Amygdala-dependent and amygdala-independent pathways for contextual fear conditioning

doi:10.1016/j.neuroscience.2007.04.026

Neuroscience

Volume 147, Issue 4, 29 July 2007, Pages 919-927

https://doi.org/10.1016/j.neuroscience.2007.04.026 Get rights and content

Abstract

The basolateral amygdala (BLA), consisting of the lateral and basal nuclei, is considered to be essential for fear learning. Using a temporary inactivation technique, we found that rats could acquire a context-specific long-term fear memory without the BLA but only if intensive overtraining was used. BLA-inactivated rats’ learning curves were characterized by slow learning that eventually achieved the same asymptotic performance as rats with the BLA functional. BLA inactivation abolished expression of overtrained fear when rats were overtrained with a functional BLA. However, BLA-inactivation had no effect on the expression of fear in rats that learned while the BLA was inactivated. These data suggest that there are primary and alternate pathways capable of mediating fear. Normally, learning is dominated by the more efficient primary pathway, which prevents learning in the alternate pathway. However, alternate pathways compensate when the dominant pathway is compromised.

Section snippets

Subjects

Male Long-Evans rats initially weighing 250–280 g were obtained from a commercial supplier (Harlan, Indianapolis, IN, USA). After arrival, the rats were housed individually in standard stainless-steel cages on a 12/-h light/dark cycle and were provided free access to food and tap water. After being housed, the rats were handled daily (60–90 s per rat) for 5 days to acclimate them to the experimenter. All procedures conformed to the U.S. National Research Council Guide to the Care and Use of

Histology for all experiments

Fig. 1 shows a photomicrograph of a coronal section stained with Cresyl Violet from a rat with cannula tip placement in the BLA and schematic diagram of each cannula placement. Animals with misplaced cannula tips were excluded from the data analysis. Histological verifications were done by an observer blind to the experimental conditions.

Effects of MUSC infusion into BLA during overtraining

To control for any non-specific or long-term effects of MUSC, rats trained in the absence of drug received an infusion of MUSC 20 min after training. Rats

Discussion

The data indicate that normally, neuronal activity in the amygdala supports fear learning probably through the mechanisms of NMDA-dependent synaptic plasticity that have been demonstrated in this region (Chapman et al 1990, Clugnet and LeDoux 1990, Miserendino et al 1990, Fanselow and Kim 1994, Maren and Fanselow 1995, Rodrigues et al 2004). Activity in this region is also necessary for performance of fear responses when the BLA has undergone plasticity suggesting that fear memory is also

Acknowledgments

This work was supported by National Institute of Mental Health grant MH62122 (M.S.F.) and 5T32MH015795 (A.M.P.). Special thanks to Quang Ma, Pia Oneill, Moriel Zelikowsky, Igor Kagan and Jeannie Huang for their help with surgery.

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Behavioural neuroscienceAmygdala-dependent and amygdala-independent pathways for contextual fear conditioning

Abstract

Section snippets

Subjects

Histology for all experiments

Effects of MUSC infusion into BLA during overtraining

Discussion

Acknowledgments

J Neurosci Methods

Trends Neurosci

Learn Motivation

Neuron

Neuron

Neurobiol Learn Mem

Physiol Behav

Neurosci Lett

Neurobiol Learn Mem

Neuron

Neuron

Behav Brain Res

Prog Neurobiol

Neurobiol Learn Mem

Neuron

Neurobiol Learn Mem

Neuroscience

Eur J Pharmacol

Neurobiol Learn Mem

Lesions of the basal amygdala block expression of conditioned fear but not extinction

J Neurosci

The spino(trigemino)pontoamygdaloid pathway: electrophysiological evidence for an involvement in pain processes

J Neurophysiol

Effects of selective excitotoxic lesions of the nucleus accumbens core, anterior cingulate cortex, and central nucleus of the amygdala on autoshaping performance in rats

Behav Neurosci

Long-term synaptic potentiation in the amygdala

Synapse

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

The role of the amygdala in fear and anxiety

Annu Rev Neurosci

The role of the amygdala in conditioned and unconditioned fear and anxiety

Distinct regions of the periaqueductal gray are involved in the acquisition and expression of defensive responses

J Neurosci

Organization of axonal projections from the anterolateral area of the bed nuclei of the stria terminalis

J Comp Neurol

Projections from bed nuclei of the stria terminalis, anteromedial area: cerebral hemisphere integration of neuroendocrine, autonomic, and behavioral aspects of energy balance

J Comp Neurol

Conditioned and unconditional components of post-shock freezing

Pavlov J Biol Sci

The midbrain periaqueductal gray as a coordinator of action in response to fear and anxiety

Acquisition of contextual pavlovian fear conditioning is blocked by application of an NMDA receptor antagonist D,L-2-amino-5-phosphonovaleric acid to the basolateral amygdala

Behav Neurosci

Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats

J Neurosci

Classical conditioning as a nonstationary, multivariate time series analysis: A spreadsheet model

Behav Res Methods Instr Comput

Behavioural neuroscience
Amygdala-dependent and amygdala-independent pathways for contextual fear conditioning