene (ARC). Brain Res Mol Brain Res 121(1-2):131-136
84. Toni N, Buchs PA, Nikonenko I, Bron CR, Muller D (1999) LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402(6760):421-425
85. Toni N, Buchs PA, Nikonenko I, Povilaitite P, Parisi L, Muller D (2001) Remodeling of synaptic membranes after induction of long-term potentiation. J Neurosci 21(16):6245-6251
86. van den Pol AN (1991) Glutamate and aspartate immunoreactivity in hypothalamic presynaptic axons. J Neurosci 11(7):2087-2101
87. Vazdarjanova A, Ramírez-Amaya V, Insel N, Plummer TK, Rosi S, Chowdhury S, Mikhael D, Worley PF, Guzowski JF, Barnes CA (2006) Spatial exploration induces ARC, a plasticity-related immediate-early gene, only in calcium/calmodulin-dependent protein kinase II-positive principal excitatory and inhibitory neurons of the rat forebrain. J Comp Neurol 498(3):317-329
88. Wallace CS, Lyford GL, Worley PF, Steward O (1998) Differential intracellular sorting of immediate early gene mRNAs depends on signals in the mRNA sequence. J Neurosci 18(1):26-35
89. Wang JQ, McGinty JF (1995) Alterations in striatal zif/268, preprodynorphin and preproenkephalin mRNA expression induced by repeated amphetamine administration in rats. Brain Res 673(2):262-274
90. Wang H, Pickel VM (2004) Activity-regulated cytoskeleton-associated protein Arc is targeted to dendrites and coexpressed with mu-opioid receptors in postnatal rat caudate-putamen nucleus. J Neurosci Res 77(3):323-333
91. White NM (1996) Addictive drugs as reinforcers: multiple partial actions on memory systems. Addiction 91(7):921-949 (Discussion 951-965)
92. Woodruff AR, Monyer H, Sah P (2006) GABAergic excitation in the basolateral amygdala. J Neurosci 26(46):11881-11887
93. Waung MW, Pfeiffer BE, Nosyreva ED, Ronesi JA, Huber KM (2008) Rapid translation of Arc/Arc3.1 selectively mediates mGluR-dependent LTD through persistent increases in AMPAR endocytosis rate. Neuron 59(1):84-97
94. Zhang WP, Guzowski JF, Thomas SA (2005) Mapping neuronal activation and the influence of adrenergic signaling during contextual memory retrieval. Learn Mem 12(3):239-247
95. Zhou W, Mailloux AW, Jung BJ, Edmunds HS Jr, McGinty JF (2004) GABAB receptor stimulation decreases amphetamine-induced behavior and neuropeptide gene expression in the striatum. Brain Res 1004(1-2):18-28