The structure of Pavlovian fear conditioning in the amygdala

Brain Structure and Function

Volumn 218, Issue 6, 2013, Pages 1569-1589

  Bergstrom, Hadley C ^a   McDonald, Craig G ^b   Dey, Smita ^a   Tang, Haying ^a   Selwyn, Reed G ^a   Johnson, Luke R ^a  

^a Uniformed Services University of the Health Sciences   (United States)

^b GEORGE MASON UNIVERSITY   (United States)

Author keywords

Basal amygdala; Calcium calmodulin dependent protein kinase II (CAMKII); Consolidation; Cytoarchitecture; Dual labeling immunofluorescence; Fear; Fear learning; Lateral amygdala; Lateral ventricle; Magnetic resonance imaging (MRI); Mapping; Memory; Micro anatomy; Mitogen activated protein kinase (MAPK); Multiple discriminant analysis (MDA); Multivariate ANOVA (MANOVA); Network; Neural circuit; Organization; Principal cell type; Principal components analysis (PCA); Sprague Dawley rat; Stability; Topography

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL DENSITY; CONDITIONED REFLEX; CONTROLLED STUDY; CYTOARCHITECTURE; FEAR; FEMALE; FUNCTIONAL MORPHOLOGY; IN VITRO STUDY; IN VIVO STUDY; LEARNING; MALE; MEMORY CONSOLIDATION; MORPHOMETRICS; NERVE CELL PLASTICITY; NEUROANATOMY; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; TASK PERFORMANCE;

RATTUS;

AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; BODY WEIGHTS AND MEASURES; BRAIN MAPPING; CONDITIONING, CLASSICAL; FEAR; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MAGNETIC RESONANCE IMAGING; MALE; MEMORY; MITOGEN-ACTIVATED PROTEIN KINASE 1; PRINCIPAL COMPONENT ANALYSIS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84887259782     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-012-0478-2     Document Type: Article

References (55)

1. Bergstrom HC, McDonald CG, French HT, Smith RF (2008) Continuous nicotine administration produces selective, age-dependent structural alteration of pyramidal neurons from prelimbic cortex. Synapse 62(1):31-39
2. Bergstrom HC, McDonald CG, Johnson LR (2011) Pavlovian fear conditioning activates a common pattern of neurons in the lateral amygdala of individual brains. PLoS ONE 6(1):e15698
3. Bernard JF, Alden M, Besson JM (1993) The organization of the efferent projections from the pontine parabrachial area to the amygdaloid complex: a Phaseolus vulgaris leucoagglutinin (PHA-L) study in the rat. J Comp Neurol 329(2):201-229
4. Blair HT, Schafe GE, Bauer EP, Rodrigues SM, LeDoux JE (2001) Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. Learn Mem 8(5):229-242
5. Calandreau L, Desmedt A, Decorte L, Jaffard R (2005) A different recruitment of the lateral and basolateral amygdala promotes contextual or elemental conditioned association in Pavlovian fear conditioning. Learn Mem 12(4):383-388
6. Davis M (1992) The role of the amygdala in fear and anxiety. Annu Rev Neurosci 15:353-375
7. Davis S, Laroche S (2006) Mitogen-activated protein kinase/extracellular regulated kinase signalling and memory stabilization: a review. Genes Brain Behav 5(Suppl 2):61-72
8. de Smith MJ, Goodchild MF, Longly PA (2009) Geospatial Analysis. Matador, Leicester
9. Di Benedetto B, Kallnik M, Weisenhorn DM, Falls WA, Wurst W, Holter SM (2009) Activation of ERK/MAPK in the lateral amygdala of the mouse is required for acquisition of a fear-potentiated startle response. Neuropsychopharmacology 34(2):356-366
10. Doron NN, Ledoux JE (1999) Organization of projections to the lateral amygdala from auditory and visual areas of the thalamus in the rat. J Comp Neurol 412(3):383-409
11. Duvarci S, Nader K, LeDoux JE (2005) Activation of extracellular signal-regulated kinase- mitogen-activated protein kinase cascade in the amygdala is required for memory reconsolidation of auditory fear conditioning. Eur J Neurosci 21(1):283-289
12. Fanselow MS (1980) Conditioned and unconditional components of post-shock freezing. Pavlov J Biol Sci 15(4):177-182
13. Fanselow MS, LeDoux JE (1999) Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 23(2):229-232
14. Han JH, Kushner SA, Yiu AP, Cole CJ, Matynia A, Brown RA, Neve RL, Guzowski JF, Silva AJ, Josselyn SA (2007) Neuronal competition and selection during memory formation. Science 316(5823):457-460
15. Han JH, Kushner SA, Yiu AP, Hsiang HL, Buch T, Waisman A, Bontempi B, Neve RL, Frankland PW, Josselyn SA (2009) Selective erasure of a fear memory. Science 323(5920):1492-1496
16. Herry C, Trifilieff P, Micheau J, Luthi A, Mons N (2006) Extinction of auditory fear conditioning requires MAPK/ERK activation in the basolateral amygdala. Eur J Neurosci 24(1):261-269
17. Johnson LR, Ledoux JE (eds) (2004) The anatomy of fear: microcircuits of the lateral amygdala. In: Fear and anxiety: the benefits of translational research. American Psychiatric Publishing, Inc, Washington, DC
18. Johnson LR, LeDoux JE (2010) Amygdala Microcircuits. In: Shepherd GM, Grillner S (eds) Handbook of brain microcircuits. Oxford University Press, Oxford
19. Johnson LR, Hou M, Ponce-Alvarez A, Gribelyuk LM, Alphs HH, Albert L, Brown BL, Ledoux JE, Doyere V (2008) A recurrent network in the lateral amygdala: a mechanism for coincidence detection. Front Neural Circuits 2:3
20. Johnson LR, Ledoux JE, Doyere V (2009) Hebbian reverberations in emotional memory micro circuits. Front Neurosci 3(2):198-205
21. Jolliffe IT (2002) Principal component analysis, vol 2. Wiley Online Library, New York
22. Kim JJ, Fanselow MS (1992) Modality-specific retrograde amnesia of fear. Science 256(5057):675-677
23. Lamprecht R, LeDoux J (2004) Structural plasticity and memory. Nat Rev Neurosci 5(1):45-54
24. LeDoux JE, Cicchetti P, Xagoraris A, Romanski LM (1990a) The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 10(4):1062-1069
25. LeDoux JE, Farb C, Ruggiero DA (1990b) Topographic organization of neurons in the acoustic thalamus that project to the amygdala. J Neurosci 10(4):1043
26. LeDoux JE, Farb CR, Romanski LM (1991) Overlapping projections to the amygdala and striatum from auditory processing areas of the thalamus and cortex. Neurosci Lett 134(1):139-144
27. Maren S, Fanselow MS (1996) The amygdala and fear conditioning: has the nut been cracked? Neuron 16(2):237-240
28. Maren S, Quirk GJ (2004) Neuronal signalling of fear memory. Nat Rev Neurosci 5(11):844-852
29. McDonald AJ (1984) Neuronal organization of the lateral and basolateral amygdaloid nuclei in the rat. J Comp Neurol 222(4):589-606
30. McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol 55(3):257-332
31. McDonald AJ (2003) Is there an amygdala and how far does it extend? An anatomical perspective. Ann N Y Acad Sci 985:1-21
32. McDonald AJ, Muller JF, Mascagni F (2002) GABAergic innervation of alpha type II calcium/calmodulin-dependent protein kinase immunoreactive pyramidal neurons in the rat basolateral amygdala. J Comp Neurol 446(3):199-218
33. Nader K, Majidishad P, Amorapanth P, LeDoux JE (2001) Damage to the lateral and central, but not other, amygdaloid nuclei prevents the acquisition of auditory fear conditioning. Learn Mem 8(3):156-163
34. Nomura H, Nonaka A, Imamura N, Hashikawa K, Matsuki N (2011) Memory coding in plastic neuronal subpopulations within the amygdala. Neuroimage 60(1):153-161
35. Onishi BK, Xavier GF (2010) Contextual, but not auditory, fear conditioning is disrupted by neurotoxic selective lesion of the basal nucleus of amygdala in rats. Neurobiol Learn Mem 93(2):165-174
36. Pape HC, Pare D (2010) Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol Rev 90(2):419-463
37. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, 6th edn. Elsevier Academic Press, London
38. Phillips RG, LeDoux JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106(2):274-285
39. Pitkänen A (2000) Connectivity of the rat amygdaloid complex. In: Aggleton JP (ed) The amygdala, 2nd edn. Oxford University Press, New York
40. Quirk GJ, Repa C, LeDoux JE (1995) Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat. Neuron 15(5):1029-1039
41. Radley JJ, Farb CR, He Y, Janssen WG, Rodrigues SM, Johnson LR, Hof PR, LeDoux JE, Morrison JH (2007) Distribution of NMDA and AMPA receptor subunits at thalamo-amygdaloid dendritic spines. Brain Res 1134(1):87-94
42. Radwanska K, Nikolaev E, Knapska E, Kaczmarek L (2002) Differential response of two subdivisions of lateral amygdala to aversive conditioning as revealed by c-Fos and P-ERK mapping. NeuroReport 13(17):2241-2246
43. Reijmers LG, Perkins BL, Matsuo N, Mayford M (2007) Localization of a stable neural correlate of associative memory. Science 317(5842):1230-1233
44. Repa JC, Muller J, Apergis J, Desrochers TM, Zhou Y, LeDoux JE (2001) Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat Neurosci 4(7):724-731
45. Romanski LM, Clugnet MC, Bordi F, LeDoux JE (1993) Somatosensory and auditory convergence in the lateral nucleus of the amygdala. Behav Neurosci 107(3):444-450
46. Rumpel S, LeDoux J, Zador A, Malinow R (2005) Postsynaptic receptor trafficking underlying a form of associative learning. Science 308(5718):83-88
47. Schafe GE, Nadel NV, Sullivan GM, Harris A, LeDoux JE (1999) Memory consolidation for contextual and auditory fear conditioning is dependent on protein synthesis, PKA, and MAP kinase. Learn Mem 6(2):97-110
48. Schafe GE, Atkins CM, Swank MW, Bauer EP, Sweatt JD, LeDoux JE (2000) Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of pavlovian fear conditioning. J Neurosci 20(21):8177-8187
49. Schafe GE, Doyere V, LeDoux JE (2005) Tracking the fear engram: the lateral amygdala is an essential locus of fear memory storage. J Neurosci 25(43):10010-10014
50. Schafe GE, Swank MW, Rodrigues SM, Debiec J, Doyere V (2008) Phosphorylation of ERK/MAP kinase is required for long-term potentiation in anatomically restricted regions of the lateral amygdala in vivo. Learn Mem 15(2):55-62
51. Sweatt JD (2001) The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76(1):1-10
52. Thomas GM, Huganir RL (2004) MAPK cascade signalling and synaptic plasticity. Nat Rev Neurosci 5(3):173-183
53. Trogrlic L, Wilson YM, Newman AG, Murphy M (2011) Context fear learning specifically activates distinct populations of neurons in amygdala and hypothalamus. Learn Mem 18(10):678-687
54. Wilensky AE, Schafe GE, LeDoux JE (1999) Functional inactivation of the amygdala before but not after auditory fear conditioning prevents memory formation. J Neurosci 19((24)):RC48
55. Wilson YM, Murphy M (2009) A discrete population of neurons in the lateral amygdala is specifically activated by contextual fear conditioning. Learn Mem 16(6):357-361