Intrinsic Neuronal Excitability Is Reversibly Altered by a Single Experience in Fear Conditioning

McKay, Bridget M.; Matthews, Elizabeth; Oliveira, Fernando A.; Disterhoft, John F.

doi:10.1152/jn.00347.2009

Cited by 82 publications

(76 citation statements)

References 34 publications

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“…After LTP induction in vivo, we observed increased excitability in vitro even though synaptic potentiation did not survive the slice preparation procedure. Changes in cellular excitability have also been observed ex vivo following different learning tasks, such as trace eye-blink conditioning Thompson et al 1996) and contextual fear conditioning (McKay et al 2009). Similar changes in excitability also occur in the piriform cortex following olfactory discrimination learning (Saar et al 1998).…”

Section: Discussionmentioning

confidence: 99%

Physiological effects of enriched environment exposure and LTP induction in the hippocampus in vivo do not transfer faithfully to in vitro slices

Eckert

Abraham²

2010

Learn. Mem.

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A number of experimental paradigms use in vitro brain slices to test for changes in synaptic transmission and plasticity following a behavioral manipulation. For example, a number of previous studies have reported a variety of effects of environmental enrichment (EE) exposure on field potential responses in hippocampal slices, but in no study was is it known what changes had been elicited in vivo. In the present study, we recorded from the hippocampus in vivo while rats underwent a brief period of EE. There was no detectable EE-induced change in synaptic efficacy in the dentate gyrus in vivo, but there was an increase in cellular excitability. In slices prepared from the same animals, we failed to observe any evidence of the excitability increase. We next tested whether LTP induction in vivo was better preserved in vitro. However, when slices from these rats were examined, there was no observable change in perforant path synaptic strength, although there was a modest increase in excitability that correlated with the increased excitability observed in vivo. These findings suggest that synaptic changes induced in vivo either are not preserved faithfully or are difficult to detect in hippocampal slices, while changes in cellular excitability are better preserved.

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Section: Discussionmentioning

confidence: 99%

Physiological effects of enriched environment exposure and LTP induction in the hippocampus in vivo do not transfer faithfully to in vitro slices

Eckert

Abraham²

2010

Learn. Mem.

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“…Among these, trace or context fear conditioning enhances intrinsic excitability of hippocampal neurons (Kaczorowski and Disterhoft 2009;McKay et al 2009;Song et al 2012). Fear conditioning and extinction also modulate the intrinsic excitability of infralimbic medial prefrontal cortex (mPFC) neurons in a bidirectional manner (Santini et al 2008).…”

Section: Fear Conditioning Enhances Intrinsic Excitability Within Lamentioning

confidence: 99%

“…These include modulation of intrinsic excitability within hippocampus Oh et al 2003;Zelcer et al 2006), piriform cortex (Saar et al 1998;Cohen-Matsliah et al 2009) as well as the infralimbic cortex (Santini et al 2008). Although fear learning modulates excitability of neurons in hippocampus and infralimbic cortex (Santini et al 2008;Kaczorowski and Disterhoft 2009;McKay et al 2009;Song et al 2012), whether fear conditioning leads to modulation of intrinsic excitability of lateral amygdala neurons has yet to be investigated.In the current study, we investigated whether learning causes modulation of intrinsic excitability of LA neurons using fear conditioning, an amygdala-dependent task. To assess any timedependent effects of fear learning on intrinsic excitability, acute brain slices were collected either immediately or 24 h following fear conditioning, and intracellular recordings were obtained from LA neurons.…”

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confidence: 99%

Learning enhances intrinsic excitability in a subset of lateral amygdala neurons

2014

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Learning-induced modulation of neuronal intrinsic excitability is a metaplasticity mechanism that can impact the acquisition of new memories. Although the amygdala is important for emotional learning and other behaviors, including fear and anxiety, whether learning alters intrinsic excitability within the amygdala has received very little attention. Fear conditioning was combined with intracellular recordings to investigate the effects of learning on the intrinsic excitability of lateral amygdala (LA) neurons. To assess time-dependent changes, brain slices were prepared either immediately or 24-h post-conditioning. Fear conditioning significantly enhanced excitability of LA neurons, as evidenced by both decreased afterhyperpolarization (AHP) and increased neuronal firing. These changes were time-dependent such that reduced AHPs were evident at both time points whereas increased neuronal firing was only observed at the later (24-h) time point. Moreover, these changes occurred within a subset (32%) of LA neurons. Previous work also demonstrated that learning-related changes in synaptic plasticity are also evident in less than one-third of amygdala neurons, suggesting that the neurons undergoing intrinsic plasticity may be critical for fear memory. These data may be clinically relevant as enhanced LA excitability following fear learning could influence future amygdala-dependent behaviors.The amygdala is critical for the processing of emotional stimuli (LeDoux 2000). Plasticity within the amygdala is essential for storage of emotional memories (Johansen et al. 2011), and in the manifestation of emotional disorders (Rauch et al. 2000;Mahan and Ressler 2012). Although synaptic plasticity within the amygdala has been investigated extensively (McKernan and ShinnickGallagher 1997;Rogan et al. 1997;Rumpel et al. 2005), intrinsic plasticity has received relatively little attention (but see Rosenkranz et al. 2010;Motanis et al. 2012).Intrinsic plasticity is a change in the intrinsic firing properties of a neuron that regulates two important aspects of learning and memory. First, modulation of intrinsic excitability can allow neuronal ensembles to enter a "learning mode" (Saar et al. 1998). Once neurons enter this learning mode, acquisition of skills or learning dependent on these ensembles is accelerated. For example, acquisition of an olfactory discrimination task enhances intrinsic excitability of hippocampal neurons in a transient manner, and acquisition of a hippocampus-dependent task, such as the Morris water maze, is enhanced during this period of increased excitability (Zelcer et al. 2006). Furthermore, pharmacological or genetic manipulations that increase or decrease intrinsic excitability can enhance or impair learning, respectively (Han et al. 2007;Zhou et al. 2009;Santini and Porter 2010;Santini et al. 2012). Thus, intrinsic excitability influences the strength of the new learning. Second, neurons with greater intrinsic excitability are more likely to be a part of the memory engram than neighboring neurons (Han ...

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“…Although changes in synaptic efficacy have been the primary focus of the past studies on the cellular basis of experience or activity-induced neural plasticity, more recent work has highlighted the importance of changes in intrinsic excitability of neurons in such processes (McKay et al, 2009;Santini et al, 2008;Zhang and Linden, 2003). Further, modulation of spike firing in LA neurons plays a pivotal role in neuronal signaling related to emotional information processing in the amygdala (Maren and Quirk, 2004).…”

Section: Tianeptine Reduces Action Potential Firing In La Neuronsmentioning

confidence: 99%

The Same Antidepressant Elicits Contrasting Patterns of Synaptic Changes in the Amygdala vs Hippocampus

Pillai

Anilkumar

Chattarji

2012

Neuropsychopharmacol

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As depression-like symptoms are often precipitated by some form of stress, animal models of stress have been used extensively to investigate cellular mechanisms of depression. Despite being implicated in the emotional symptoms of depression, the amygdala has received little attention compared to the hippocampus in the past studies of antidepressant action. Further, these investigations have not taken into account the contrasting effects of chronic stress on the hippocampus vs amygdala. If an antidepressant is to be equally effective in countering the differential effects of stress on both brain areas, then it is faced with the challenge of eliciting contrasting effects in these two structures. We tested this prediction by examining the impact of tianeptine, an antidepressant with proven clinical efficacy, on neurons of the lateral amygdala (LA) and hippocampal area CA1. Tianeptine reduces N-methyl-D-aspartate (NMDA)-receptor-mediated synaptic currents, without affecting a-amino-3-hydroxy-5-methyl-4-isoxazole propionate (AMPA) currents, in LA neurons. By contrast, tianeptine enhances both NMDA and AMPA currents in area CA1. Tianeptine also lowers action potential firing in LA neurons. As tianeptine modulates cellular metrics that, in addition to mediating amygdalar behavioral output, are also affected by stress, we tested if tianeptine succeeds in countering stress effects in the intact animal. We find that tianeptine prevents two important functional consequences of chronic stress-induced plasticity in the amygdalaFdendritic growth and enhanced anxiety-like behavior. These results provide evidence for antidepressant action on amygdalar neurons that are not only distinct from the hippocampus, but also protect against the debilitating impact of stress on amygdalar structure and function.

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Intrinsic Neuronal Excitability Is Reversibly Altered by a Single Experience in Fear Conditioning

Cited by 82 publications

References 34 publications

Physiological effects of enriched environment exposure and LTP induction in the hippocampus in vivo do not transfer faithfully to in vitro slices

Physiological effects of enriched environment exposure and LTP induction in the hippocampus in vivo do not transfer faithfully to in vitro slices

Learning enhances intrinsic excitability in a subset of lateral amygdala neurons

The Same Antidepressant Elicits Contrasting Patterns of Synaptic Changes in the Amygdala vs Hippocampus

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