AMPA receptor facilitation accelerates fear learning without altering the level of conditioned fear acquired

Journal of Neuroscience

Volumn 17, Issue 15, 1997, Pages 5928-5935

  Rogan, Michael T ^a   Stäubli, Ursula V ^a   LeDoux, Joseph E ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

AMPA receptors; Amygdala; Fear; Glutamate; Learning; NMDA receptors

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONDITIONING; CONTROLLED STUDY; DISSOCIATION; FACILITATION; FEAR; INFORMATION PROCESSING; LEARNING; LOCOMOTION; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0342601397     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.17-15-05928.1997     Document Type: Article

References (47)

1. Arai A, Lynch G (1992) Factors regulating the magnitude of long-term potentiation induced by theta pattern stimulation. Brain Res 598:173-184.
2. Arai A, Kessler M, Xiao P, Ambros-Ingerson J, Rogers G, Lynch G (1994) A centrally active drug that modulates AMPA receptor gated currents. Brain Res 638:343-346.
3. Arai A, Kessler M, Rogers G, Lynch G (1996) Effects of a memory-enhancing drug on DL-α-amino-3-hydroxy-5-methyl-4-isoxazoleproionic acid receptor currents and synaptic transmission in hippocampus. J Pharmacol Exp Ther 278:627-638.
4. Barnes CA, Erickson CA, Davis S, McNaughton BL (1995) Hippocampal synaptic enhancement as a basis for learning and memory: a selected review of current evidence from behaving animals. In: Brain and memory: modulation and mediation of neuroplasticity (McGaugh JL, Weinberger NM, Lynch G, eds), pp 259-276. New York: Oxford UP.
5. Blanchard RJ, Blanchard DC (1969a) Crouching as an index of fear. J Comp Physiol Psychol 67:370-375.
6. Blanchard RJ, Blanchard DC (1969b) Passive and active reactions to fear-eliciting stimuli. J Comp Physiol Psychol 68:129-135.
7. Bliss TVP, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
8. Bouton ME, Bolles RC (1980) Conditioned fear assessed by freezing and by the suppression of three different baselines. Anim Learn Behav 8:429-434.
9. Brown TH, Chapman PF, Kairiss EW, Keenan CL (1988) Long-term synaptic potentiation. Science 242:724-728.
10. Campeau S, Miserendino MJD, Davis M (1992) Intra-amygdala infusion of the N-methyl-D-aspartate receptor antagonist AP5 blocks acquisition but not expression of fear-potentiated startle to an auditory conditioned stimulus. Behav Neurosci 106:569-574.
11. Chapman PF, Kairiss EW, Keenan CL, Brown TH (1990) Long-term synaptic potentiation in the amygdala. Synapse 6:271-278.
12. Clugnet MC, LeDoux JE (1990) Synaptic plasticity in fear conditioning circuits: induction of LTP in the lateral nucleus of the amygdala by stimulation of the medial geniculate body. J Neurosci 10:2818-2824.
13. Collingridge GL, Kehl SJ, McLennan H (1983) Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol (Lond) 334:33-46.
14. Davis M (1992) The role of the amygdala in conditioned fear. In: The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction (Aggleton JP, ed), pp 255-306. New York: Wiley.
15. Fanselow MS (1980) Conditional and unconditional components of post-shock freezing. Pavlov J Biol Sci 15:177-182.
16. Fanselow MS, Kim JJ, Yipp J, De Oca B (1994) Differential effects of the N-methyl-D-aspartate antagonist DL-2-amino-5-phosphonovalerate on acquisition of fear of auditory and contextual cues. Behav Neurosci 108:235-240.
17. Farb C, Aoki C, Milner T, Kaneko T, LeDoux J (1992) Glutamate immunoreactive terminals in the lateral amygdaloid nucleus: a possible substrate for emotional memory. Brain Res 593:145-158.
18. Farb CR, Aoki C, LeDoux JE (1995) Differential localization of NMDA and AMPA receptor subunits in the lateral and basal nuclei of the amygdala: a light and electron microscopic study. J Comp Neurol 362:86-108.
19. Granger R, Stäubli U, Davis M, Perez Y, Nilsson L, Rogers GA, Lynch G (1993) A drug that facilitates glutamaturgic transmission reduces exploratory activity and improves performance in a learning-dependent task. Synapse 15:326-329.
20. Gray JA (1987) The psychology of fear and stress, Vol 2. New York: Cambridge UP.
21. Kim JJ, DeCola JP, Landeira-Fernandez J, Fanselow MS (1991) N-methyl-D-aspartate receptor antagonist APV blocks acquisition but not expression of fear conditioning. Behav Neurosci 105:126-133.
22. Kim M, Campeau S, Falls WA, Davis M (1993) Infusion of the non-NMDA receptor antagonist CNQX into the amygdala blocks the expression fear-potentiated startle. Behav Neural Biol 59:5-8.
23. Klein SB (1987) Learning: Principles and applications. New York: McGraw-Hill.
24. Larson J, Lieu T, Petchpradub V, LeDuc B, Ngo H, Rogers GA, Lynch G (1995) Facilitation of olfactory learning by a modulator of AMPA receptors. J Neurosci 15:8023-8030.
25. LeDoux JE, Farb CR (1991) Neurons of the acoustic thalamus that project to the amygdala contain glutamate. Neurosci Lett 134:145-149.
26. LeDoux JE, Sakaguchi A, Reis DJ (1984) Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned by acoustic stimuli. J Neurosci 4:683-698.
27. LeDoux JE, Cicchetti P, Xagoraris A, Romanski LM (1990) The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 10:1062-1069.
28. Li X, Phillips RG, LeDoux JE (1995) NMDA and non-NMDA receptors contribute to synaptic transmission between the medial geniculate body and the lateral nucleus of the amygdala. Exp Brain Res 105:87-100.
29. Li XF, Stutzmann GE, LeDoux JL (1996) Convergent but temporally separated inputs to lateral amygdala neurons from the auditory thalamus and auditory cortex use different postsynaptic receptors: in vivo intracellular and extracellular recordings in fear conditioning pathways. Learn Memory 3:229-242.
30. Lynch G (1986) Synapses, circuits, and the beginnings of memory. Cambridge, MA: MIT.
31. Mackintosh NJ (1975) The psychology of animal learning. New York: Academic.
32. Malenka RC, Nicoll, RA (1993) NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci 16:521-527.
33. Maren S, Fanselow MS (1995) Synaptic plasticity in the basoateral amygdala induced by hippocampal formation stimulation in vivo. J Neurosci 15:7548-7564.
34. Maren S, Fanselow MS (1996) The amygdala and fear conditioning: has the nut been cracked? Neuron 16:237-240.
35. Maren S, Aharonov G, Stote DL, Fanselow MS (1996) N-Methyl-D-aspartate receptors in the basolateral amygdala are required for both acquisition and expression of the conditional fear in rats. Behav Neurosci 110:1365-1374.
36. Miserendino MJD, Sananes CB, Melia KR, Davis M (1990) Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala. Nature 345:716-718.
37. Phillips RG, LeDoux JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106:274-285.
38. Rescorla RA, Wagner AR (1972) A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. In: Classical conditioning II: current research and theory (Black AA, Prokasy WF, eds), pp 64-99. New York: Appleton-Century-Crofts.
39. Rogan MT, LeDoux JE (1995a) LTP is accompanied by commensurate enhancement of auditory-evoked responses in a fear conditioning circuit. Neuron 15:127-136.
40. Rogan MT, LeDoux JE (1995b) Intra-amygdala infusion of APV blocks both auditory evoked potentials in the lateral amygdala and thalamoamygdala transmission, but spares cortico-amygdala transmission. Soc Neurosci Abstr 21:1930.
41. Rogan MT, LeDoux JE (1996) Emotion: Systems, cells, synaptic plasticity. Cell 85:469-475.
42. Shors TJ, Servatius RJ, Thompson RF, Rogers G, Lynch G (1995) Enhanced glutamatergic neurotransmission facilitates classical conditioning in the freely moving rat. Neurosci Lett 186:153-156.
43. Stäubli UV (1995) Parallel properties of long-term potentiation and memory. In: Brain and memory: modulation and mediation of neuroplasticity (McGaugh JL, Weinberger NM, Lynch G, eds), pp 303-318. New York: Oxford UP.
44. Stäubli U, Izrael Z, Xu F (1996) Remembrance of odors past: enhancement via central facilitation of glutamate receptors. Behav Neurosci 110:1067-1073.
45. Stäubli U, Rogers G, Lynch G (1994a) Facilitation of glutamate receptors enhances memory. Proc Natl Acad Sci USA 91:777-781.
46. Stäubli U, Perez Y, Xu F, Rogers G, Ingvar M, Stone-Elander S, Lynch G (1994b) Centrally active modulators of glutamate receptors facilitate the induction of long-term potentiation in vivo. Proc Natl Acad Sci USA 91:1158-1162.
47. Teyler JT (1992) Long-term potentiation and memory. In: Neuroscience year: Suppl 2, encyclopedia of neuroscience (Smith B, Adelman G, eds), pp 91-93. Cambridge, MA: Brikhauser Boston.