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Optical activation of lateral amygdala pyramidal cells instructs associative fear learning

Open access
Johansen, Joshua P., Hamanaka, Hiroki, Monfils, Marie H., Behnia, Rudy, Deisseroth, Karl, Blair, Hugh T., LeDoux, Joseph E.·2010·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.1002418107PMC PMC2906568
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Abstract

Humans and animals can learn that specific sensory cues in the environment predict aversive events through a form of associative learning termed fear conditioning. This learning occurs when the sensory cues are paired with an aversive event occuring in close temporal proximity. Activation of lateral amygdala (LA) pyramidal neurons by aversive stimuli is thought to drive the formation of these associative fear memories; yet, there have been no direct tests of this hypothesis. Here we demonstrate that viral-targeted, tissue-specific expression of the light-activated channelrhodopsin (ChR2) in LA pyramidal cells permitted optical control of LA neuronal activity. Using this approach we then paired an auditory sensory cue with optical stimulation of LA pyramidal neurons instead of an aversive stimulus. Subsequently presentation of the tone alone produced behavioral fear responses. These results demonstrate in vivo optogenetic control of LA neurons and provide compelling support for the idea that fear learning is instructed by aversive stimulus-induced activation of LA pyramidal cells.

AI snapshot

Written from the paper’s full text.

TL;DR

Viral expression of channelrhodopsin in lateral amygdala (LA) pyramidal cells allowed optical stimulation to substitute for an aversive shock unconditioned stimulus (US), and pairing this stimulation with an auditory cue produced associative fear learning and 24-h memory. The results support the idea that aversive stimulus-induced activation of LA pyramidal cells can instruct fear learning.

Key findings

  • ChR2/YFP expression was largely restricted to CaMKII-expressing pyramidal neurons (92 ± 1%) and very low in GABA-expressing cells (1.8 ± 0.0%).
  • In vivo, 20-Hz laser stimulation with 10-ms pulses produced robust, reliable action potential firing in LA cells (total n = 15 cells from four animals) and activated large numbers of LA neurons, with 253 ± 46 CFOS+ cells/section on the stimulated side versus 29 ± 4 on the nonstimulated side (n = 3 animals); total CaMKII+ cells were 402 ± 37 per LA section.
  • In behaving rats, pairing an auditory CS with laser stimulation of LA pyramidal cells as the US produced greater CS-evoked freezing than GFP/paired or ChR2/unpaired controls, with a significant trial block × treatment interaction (F6,63 = 4.7795, P = 0.00045).
  • At 24-h long-term memory testing in a separate context, ChR2/paired animals froze significantly more than GFP/paired and ChR2/unpaired animals (one-way ANOVA F2,21 = 5.41, P = 0.013; post hoc P = 0.017 for both comparisons).

Methods

  • Male Sprague-Dawley rats (275–300 g) received unilateral LA injections of AAV-CaMKII-ChR2/EYFP or AAV-CaMKII-GFP, with guide cannulae for fiber-optic laser stimulation; experiments included immunocytochemistry, in vivo electrophysiology, CFOS mapping, and behavioral fear conditioning.
  • For conditioning, paired groups received 16 CS–US pairings: a 20-s auditory CS (5-kHz tone pips, 1 Hz, 250 ms on/750 ms off) coterminating with a 2-s laser US (20 Hz, 10-ms pulses); an unpaired group received 16 CS and 16 laser US presentations randomly and explicitly unpaired.
  • Freezing was scored by a blind rater during training and during two CS presentations 24 h later in a novel context; data were analyzed with repeated-measures ANOVA, one-way ANOVA, and Newman–Keuls post hoc tests.

Limitations

  • The paper states that freezing scores during long-term memory testing were relatively low compared with those typically obtained with an electric shock US, and it discusses possible explanations, including the need for plasticity in other fear-circuit regions, more specific cell targeting, or coactivation of neuromodulatory systems for maximal memory formation.
  • The paper notes that laser stimulation itself produced a small but statistically significant amount of unconditioned freezing (paired t5 = 4.89, P = 0.005).
  • Evident from the text: behavioral groups were small (n = 8 per group), CFOS and electrophysiology samples were limited (n = 3 animals; n = 15 cells), only male rats were used, and 3 ChR2/paired and 2 ChR2/unpaired animals were excluded because ChR2 expression or cannula placement criteria were not met.

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Integrity signals

Registry

Crossref · 10.1073/pnas.1002418107

Cites

60 of 60 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 37 cited sources checked · 0 supported · 0 flagged

  • Findingown data
    § Results

    Constant laser illumination and eyelid shock activated comparable levels of action potential firing.

    “Laser stimulation at 20 Hz produced significantly more action potential firing than either constant illumination or eyelid shock, whereas the latter two activated comparable levels of action potential firing (Fig. S3).”
    Quote in the paperNot a substantial claim
  • Findingown data
    § Results

    Laser stimulation at 20 Hz produced significantly more action potential firing than either constant laser illumination or eyelid shock.

    “Laser stimulation at 20 Hz produced significantly more action potential firing than either constant illumination or eyelid shock, whereas the latter two activated comparable levels of action potential firing (Fig. S3).”
    • Also stated in: § Discussion · hedged
      “However, the CFOS experiments reported here demonstrate that large numbers of LA neurons were activated by laser stimulation and the electrophysiology experiments provide evidence that 20-Hz laser stimulation caused more action potential firing in LA cells than a shock US, suggesting that these were not the reasons for lower levels of fear learning.”
    Quote in the paperSubstantial claim
  • Findingown data
    § Discussion

    Using the same fear conditioning protocol, substantial levels of fear conditioning were induced by a unilateral eyelid shock US.

    “In fact, using the same fear conditioning protocol, we also found substantial levels of fear conditioning induced by a unilateral eyelid shock US (see Fig. S6 for comparison of shock vs. laser stimulation US-induced learning).”
    Quote in the paperSubstantial claim
  • Findingown data
    § Results

    Using 2-s constant laser illumination as a US produced similar levels of fear conditioning to that evoked by the 20-Hz laser US.

    “Because using constant illumination to stimulate LA neurons produced similar levels of action potential firing as that evoked by eyelid shocks (Fig. S3), we also used 2-s constant laser illumination as an US (instead of 10-ms laser pulses at 20 Hz described above) and found that this stimulation protocol produced similar levels of fear conditioning (Fig. S5) to that evoked by the 20-Hz laser US.”
    Quote in the paperNot a substantial claim
  • Findingown data
    § Results

    During training, ChR2/paired animals froze significantly more to the CS than GFP/paired and ChR2/unpaired groups, especially later in training.

    “During training, ChR2/paired animals froze significantly more to the CS than the GFP/paired and ChR2/unpaired groups especially later in training (Fig. 3A).”
    • Also stated in: § Results · boosted
      “post hoc comparisons demonstrated that CS-evoked freezing responses in ChR2/paired animals during trial blocks 3 and 4 were significantly greater than CS freezing responses in GFP/paired (P = 0002 and P = 0.0001 respectively) or ChR2/unpaired (P = 002 and P = 0.0001, respectively) groups.”
    Quote in the paperSubstantial claim
  • May combine two claims. 6
  • Classified as probably not a substantial claim. 15

  • May combine two claims.

    Interpretationcitation
    § Discussion

    Optical stimulation of LA pyramidal neurons produced some freezing behavior, but these levels were considerably lower than fear responses evoked by stimulation of the central nucleus of the amygdala (CeA).

    “Although optical stimulation of LA pyramidal neurons produced some freezing behavior, these levels were considerably lower than fear responses evoked by stimulation of the central nucleus of the amygdala (CeA) (reviewed in ref. 27), suggesting that the CeA is more directly connected with the behavioral output pathways responsible for fear responses.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [27] Davis M. The role of the amygdala in conditioned and unconditioned fear and anxiety. In: Aggleton JP, editor. The Amygdala. 2nd Ed. Oxford: Oxford Univ Press; 2000. pp. 213–288. [Google Scholar] source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation
    § Discussion

    A large number of studies have provided convincing evidence that associative plasticity in the LA contributes to fear memory formation.

    “A large number of studies have provided convincing evidence that associative plasticity in the LA contributes to fear memory formation (4, 6, 7).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [4] Sah P, Westbrook RF, Lüthi A. Fear conditioning and long-term potentiation in the amygdala: What really is the connection? Ann N Y Acad Sci. 2008;1129:88–95. doi: 10.1196/annals.1417.020. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [6] Blair HT, Schafe GE, Bauer EP, Rodrigues SM, LeDoux JE. Synaptic plasticity in the lateral amygdala: A cellular hypothesis of fear conditioning. Learn Mem. 2001;8:229–242. doi: 10.1101/lm.30901. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [7] Maren S, Quirk GJ. Neuronal signalling of fear memory. Nat Rev Neurosci. 2004;5:844–852. doi: 10.1038/nrn1535. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing). May combine two claims.

    Premisecitation
    § Abstract

    Fear conditioning is a simple form of associative learning that provides a powerful model system to study associative plasticity and memory formation.

    “Fear conditioning is a simple form of associative learning that provides a powerful model system to study associative plasticity and memory formation (1–4).”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [1] LeDoux JE. Emotion circuits in the brain. Annu Rev Neurosci. 2000;23:155–184. doi: 10.1146/annurev.neuro.23.1.155. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [2] Lang PJ, Davis M. Emotion, motivation, and the brain: Reflex foundations in animal and human research. Prog Brain Res. 2006;156:3–29. doi: 10.1016/S0079-6123(06)56001-7. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [3] Fanselow MS, Poulos AM. The neuroscience of mammalian associative learning. Annu Rev Psychol. 2005;56:207–234. doi: 10.1146/annurev.psych.56.091103.070213. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [4] Sah P, Westbrook RF, Lüthi A. Fear conditioning and long-term potentiation in the amygdala: What really is the connection? Ann N Y Acad Sci. 2008;1129:88–95. doi: 10.1196/annals.1417.020. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S1 (asserted).

    Premisecitation
    § Discussion

    It is widely believed that LA plasticity underlying fear learning occurs as a result of a Hebbian mechanism whereby the shock US directly depolarizes LA pyramidal cells that are concurrently activated by weaker CS inputs, resulting in potentiation of the CS input synapses.

    “It is widely believed that LA plasticity underlying fear learning occurs as a result of a Hebbian mechanism whereby the shock US directly depolarizes LA pyramidal cells that are concurrently activated by weaker CS inputs, resulting in potentiation of the CS input synapses (5, 6, 9, 31).”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [5] Rogan MT, Weisskopf MG, Huang YY, Kandel ER, LeDoux JE. Long term potentiation in the amygdala: Implications for memory formation. In: Holscher C, editor. Neuronal Mechanisms of Memory Formation. Cambridge, UK: Cambridge Univ Press; 2000. pp. 58–76. [Google Scholar] source

      Not checked in the free run.

    • cites [6] Blair HT, Schafe GE, Bauer EP, Rodrigues SM, LeDoux JE. Synaptic plasticity in the lateral amygdala: A cellular hypothesis of fear conditioning. Learn Mem. 2001;8:229–242. doi: 10.1101/lm.30901. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [9] Rosenkranz JA, Grace AA. Dopamine-mediated modulation of odour-evoked amygdala potentials during pavlovian conditioning. Nature. 2002;417:282–287. doi: 10.1038/417282a. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [31] Paré D. Mechanisms of Pavlovian fear conditioning: Has the engram been located? Trends Neurosci. 2002;25:436–437. doi: 10.1016/s0166-2236(02)02243-9. discussion 437–438. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Results

    ChR2 has been used in other neural systems to activate specific cell populations and produce learning.

    “The light activated channelrhodopsin (ChR2) (19, 20) has been used in other neural systems to activate specific cell populations and produce learning (21–23).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [21] Tsai HC, et al. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science. 2009;324:1080–1084. doi: 10.1126/science.1168878. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [22] Claridge-Chang A, et al. Writing memories with light-addressable reinforcement circuitry. Cell. 2009;139:405–415. doi: 10.1016/j.cell.2009.08.034. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [23] Huber D, et al. Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice. Nature. 2008;451:61–64. doi: 10.1038/nature06445. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation
    § Abstract

    The lateral nucleus of the amygdala (LA) is a site of associative plasticity, where US-evoked depolarization of LA pyramidal neurons is thought to instruct plasticity at synapses formed by CS inputs onto the same neurons.

    “The lateral nucleus of the amygdala (LA) is a site of associative plasticity, where US-evoked depolarization of LA pyramidal neurons is thought to instruct plasticity at synapses formed by CS inputs onto the same neurons (5–7).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [5] Rogan MT, Weisskopf MG, Huang YY, Kandel ER, LeDoux JE. Long term potentiation in the amygdala: Implications for memory formation. In: Holscher C, editor. Neuronal Mechanisms of Memory Formation. Cambridge, UK: Cambridge Univ Press; 2000. pp. 58–76. [Google Scholar] source

      Not checked in the free run.

    • cites [6] Blair HT, Schafe GE, Bauer EP, Rodrigues SM, LeDoux JE. Synaptic plasticity in the lateral amygdala: A cellular hypothesis of fear conditioning. Learn Mem. 2001;8:229–242. doi: 10.1101/lm.30901. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [7] Maren S, Quirk GJ. Neuronal signalling of fear memory. Nat Rev Neurosci. 2004;5:844–852. doi: 10.1038/nrn1535. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S1 (asserted), S4 (based).

    Interpretationreasoning
    § Discussion

    Depolarization of LA pyramidal cells by the US provides an instructive signal for LA plasticity and fear learning.

    “This model suggests that depolarization of LA pyramidal cells by the US provides an instructive signal for LA plasticity and fear learning.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Discussion

    Plasticity in the LA is required for several forms of appetitively motivated learning.

    “In addition to being essential for aversively motivated learning, plasticity in the LA is also required for several forms of appetitively motivated learning (43–45) and a number of studies have found that separate populations of amygdala neurons mediate aversive and appetitive processing (46–48).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [43] Burns LH, Everitt BJ, Robbins TW. Intra-amygdala infusion of the N-methyl-D-aspartate receptor antagonist AP5 impairs acquisition but not performance of discriminated approach to an appetitive CS. Behav Neural Biol. 1994;61:242–250. doi: 10.1016/s0163-1047(05)80007-x. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [44] Baldwin AE, Holahan MR, Sadeghian K, Kelley AE. N-methyl-D-aspartate receptor-dependent plasticity within a distributed corticostriatal network mediates appetitive instrumental learning. Behav Neurosci. 2000;114:84–98. doi: 10.1037//0735-7044.114.1.84. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [45] Tye KM, Stuber GD, de Ridder B, Bonci A, Janak PH. Rapid strengthening of thalamo-amygdala synapses mediates cue-reward learning. Nature. 2008;453:1253–1257. doi: 10.1038/nature06963. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation
    § Discussion

    This process is associative, requiring close temporal contiguity of the CS and laser US and that the laser US occurrence is contingent upon the CS preceding it, as it does not occur when the CS and light US are temporally unpaired during training in ChR2-treated animals.

    “Finally, this process is associative (i.e., requires the close temporal contiguity of the CS and laser US and that the laser US occurrence is contingent upon the CS preceding it, ref. 26) as it does not occur when the CS and the light US are temporally unpaired during training in ChR2-treated animals.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [26] Rescorla RA. Probability of shock in the presence and absence of CS in fear conditioning. J Comp Physiol Psychol. 1968;66:1–5. doi: 10.1037/h0025984. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductnone given
    § Materials and Methods

    A rater blind to treatment group scored animals' behavioral freezing during the first 18 s of the CS in training and during all 20 CS presentations in testing.

    “A rater who was blind with respect to the treatment group scored animals’ behavioral freezing during the first 18 s of the CS (during the training phase) and during all of the 20 CS (during “testing”) offline using a digital stopwatch.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given
    § Materials and Methods

    The fiber optic cable was inserted into the chronic guide cannula by an experimenter blind to the animals' treatment.

    “A fiber optic cable, which had been threaded through a polyethylene tether (Plastics One) and then through the tip of a stainless steel tube (26 g, Plastics One), was inserted into the chronic guide cannula on the animal's head by an experimenter who was blind as to what treatment the animals would receive.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data
    § Materials and Methods

    Three ChR2/paired and two ChR2/unpaired animals were excluded from the final analysis because the criteria for ChR2 expression in LA neurons and guide cannula placement were not met.

    “Three ChR2/paired and 2 ChR2/unpaired were not included in the final analysis as these criteria were not met.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given
    § Materials and Methods

    Single neuron waveforms had to exhibit a refractory period of at least 1 ms and a mean spike amplitude of at least 80 μV to be included in the study.

    “Single neuron waveforms were then isolated offline and had to exhibit a refractory period of at least 1 ms and mean spike amplitude of at least 80 μV to be included in the study.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S1 (asserted), S3 (load-bearing).

    Premisecitation
    § Discussion

    Coactivation of noradrenergic β receptors and subsequent G protein-coupled signaling pathways in conjunction with depolarization of LA neurons cooperatively regulates LA plasticity and fear conditioning.

    “In fact it has been suggested that coactivation of noradrenergic β receptors and subsequent G protein-coupled signaling pathways in conjunction with depolarization of LA neurons cooperatively regulates LA plasticity and fear conditioning (50).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [50] Bailey CH, Giustetto M, Huang YY, Hawkins RD, Kandel ER. Is heterosynaptic modulation essential for stabilizing Hebbian plasticity and memory? Nat Rev Neurosci. 2000;1:11–20. doi: 10.1038/35036191. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given
    § Materials and Methods

    Experimenters were blind as to what virus (AAV-CaMKII-ChR2/EYFP or AAV-CaMKII-GFP) was being injected.

    “Experimenters were blind as to what virus (AAV-CaMKII-ChR2/EYFP or AAV-CaMKII-GFP) was being injected.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given
    § Materials and Methods

    All procedures were approved by the New York University Animal Care and Use Committee and conducted in accordance with the National Institutes of Health Guide for the Care and Use of Experimental Animals.

    “All procedures were approved by the New York University Animal Care and Use Committee and conducted in accordance with the National Institutes of Health Guide for the Care and Use of Experimental Animals.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductnone given
    § Materials and Methods

    For behavioral experiments, an experimenter blind to animal and treatment group assessed whether ChR2 was expressed in LA neurons and whether the guide cannula tip was dorsal and proximal to the LA.

    “For behavioral experiments, sections were processed as described above and an experimenter blind as to animal and treatment group assessed whether ChR2 was expressed in the LA neurons and whether the tip of the guide cannula was dorsal and proximal to the LA.”
    Quote in the paperSubstantial claim
17 of 17

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Activation of lateral amygdala neurons induces unconditioned freezing.

    “Briefly, activation of lateral amygdala neurons induces unconditioned freezing70.”

    From Resolving the neural circuits of anxiety (2015) · cites this paper as [70]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Stimulation trials are described as both 1 s and 1 min long

    Minor

    The electrophysiology methods define a trial as a 1-s stimulation period, but then say the calculation divides by the number of 1-min stimulation trials. Those descriptions assign different durations to the same unit of analysis.

1 of 1

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Related

Authors
Johansen, J. P., Hamanaka, H., Monfils, M. H., Behnia, R., Deisseroth, K., Blair, H. T., & LeDoux, J. E.
Affiliations
  • New York University (US)
  • Howard Hughes Medical Institute (US)
  • University of California, Los Angeles (US)
  • Nathan Kline Institute for Psychiatric Research (US)
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2010-06-25
Volume
107
Issue
28
Pages
12692-12697
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.1002418107
PMC
PMC2906568
OpenAlex
W2090654839
Semantic Scholar
0820aaefabf3c978a0c6e0954f97ebe130e1bb9f
Cited by
308
References
57
Citations by year
2026: 3 · 2025: 8 · 2024: 21 · 2023: 11 · 2022: 8 · 2021: 21 · 2020: 22 · 2019: 21 · 2018: 14 · 2017: 20 · 2016: 21 · 2015: 35 · 2014: 28 · 2013: 32 · 2012: 23
FWCI
14.51
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Howard Hughes Medical Institute
  • Deutsches Krebsforschungszentrum
  • York University
  • National Institute of Mental Health (R01MH046516, F32MH082505)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
Keywords
lateral amygdala, pyramidal neurons, fear conditioning, optogenetics, channelrhodopsin, auditory fear conditioning, aversive stimuli, fear memory, neuronal activity control
MeSH terms
Amygdala, Animals, Conditioning, Psychological, Conditioning, Classical, Cues, Fear, Male, Neurons, Phobic Disorders, Photic Stimulation, Rats, Sprague-Dawley, Pyramidal Cells, Rats

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