 |
Previous Article | Next Article 
Journal of Neuroscience, Vol 15, 2312-2327, Copyright © 1995 by Society for Neuroscience
Involvement of subcortical and cortical afferents to the lateral nucleus of the amygdala in fear conditioning measured with fear- potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli
S Campeau and M Davis
Department of Psychology, Yale University School of Medicine, New Haven, Connecticut.
The goal of this work was to test the involvement, in fear conditioning, of
afferents to the lateral nucleus of the amygdala originating from the
auditory thalamus, auditory cortex, and perirhinal area. The acoustic
startle reflex was used as the behavioral index of conditioning because it
is reliably enhanced in the presence of a conditioned stimulus (CS)
previously paired with a footshock. Auditory and visual CSs were used to
assess the modality specificity of lesions to the above brain areas. Pre-
or posttraining lesions of the entire auditory thalamus including the
ventral, dorsal, and medial divisions of the medial geniculate body, the
posterior intralaminar nucleus, and the suprageniculate nucleus, completely
blocked fear-potentiated startle to the auditory CS, but had no effect on
fear-potentiated startle to the visual CS. Posttraining lesions mostly
restricted to the ventral and dorsal divisions of the medial geniculate
body specifically disrupted fear-potentiated startle to the auditory CS.
However, retraining in rats sustaining ventral and dorsal medial geniculate
body lesions led to reliable fear-potentiated startle to the auditory CS.
Posttraining lesions mostly restricted to the medial division of the medial
geniculate body, posterior intralaminar, and suprageniculate nuclei did not
disrupt fear-potentiated startle. These results indicate that the auditory
thalamus is specifically involved, through either its direct or indirect
amygdaloid afferents, in fear conditioning to auditory CSs. Pre- or
posttraining lesions mostly restricted to the primary auditory cortex did
not reliably attenuate fear-potentiated startle to the auditory or visual
CSs. Extensive posttraining lesions of the perirhinal area (including
secondary auditory cortices), but not its rostral aspect alone, blocked
fear-potentiated startle to both CSs. However, reliable potentiated startle
was observed to both CSs following similarly extensive pretraining lesions
of the perirhinal area. Because post- but not pretraining lesions of the
perirhinal area blocked fear-potentiated startle nonspecifically, at least
with regard to auditory and visual CSs, the results are consistent with the
involvement of the perirhinal area in general memory functions such as
information storage or retrieval. Alternatively, the secondary auditory
and/or perirhinal cortices might function as multimodal sensory relays to
the amygdala.
This article has been cited by other articles:

|
 |

|
 |
 
F. Z. Nagy and D. Pare
Timing of Impulses From the Central Amygdala and Bed Nucleus of the Stria Terminalis to the Brain Stem
J Neurophysiol,
December 1, 2008;
100(6):
3429 - 3436.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. M. Rodgers, A. M. Benison, A. Klein, and D. S. Barth
Auditory, Somatosensory, and Multisensory Insular Cortex in the Rat
Cereb Cortex,
December 1, 2008;
18(12):
2941 - 2951.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y.-Y. Huang, E. R. Kandel, and A. Levine
Chronic nicotine exposure induces a long-lasting and pathway-specific facilitation of LTP in the amygdala
Learn. Mem.,
August 6, 2008;
15(8):
603 - 610.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.-H. Han, A. P. Yiu, C. J. Cole, H.-L. Hsiang, R. L. Neve, and S. A. Josselyn
Increasing CREB in the auditory thalamus enhances memory and generalization of auditory conditioned fear
Learn. Mem.,
May 30, 2008;
15(6):
443 - 453.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B.-X. Pan, F. Vautier, W. Ito, V. Y. Bolshakov, and A. Morozov
Enhanced Cortico-Amygdala Efficacy and Suppressed Fear in Absence of Rap1
J. Neurosci.,
February 27, 2008;
28(9):
2089 - 2098.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. D. Cohen and M. A. Castro-Alamancos
Early Sensory Pathways for Detection of Fearful Conditioned Stimuli: Tectal and Thalamic Relays
J. Neurosci.,
July 18, 2007;
27(29):
7762 - 7776.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. A. Corcoran and G. J. Quirk
Activity in Prelimbic Cortex Is Necessary for the Expression of Learned, But Not Innate, Fears
J. Neurosci.,
January 24, 2007;
27(4):
840 - 844.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. A. Kodirov, S. Takizawa, J. Joseph, E. R. Kandel, G. P. Shumyatsky, and V. Y. Bolshakov
Synaptically released zinc gates long-term potentiation in fear conditioning pathways
PNAS,
October 10, 2006;
103(41):
15218 - 15223.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. J. Plessen, R. Bansal, H. Zhu, R. Whiteman, J. Amat, G. A. Quackenbush, L. Martin, K. Durkin, C. Blair, J. Royal, et al.
Hippocampus and Amygdala Morphology in Attention-Deficit/Hyperactivity Disorder.
Arch Gen Psychiatry,
July 1, 2006;
63(7):
795 - 807.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Anglada-Figueroa and G. J. Quirk
Lesions of the Basal Amygdala Block Expression of Conditioned Fear But Not Extinction
J. Neurosci.,
October 19, 2005;
25(42):
9680 - 9685.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Zhao and M. Davis
Fear-Potentiated Startle in Rats Is Mediated by Neurons in the Deep Layers of the Superior Colliculus/Deep Mesencephalic Nucleus of the Rostral Midbrain through the Glutamate Non-NMDA Receptors
J. Neurosci.,
November 17, 2004;
24(46):
10326 - 10334.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. H. Lindquist, L. E. Jarrard, and T. H. Brown
Perirhinal Cortex Supports Delay Fear Conditioning to Rat Ultrasonic Social Signals
J. Neurosci.,
April 7, 2004;
24(14):
3610 - 3617.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. SAH, E. S. L. FABER, M. LOPEZ DE ARMENTIA, and J. POWER
The Amygdaloid Complex: Anatomy and Physiology
Physiol Rev,
July 1, 2003;
83(3):
803 - 834.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. J. Howse, A. S. Squires, G. M. Martin, and D. M. Skinner
Perirhinal Cortex Lesions Impair Context Aversion Learning
Learn. Mem.,
May 1, 2003;
10(3):
161 - 167.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Kajiwara, I. Takashima, Y. Mimura, M. P. Witter, and T. Iijima
Amygdala Input Promotes Spread of Excitatory Neural Activity From Perirhinal Cortex to the Entorhinal-Hippocampal Circuit
J Neurophysiol,
April 1, 2003;
89(4):
2176 - 2184.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Poremba, R. C. Saunders, A. M. Crane, M. Cook, L. Sokoloff, and M. Mishkin
Functional Mapping of the Primate Auditory System
Science,
January 24, 2003;
299(5606):
568 - 572.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C.-H. Lin, C.-C. Lee, and P.-W. Gean
Involvement of a Calcineurin Cascade in Amygdala Depotentiation and Quenching of Fear Memory
Mol. Pharmacol.,
January 1, 2003;
63(1):
44 - 52.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. A. Marsh, Z. M. Fuzessery, C. D. Grose, and J. J. Wenstrup
Projection to the Inferior Colliculus from the Basal Nucleus of the Amygdala
J. Neurosci.,
December 1, 2002;
22(23):
10449 - 10460.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. G. Pelletier and D. Pare
Uniform Range of Conduction Times From the Lateral Amygdala to Distributed Perirhinal Sites
J Neurophysiol,
March 1, 2002;
87(3):
1213 - 1221.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. Rosenkranz and A. A. Grace
Cellular Mechanisms of Infralimbic and Prelimbic Prefrontal Cortical Inhibition and Dopaminergic Modulation of Basolateral Amygdala Neurons In Vivo
J. Neurosci.,
January 1, 2002;
22(1):
324 - 337.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Shi and M. Davis
Visual Pathways Involved in Fear Conditioning Measured with Fear-Potentiated Startle: Behavioral and Anatomic Studies
J. Neurosci.,
December 15, 2001;
21(24):
9844 - 9855.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. T. Blair, G. E. Schafe, E. P. Bauer, S. M. Rodrigues, and J. E. LeDoux
Synaptic Plasticity in the Lateral Amygdala: A Cellular Hypothesis of Fear Conditioning
Learn. Mem.,
September 1, 2001;
8(5):
229 - 242.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. Rosenkranz and A. A. Grace
Dopamine Attenuates Prefrontal Cortical Suppression of Sensory Inputs to the Basolateral Amygdala of Rats
J. Neurosci.,
June 1, 2001;
21(11):
4090 - 4103.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. R. Collins, J. G. Pelletier, and D. Pare
Slow and Fast (Gamma) Neuronal Oscillations in the Perirhinal Cortex and Lateral Amygdala
J Neurophysiol,
April 1, 2001;
85(4):
1661 - 1672.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Schauz and M. Koch
Blockade of NMDA Receptors in the Amygdala Prevents Latent Inhibition of Fear-Conditioning
Learn. Mem.,
November 1, 2000;
7(6):
393 - 399.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
J. C. Gewirtz and M. Davis
Using Pavlovian Higher-Order Conditioning Paradigms to Investigate the Neural Substrates of Emotional Learning and Memory
Learn. Mem.,
September 1, 2000;
7(5):
257 - 266.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
F. Clasca, A. Llamas, and F. Reinoso-Suarez
Cortical Connections of the Insular and Adjacent Parieto-temporal Fields in the Cat
Cereb Cortex,
April 1, 2000;
10(4):
371 - 399.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Kobayashi, Y. Noda, N. Matsushita, K. Nishii, H. Sawada, T. Nagatsu, D. Nakahara, R. Fukabori, Y. Yasoshima, T. Yamamoto, et al.
Modest Neuropsychological Deficits Caused by Reduced Noradrenaline Metabolism in Mice Heterozygous for a Mutated Tyrosine Hydroxylase Gene
J. Neurosci.,
March 15, 2000;
20(6):
2418 - 2426.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. Rosenkranz and A. A. Grace
Modulation of Basolateral Amygdala Neuronal Firing and Afferent Drive by Dopamine Receptor Activation In Vivo
J. Neurosci.,
December 15, 1999;
19(24):
11027 - 11039.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Sacchetti, C. A. Lorenzini, E. Baldi, G. Tassoni, and C. Bucherelli
Auditory Thalamus, Dorsal Hippocampus, Basolateral Amygdala, and Perirhinal Cortex Role in the Consolidation of Conditioned Freezing to Context and to Acoustic Conditioned Stimulus in the Rat
J. Neurosci.,
November 1, 1999;
19(21):
9570 - 9578.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Shi and M. Davis
Pain Pathways Involved in Fear Conditioning Measured with Fear-Potentiated Startle: Lesion Studies
J. Neurosci.,
January 1, 1999;
19(1):
420 - 430.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Poremba and M. Gabriel
Medial Geniculate Lesions Block Amygdalar and Cingulothalamic Learning-Related Neuronal Activity
J. Neurosci.,
November 1, 1997;
17(21):
8645 - 8655.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Campeau, H. Akil, and S. J. Watson
Lesions of the Medial Geniculate Nuclei Specifically Block Corticosterone Release and Induction of c-fos mRNA in the Forebrain Associated with Audiogenic Stress in Rats
J. Neurosci.,
August 1, 1997;
17(15):
5979 - 5992.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Stripling, S. F. Volman, and D. F. Clayton
Response Modulation in the Zebra Finch Neostriatum: Relationship to Nuclear Gene Regulation
J. Neurosci.,
May 15, 1997;
17(10):
3883 - 3893.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G.J. Quirk, J.L. Armony, J.C. Repa, X.-F. Li, and J.E. LeDoux
Emotional Memory: A Search for Sites of Plasticity
Cold Spring Harb Symp Quant Biol,
January 1, 1996;
61(0):
247 - 257.
[Abstract]
[PDF]
|
 |
|
|