Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues

Selden, Nathan R.; Everitt, Barry J.; Jarrard, Leonard E.; Robbins, Trevor W.

doi:10.1016/0306-4522(91)90379-3

Cited by 540 publications

(368 citation statements)

References 38 publications

Supporting

Mentioning

330

Contrasting

Unclassified

Order By: Relevance

“…When the tone CS predicts the occurrence of the US in a precise (explicit) time-dependent manner (CS-US pairing; context in the background), the increment in ACh release is less than in a situation in which contextual stimuli are the primary stimuli to enter into association with the US (CS-US unpairing; context in the foreground). Hence, in agreement with the well documented role of the hippocampus in contextual conditioning (Selden et al, 1991;Holland and Bouton, 1999;LeDoux, 2000;Nail-Boucherie et al, 2000;Anagnostaras et al, 2001;Maren, 2001;Desmedt et al, 2003;Rudy et al, 2004), the magnitude of ACh release would reflect the degree to which the static contextual stimuli are processed by the hippocampus for their subsequent association with the US.…”

Section: Hippocampal Ach Contributes To the Selection Of Relevant Cssupporting

confidence: 74%

Extracellular Hippocampal Acetylcholine Level Controls Amygdala Function and Promotes Adaptive Conditioned Emotional Response

Calandreau¹,

Trifilieff²,

Mons³

et al. 2006

J. Neurosci.

View full text Add to dashboard Cite

Ample data indicate that tone and contextual fear conditioning differentially require the amygdala and the hippocampus. However, mechanisms subserving the adaptive selection among environmental stimuli (discrete tone vs context) of those that best predict an aversive event are still elusive. Because the hippocampal cholinergic neurotransmission is thought to play a critical role in the coordination between different memory systems leading to the selection of appropriate behavioral strategies, we hypothesized that this cholinergic signal may control the competing acquisition of amygdala-mediated tone and contextual conditioning. Using pavlovian fear conditioning in mice, we first show a higher level of hippocampal acetylcholine release and a specific pattern of extracellular signalregulated kinase 1/2 (ERK1/2) activation within the lateral (LA) and basolateral (BLA) amygdala under conditions in which the context is a better predictor than a discrete tone stimulus. Second, we demonstrate that levels of hippocampal cholinergic neurotransmission are causally related to the patterns of ERK1/2 activation in amygdala nuclei and actually determine the selection among the context or the simple tone the stimulus that best predicts the aversive event. Specifically, decreasing the hippocampal cholinergic signal not only impaired contextual conditioning but also mimicked conditioning to the discrete tone, both in terms of the behavioral outcome and the LA/BLA ERK1/2 activation pattern. Conversely, increasing this cholinergic signal not only disrupted tone conditioning but also promoted contextual fear conditioning. Hence, these findings highlight that hippocampal cholinergic neurotransmission controls amygdala function, thereby leading to the selection of relevant emotional information.

show abstract

Section: Hippocampal Ach Contributes To the Selection Of Relevant Cssupporting

confidence: 74%

Extracellular Hippocampal Acetylcholine Level Controls Amygdala Function and Promotes Adaptive Conditioned Emotional Response

Calandreau¹,

Trifilieff²,

Mons³

et al. 2006

J. Neurosci.

View full text Add to dashboard Cite

show abstract

“…The rat will often begin to freeze when placed in the chamber, suggesting that it has been conditioned to the apparatus where the tone and shock were paired, as well as to the tone itself. Lesions of the hippocampus have no e¡ect on simple or discrimination fear conditioning, but disrupt contextual conditioning (Phillips & LeDoux 1992;Kim & Fanselow 1992;Selden et al 1991). This is consistent with the long-held belief that the hippocampus plays an important role in situations in which the interrelation of various stimuli is important (O'Keefe & Nadel 1978;Nadel & Willner 1980;Eichenbaum et al 1992;Sutherland & Rudy 1989).…”

Section: On T R I Bu T Ion Of T H E a M Yg Da L A A N D I T S C On supporting

confidence: 71%

Emotional memory and psychopathology

LeDoux

Muller

1997

Phil. Trans. R. Soc. Lond. B

104

View full text Add to dashboard Cite

A leading model for studying how the brain forms memories about unpleasant experiences is fear conditioning. A cumulative body of work has identi¢ed major components of the neural system mediating this form of learning. The pathways involve transmission of sensory information from processing areas in the thalamus and cortex to the amygdala. The amygdala's lateral nucleus receives and integrates the sensory inputs from the thalamic and cortical areas, and the central nucleus provides the interface with motor systems controlling speci¢c fear responses in various modalities (behavioural, autonomic, endocrine). Internal connections within the amygdala allow the lateral and central nuclei to communicate. Recent studies have begun to identify some sites of plasticity in the circuitry and the cellular mechanisms involved in fear conditioning. Through studies of fear conditioning, our understanding of emotional memory is being taken to the level of cells and synapses in the brain. Advances in understanding emotional memory hold out the possibility that emotional disorders may be better de¢ned and treatment improved.

show abstract

“…Several studies indicated fear conditioning to context to be more sensitive to lesions of the rat dorsal hippocampus than fear conditioning to tone (Selden et al, 1991;LeDoux, 1992, 1994;Anagnostaras et al, 1999a), even though impaired fear conditioning to a tone (Maren et al, 1997) and intact contextual fear conditioning (Phillips and LeDoux, 1994;Maren et al, 1997;Richmond et al, 1999) were also found after such lesions. Moreover, infusion of the competitive NMDA receptor antagonist APV into the rat dorsal hippocampus resulted in anterograde amnesia of foreground contextual fear conditioning, while this manipulation's effects on fear conditioning to a tone have not been examined (Young et al, 1994).…”

Section: Fear Conditioning To Contextmentioning

confidence: 99%

Dorsal hippocampus and classical fear conditioning to tone and context in rats: Effects of local NMDA‐receptor blockade and stimulation

2003

View full text Add to dashboard Cite

ABSTRACT:Consistent with the importance of the hippocampus in learning more complex stimulus relations, but not in simple associative learning, the dorsal hippocampus has commonly been implicated in classical fear conditioning to context, but not to discrete stimuli, such as a tone. In particular, a specific and central role in contextual fear conditioning has been attributed to mechanisms mediated by dorsal hippocampal N-methyl-D-aspartate (NMDA)-type glutamate receptors. The present study characterized the effects of blockade or tonic stimulation of dorsal hippocampal NMDA receptors by bilateral local infusion of the noncompetitive NMDA receptor antagonist MK-801 (dizocilpine maleate; 6.25 g/side) or of NMDA (0.7 g/side), respectively, on classical fear conditioning to tone and context in Wistar rats. Freezing was used to measure conditioned fear. Regardless of whether conditioning was conducted with tone-shock pairings or unsignaled footshocks (background or foreground contextual conditioning), both NMDA and MK-801 infusion before conditioning resulted in reduced freezing during subsequent exposure to the conditioning context. Freezing during subsequent tone presentation in a new context, normally resulting from conditioning with tone-shock pairings, was not impaired by MK-801 but was strongly reduced by NMDA infusion before conditioning; this freezing was also reduced by NMDA infusion before tone presentation (in an experiment involving NMDA infusions before conditioning and subsequent tone presentation to assess the role of state-dependent learning). It was assessed whether unspecific infusion effects (altered sensorimotor functions, state dependency) or infusion-induced dorsal hippocampal damage contributed to the observed reductions in conditioned freezing. Our data suggest that formation of fear conditioning to context, but not tone, requires NMDA receptor-mediated mechanisms in the dorsal hippocampus. As indicated by the effects of NMDA, some dorsal hippocampal processes may also contribute to fear conditioning to tone. The role of the dorsal hippocampus and local NMDA receptor-mediated processes in fear conditioning to tone and context is discussed in comparison with ventral hippocampal processes.

show abstract

Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues

Cited by 540 publications

References 38 publications

Extracellular Hippocampal Acetylcholine Level Controls Amygdala Function and Promotes Adaptive Conditioned Emotional Response

Extracellular Hippocampal Acetylcholine Level Controls Amygdala Function and Promotes Adaptive Conditioned Emotional Response

Emotional memory and psychopathology

Dorsal hippocampus and classical fear conditioning to tone and context in rats: Effects of local NMDA‐receptor blockade and stimulation

Contact Info

Product

Resources

About