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Publication Date: 2010-06-18
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Sánchez Ramírez, J. D., & Uribe Velásquez, L. F. (2010). Intracellular mechanisms involved in the learning and memory of fear. Biosalud, 9(1), 47–63. Retrieved from https://revistasojs.ucaldas.edu.co/index.php/biosalud/article/view/5512
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Abstract
The neurobiology of fear is a large cellular configuration that implies the group activity of a large number of neurons. These connections suffer changes along the life cycle in a cellular activity-dependant process. This changes the effectiveness of the synaptic communication, facilitating the unchaining process of fear. Hence, the objective of this review is to describe the physiological process that cause those changes in fear, which begin with the activation of ionics and metabotropics receptors, and ending with the genomic stimulation and protein synthesis. Additionally, this paper explains the relation of fear while memories associated with it are established, as a factor that contributes to a higher frequency of discharging and cellular depolarization that favors long term changes due to intense neural excitation. In conclusion, fear can be neurobiologically strengthened after aversive stimulations, by the formation of associations between stimuli, as well as between them and the context, encouraging the organism to have a more efficient reactivity regarding a later meeting with the same threat or circumstance.
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References
Sánchez-Ramírez JD, Uribe-Velásquez LF. Aspectos neurobiológicos implicados en el miedo animal. Biosalud 2009; 8:189-213.
Sánchez-Ramírez JD, Uribe-Velásquez LF. Neurobiología del miedo factor emocional y desencadenante motor visto desde sus bases moleculares, celulares y neuroanatómicas causantes. Monografía del Programa de Medicina Veterinaria y Zootecnia, Facultad de Ciencias Agropecuarias, Universidad de Caldas, Manizales; 2009. pp. 4-67.
Huang YY, Martin KC, Kandel ER. Both protein kinase A and mitogen-activated protein kinase are required in the amygdala for the macromolecular synthesis- dependent late phase of long-term potentiation. J Neurosci 2000; 20(17):6317-6325.
Ginas RR. El cerebro y el mito del yo. 1ra edición. Bogotá: Norma; 2003. pp. 181-201.
Álvarez RP, Biggs A, Chen G, Pine DS, Grillon C. Contextual fear conditioning in humans: Corticalhippocampal and amygdala contributions. J Neurosci 2008; 28(24):6211–6219.
Huang YY, Kandel ER. 5-Hydroxytryptamine induces a protein kinase A/ Mitogen-activated protein kinase-mediated and macromolecular synthesis-dependent late phase of long-term potentiation in the amygdala. J Neurosci 2007; 27(12):3111-3119.
Kalin NH. Neurobiología del miedo. Sci Am 1993; 268(5):94-101.
Carlson NR. Fisiología de la conducta. 6ta edición. Barcelona: Ariel Neurociencia; 1999. pp. 405-430.
Schafe GE, LeDoux JE. Memory consolidation of auditory Pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. J Neurosci 2000; 20:1-5.
Cohen JD, Castro-Alamancos MA. Early sensory pathways for detection of fearful conditioned stimuli: Tectal and thalamic relays. J Neurosci 2007; 27(29):7762-7776.
LaBar KS. Beyond fear emotional memory mechanisms in the human brain. Curr Dir Psychol Sci 2007; 16(4):173-177.
Kishioka A, Fukushima F, Ito T, Kataoka H, Mori H, Ikeda T, et al. A novel form of memory for auditory fear conditioning at a low-intensity unconditioned stimulus. PLoS One 2009; 4(1):e4157.
Christensen JW, Rundgren M. Predator odour per se does not frighten domestic horses. J Applanim 2007; 112(1-2):136-145.
Guimarães-Costa R, Guimarães-Costa MB, Pippa-Gadioli L, Weltson A, Ubiali WA, Paschoalin- Maurin T, et al. Innate defensive behaviour and panic-like reactions evoked by rodents during aggressive encounters with Brazilian constrictor snakes in a complex labyrinth: Behavioural validation of a new model to study affective and agonistic reactions in a prey versus predator paradigm. J Neurosci Methods 2007; 165:25-37.
Bass SLS, Gerlai R. Zebrafish (Danio rerio) responds differentially to stimulus fish: The effects of sympatric and allopatric predators and harmless fish. Behav Brain Res 2008; 186(1):107-117.
Takahashi LK, Chan MM, Pilar ML. Predator odor fear conditioning: Current perspectives and new directions. Neurosci Biobehav Rev 2008; 32(7):1218-1227.
Schafe GE, Atkins CM, Swank MW, Bauer EP, Sweatt JD, LeDoux JE. Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of pavlovian fear conditioning. J Neurosci 2000; 20(21):8177-8187.
Apergis-Schoute AM, De˛biec J, Doyére V, LeDoux JE, Schafe GE. Auditory fear conditioning and long-term potentiation in the lateral amygdala require ERK/MAP kinase signaling in the auditory thalamus: A role for presynaptic plasticity in the fear system. J Neurosci 2005; 25:5730-5739.
Lewis MC, Gould TJ. Signal transduction mechanisms within the entorhinal cortex that support latent inhibition of cued fear conditioning. Neurobiol Learn Mem 2007; 88(3):359-368.
Schafe GE, Swank MW, Rodrigues SM, De¸biec J, Doyère V. Phosphorylation of ERK/MAP kinase is required for long-term potentiation in anatomically restricted regions of the lateral amygdala in vivo. Learn Mem 2008; 15:55-62.
Fischer A, Radulovic M, Schrick C, Sananbenesi F, Godovac-Zimmermann J, Radulovic J. Hippocampal Mek/Erk signaling mediates extinction of contextual freezing behavior. Neurobiol Learn Mem 2007; 87(1):149-158.
Santini E, Quirk GJ, Porter JT. Fear conditioning and extinction differentially modify the intrinsic excitability of infralimbic neurons. J Neurosci 2008; 28(15):4028-4036.
Schafe GE, Nadel NV, Sullivan GM, Harris A, LeDoux JE. Memory consolidation for contextual and auditory fear conditioning is dependent on protein synthesis, PKA, and MAP kinase. Learn Mem 1999; 6:97-110.
Kiyama Y, Manabe T, Sakimura K, Kawakami F, Mori H, Mishina M. Increased thresholds for long-term potentiation and contextual learning in mice lacking the NMDA-type glutamate receptor ε1 subunit. J Neurosci. 1998; 18(17):6704-6712.
Weisskopf MG, Bauer EP, LeDoux JE. L-type voltage-gated calcium channels mediate NMDA independent associative long-term potentiation at thalamic input synapses to the amygdala. J Neurosci 1999; 19(23):10512-10519.
Macrì S, Pasquali P, Bonsignore LT, Pieretti S, Cirulli F, Chiarotti F, et al. Moderate neonatal stress decreases within-group variation in behavioral, immune and HPA responses in adult mice. PLoS One 2007; 10:e1015.
Wilensky AE, Schafe GE, LeDoux JE. The amygdala modulates memory consolidation of fear-motivated inhibitory avoidance learning but not classical fear conditioning. J Neurosci 2000; 20:7059-7066.
Chourbaji S, Hellweg R, Brandis D, Zörner B, Zacher C, Lang UE, et al. Mice with reduced brain-derived neurotrophic factor expression show decreased choline acetyltransferase activity, but regular brain monoamine levels and unaltered emotional behavior. Brain Res Brain Mol Res 2004; 121:28-36.
Rodrigues SM, Farb CR, Bauer EP, LeDoux JE, Schafe GE. Pavlovian fear conditioning regulates Thr286 autophosphorylation of Ca2+/Calmodulin-dependent protein kinase II at lateral amygdala synapses. J Neurosci 2004; 24:3281-3288.
Runyan JD, Moore AN, Dash PK. A role for prefrontal cortex in memory storage for trace fear conditioning. J Neurosci 2004; 24:1288-1295.
Lubin FD, Sweatt JD. The IκB kinase regulates chromatin structure during reconsolidation of conditioned fear memories. Neuron 2007; 55:942-957.
Fails WA, Miserendino MJD, Davis M. Extinction of fear-potentiated startle: Blockade by infusion of an NMDA antagonist into the amygdala. J Neurosci 1992; 12(3):854-963.
Blum S, Runyan JD, Dash PK. Inhibition of prefrontal protein synthesis following recall does not disrupt memory for trace fear conditioning. BMC Neurosci 2006; 7(67):1-10.
Duvarci S, Nader K, LeDoux JE. de novo mRNA synthesis is required for both consolidation and reconsolidation of fear memories in the amygdala. Learn Mem 2008; 15(10):747-755.
Ouyang M, Zhang L, Zhu JJ, Schwede F, Thomas SA. Epac signaling is required for hippocampus dependent memory retrieval. PNAS 2008; 105(33):11993-11997.
Pistell PJ, Falls WA. Extended fear conditioning reveals a role for both N-methyl-D-aspartic acid and non-N-methyl-D-aspartic acid receptors in the amygdala in the acquisition of conditioned fear. Neurosci 2008; 155(4):1011-20.
Bourtchouladze R, Abel T, Berman N, Gordon R, Lapidus K, Kandel ER. Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learn Mem 1998; 5:365-374.
Lu KT, Walker DL, Davis M. Mitogen-activated protein kinase cascade in the basolateral nucleus of amygdala is involved in extinction of fear-potentiated startle. J Neurosci 2001; 21:1-5.
Lin CH, Yeh SH, Lu HY, Gean PW. The similarities and diversities of signal pathways leading to consolidation of conditioning and consolidation of extinction of fear memory. J Neurosci 2003; 23(23):8310-8317.
De˛biec J, Doyère V, Nader K, LeDoux JE. Directly reactivated, but not indirectly reactivated, memories undergo reconsolidation in the amygdala. PNAS 2006; 103:3428-3433.
Palucha A, Pilc A. Metabotropic glutamate receptor ligands as possible anxiolytic and antidepressant drugs. Pharmacol Ther 2007; 115:116-147.
Balschun D, Wolfer DP, Gass P, Mantamadiotis T, Welzl H, Schütz G, et al. Does cAMP response elementbinding protein have a pivotal role in hippocampal synaptic plasticity and hippocampus-dependent memory? J Neurosci 2003; 23(15):6304-6314.
Korzus E, Rosenfeld MG, Mayford M. CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 2004; 42:961-972.
Isiegas C, Park A, Kandel ER, Abel T, Lattal KM. Transgenic Inhibition of Neuronal Protein Kinase A Activity Facilitates Fear Extinction. J Neurosci 2006; 26(49):12700-12707.
Isiegas C, McDonough C, Huang T, Havekes R, Fabian S, Wu LJ, et al. A novel conditional genetic system reveals that increasing neuronal cAMP enhances memory and retrieval. J Neurosci 2008; 28(24):6220-6230.
Kojima N, Borlikova G, Sakamoto T, Yamada K, Ikeda T, Itohara S, et al. Inducible cAMP early repressor acts as a negative regulator for kindling epileptogenesis and long-term fear memory. J Neurosci 2008; 28(25):6459-6472.
Kelly MP, Cheung YF, Favilla C, Siegel SJ, Kanes SJ, Houslay MD, et al. Constitutive activation of the G-protein subunit Gαs within forebrain neurons causes PKA-dependent alterations in fear conditioning and cortical Arc mRNA expression. Learn Mem 2008; 15:75-83.
Wood MA, Hawk JD, Abel T. Combinatorial chromatin modifications and memory storage: A code for memory? Learn Mem 2006; 13:241-244.
Maren S, Fanselow MS. Synaptic plasticity in the basolateral induced by amygdala hippocampal formation stimulation in viva. J Neurosci 1995; 15(11):7546-7564.
Bauer EP, Schafe GE, LeDoux JE. NMDA Receptors and L-type voltage-gated calcium channels contribute to long-term potentiation and different components of fear memory formation in the lateral amygdala. J Neurosci 2002; 22(12):5239-5249.
Vaas R. Neurobiología del miedo. Mente y cerebro 2002; 1:56-63.
Kalisch R, Holt B, Petrovic P, De Martino B, Klöppel S, Büchel C, et al. The NMDA agonist D-cycloserine facilitates fear memory consolidation in humans. Cereb Cortex 2009; 19:187-196.
Wood MA, Kaplan MP, Park A, Blanchard EJ, Oliveira AMM, Lombardi TL, et al. Transgenic mice expressing a truncated form of CREB-binding protein (CBP) exhibit deficits in hippocampal synaptic plasticity and memory storage. Learn Mem 2005; 12:111-119.
English JD, Sweatt JD. Activation of p42 mitogenactivated protein kinase in hippocampal long term potentiation. J Biol Chem 1996; 271:24329-24332.
Vecsey CG, Hawk JD, Lattal KM, Stein JM, Fabian SA, Attner MA, et al. Histone Deacetylase inhibitors enhance memory and synaptic plasticity via CREB: CBP-Dependent transcriptional activation. J Neurosci 2007; 27(23):6128-6140.
Ryu J, Futai K, Feliu M, Weinberg R, Sheng M. Constitutively active Rap2 transgenic mice display fewer dendritic spines, reduced extracellular signal-regulated kinase signaling, enhanced long-term depression, and impaired spatial learning and fear extinction. J Neurosci 2008; 28(33):8178-8188.
Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R. Driving AMPA receptors into synapses by LTP and CaMKII: Requirement for GluR1 and PDZ domain interaction. Science 2000; 287:2262-2267.
Gresack JE, Schafe GE, Orr PT, Frick KM. Sex differences in contextual fear conditioning are associated with differential ventral hippocampal extracellular signal-regulated kinase activation. Neuroscience 2009; 159(2):451-67.
Schafe GE, Doyère V, LeDoux JE. Tracking the fear engram: The lateral amygdala is an essential locus of fear memory storage. J Neurosci 2005; 25(43):10010-10015.
Hebert AE, Dash PK. Plasticity in the entorhinal cortex suppresses memory for contextual fear. J Neurosci 2004; 24(45):10111-10116.
Levenson JM, O’Riordan KJ, Brown KD, Trinh MA, Molfese DL, Sweatt JD. Regulation of histone acetylation during memory formation in the hippocampus. J Biol Chem 2004; 279(39):40545-40559.
Chwang WB, Arthur JS, Schumacher A, Sweatt JD. The nuclear kinase mitogen- and stress-activated protein kinase 1 regulates hippocampal chromatin remodeling in memory formation. J Neurosci 2007; 27(46):12732-12742.
Pan BX, Vautier F, Ito W, Bolshakov VY, Morozov A. Enhanced cortico- amygdala efficacy and suppressed fear in absence of Rap1. J Neurosci 2008; 28(9):2089-2098.
Rodrigues SM, Schafe GE, LeDoux JE. Intra-amygdala blockade of the NR2B subunit of the NMDA receptor disrupts the acquisition but not the expression of fear conditioning. J Neurosci 2001; 21(17):6889-6896.
Fu Z, Lee SH, Simonetta A, Hansen J, Sheng M, Pak DTS. Differential roles of Rap1 and Rap2 small GTPases in neurite retraction and synapse elimination in hippocampal spiny neurons. J Neurochem 2007; 100(1):118-131.
Serrano P, Friedman EL, Kenney J, Taubenfeld SM, Zimmerman JM, Hanna J, et al. PKMζ Maintains spatial, instrumental, and classically conditioned long-term memories. PLoS Biology 2008; 6:2698-2706.
Sánchez-Ramírez JD, Uribe-Velásquez LF. Neurobiología del miedo factor emocional y desencadenante motor visto desde sus bases moleculares, celulares y neuroanatómicas causantes. Monografía del Programa de Medicina Veterinaria y Zootecnia, Facultad de Ciencias Agropecuarias, Universidad de Caldas, Manizales; 2009. pp. 4-67.
Huang YY, Martin KC, Kandel ER. Both protein kinase A and mitogen-activated protein kinase are required in the amygdala for the macromolecular synthesis- dependent late phase of long-term potentiation. J Neurosci 2000; 20(17):6317-6325.
Ginas RR. El cerebro y el mito del yo. 1ra edición. Bogotá: Norma; 2003. pp. 181-201.
Álvarez RP, Biggs A, Chen G, Pine DS, Grillon C. Contextual fear conditioning in humans: Corticalhippocampal and amygdala contributions. J Neurosci 2008; 28(24):6211–6219.
Huang YY, Kandel ER. 5-Hydroxytryptamine induces a protein kinase A/ Mitogen-activated protein kinase-mediated and macromolecular synthesis-dependent late phase of long-term potentiation in the amygdala. J Neurosci 2007; 27(12):3111-3119.
Kalin NH. Neurobiología del miedo. Sci Am 1993; 268(5):94-101.
Carlson NR. Fisiología de la conducta. 6ta edición. Barcelona: Ariel Neurociencia; 1999. pp. 405-430.
Schafe GE, LeDoux JE. Memory consolidation of auditory Pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. J Neurosci 2000; 20:1-5.
Cohen JD, Castro-Alamancos MA. Early sensory pathways for detection of fearful conditioned stimuli: Tectal and thalamic relays. J Neurosci 2007; 27(29):7762-7776.
LaBar KS. Beyond fear emotional memory mechanisms in the human brain. Curr Dir Psychol Sci 2007; 16(4):173-177.
Kishioka A, Fukushima F, Ito T, Kataoka H, Mori H, Ikeda T, et al. A novel form of memory for auditory fear conditioning at a low-intensity unconditioned stimulus. PLoS One 2009; 4(1):e4157.
Christensen JW, Rundgren M. Predator odour per se does not frighten domestic horses. J Applanim 2007; 112(1-2):136-145.
Guimarães-Costa R, Guimarães-Costa MB, Pippa-Gadioli L, Weltson A, Ubiali WA, Paschoalin- Maurin T, et al. Innate defensive behaviour and panic-like reactions evoked by rodents during aggressive encounters with Brazilian constrictor snakes in a complex labyrinth: Behavioural validation of a new model to study affective and agonistic reactions in a prey versus predator paradigm. J Neurosci Methods 2007; 165:25-37.
Bass SLS, Gerlai R. Zebrafish (Danio rerio) responds differentially to stimulus fish: The effects of sympatric and allopatric predators and harmless fish. Behav Brain Res 2008; 186(1):107-117.
Takahashi LK, Chan MM, Pilar ML. Predator odor fear conditioning: Current perspectives and new directions. Neurosci Biobehav Rev 2008; 32(7):1218-1227.
Schafe GE, Atkins CM, Swank MW, Bauer EP, Sweatt JD, LeDoux JE. Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of pavlovian fear conditioning. J Neurosci 2000; 20(21):8177-8187.
Apergis-Schoute AM, De˛biec J, Doyére V, LeDoux JE, Schafe GE. Auditory fear conditioning and long-term potentiation in the lateral amygdala require ERK/MAP kinase signaling in the auditory thalamus: A role for presynaptic plasticity in the fear system. J Neurosci 2005; 25:5730-5739.
Lewis MC, Gould TJ. Signal transduction mechanisms within the entorhinal cortex that support latent inhibition of cued fear conditioning. Neurobiol Learn Mem 2007; 88(3):359-368.
Schafe GE, Swank MW, Rodrigues SM, De¸biec J, Doyère V. Phosphorylation of ERK/MAP kinase is required for long-term potentiation in anatomically restricted regions of the lateral amygdala in vivo. Learn Mem 2008; 15:55-62.
Fischer A, Radulovic M, Schrick C, Sananbenesi F, Godovac-Zimmermann J, Radulovic J. Hippocampal Mek/Erk signaling mediates extinction of contextual freezing behavior. Neurobiol Learn Mem 2007; 87(1):149-158.
Santini E, Quirk GJ, Porter JT. Fear conditioning and extinction differentially modify the intrinsic excitability of infralimbic neurons. J Neurosci 2008; 28(15):4028-4036.
Schafe GE, Nadel NV, Sullivan GM, Harris A, LeDoux JE. Memory consolidation for contextual and auditory fear conditioning is dependent on protein synthesis, PKA, and MAP kinase. Learn Mem 1999; 6:97-110.
Kiyama Y, Manabe T, Sakimura K, Kawakami F, Mori H, Mishina M. Increased thresholds for long-term potentiation and contextual learning in mice lacking the NMDA-type glutamate receptor ε1 subunit. J Neurosci. 1998; 18(17):6704-6712.
Weisskopf MG, Bauer EP, LeDoux JE. L-type voltage-gated calcium channels mediate NMDA independent associative long-term potentiation at thalamic input synapses to the amygdala. J Neurosci 1999; 19(23):10512-10519.
Macrì S, Pasquali P, Bonsignore LT, Pieretti S, Cirulli F, Chiarotti F, et al. Moderate neonatal stress decreases within-group variation in behavioral, immune and HPA responses in adult mice. PLoS One 2007; 10:e1015.
Wilensky AE, Schafe GE, LeDoux JE. The amygdala modulates memory consolidation of fear-motivated inhibitory avoidance learning but not classical fear conditioning. J Neurosci 2000; 20:7059-7066.
Chourbaji S, Hellweg R, Brandis D, Zörner B, Zacher C, Lang UE, et al. Mice with reduced brain-derived neurotrophic factor expression show decreased choline acetyltransferase activity, but regular brain monoamine levels and unaltered emotional behavior. Brain Res Brain Mol Res 2004; 121:28-36.
Rodrigues SM, Farb CR, Bauer EP, LeDoux JE, Schafe GE. Pavlovian fear conditioning regulates Thr286 autophosphorylation of Ca2+/Calmodulin-dependent protein kinase II at lateral amygdala synapses. J Neurosci 2004; 24:3281-3288.
Runyan JD, Moore AN, Dash PK. A role for prefrontal cortex in memory storage for trace fear conditioning. J Neurosci 2004; 24:1288-1295.
Lubin FD, Sweatt JD. The IκB kinase regulates chromatin structure during reconsolidation of conditioned fear memories. Neuron 2007; 55:942-957.
Fails WA, Miserendino MJD, Davis M. Extinction of fear-potentiated startle: Blockade by infusion of an NMDA antagonist into the amygdala. J Neurosci 1992; 12(3):854-963.
Blum S, Runyan JD, Dash PK. Inhibition of prefrontal protein synthesis following recall does not disrupt memory for trace fear conditioning. BMC Neurosci 2006; 7(67):1-10.
Duvarci S, Nader K, LeDoux JE. de novo mRNA synthesis is required for both consolidation and reconsolidation of fear memories in the amygdala. Learn Mem 2008; 15(10):747-755.
Ouyang M, Zhang L, Zhu JJ, Schwede F, Thomas SA. Epac signaling is required for hippocampus dependent memory retrieval. PNAS 2008; 105(33):11993-11997.
Pistell PJ, Falls WA. Extended fear conditioning reveals a role for both N-methyl-D-aspartic acid and non-N-methyl-D-aspartic acid receptors in the amygdala in the acquisition of conditioned fear. Neurosci 2008; 155(4):1011-20.
Bourtchouladze R, Abel T, Berman N, Gordon R, Lapidus K, Kandel ER. Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learn Mem 1998; 5:365-374.
Lu KT, Walker DL, Davis M. Mitogen-activated protein kinase cascade in the basolateral nucleus of amygdala is involved in extinction of fear-potentiated startle. J Neurosci 2001; 21:1-5.
Lin CH, Yeh SH, Lu HY, Gean PW. The similarities and diversities of signal pathways leading to consolidation of conditioning and consolidation of extinction of fear memory. J Neurosci 2003; 23(23):8310-8317.
De˛biec J, Doyère V, Nader K, LeDoux JE. Directly reactivated, but not indirectly reactivated, memories undergo reconsolidation in the amygdala. PNAS 2006; 103:3428-3433.
Palucha A, Pilc A. Metabotropic glutamate receptor ligands as possible anxiolytic and antidepressant drugs. Pharmacol Ther 2007; 115:116-147.
Balschun D, Wolfer DP, Gass P, Mantamadiotis T, Welzl H, Schütz G, et al. Does cAMP response elementbinding protein have a pivotal role in hippocampal synaptic plasticity and hippocampus-dependent memory? J Neurosci 2003; 23(15):6304-6314.
Korzus E, Rosenfeld MG, Mayford M. CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 2004; 42:961-972.
Isiegas C, Park A, Kandel ER, Abel T, Lattal KM. Transgenic Inhibition of Neuronal Protein Kinase A Activity Facilitates Fear Extinction. J Neurosci 2006; 26(49):12700-12707.
Isiegas C, McDonough C, Huang T, Havekes R, Fabian S, Wu LJ, et al. A novel conditional genetic system reveals that increasing neuronal cAMP enhances memory and retrieval. J Neurosci 2008; 28(24):6220-6230.
Kojima N, Borlikova G, Sakamoto T, Yamada K, Ikeda T, Itohara S, et al. Inducible cAMP early repressor acts as a negative regulator for kindling epileptogenesis and long-term fear memory. J Neurosci 2008; 28(25):6459-6472.
Kelly MP, Cheung YF, Favilla C, Siegel SJ, Kanes SJ, Houslay MD, et al. Constitutive activation of the G-protein subunit Gαs within forebrain neurons causes PKA-dependent alterations in fear conditioning and cortical Arc mRNA expression. Learn Mem 2008; 15:75-83.
Wood MA, Hawk JD, Abel T. Combinatorial chromatin modifications and memory storage: A code for memory? Learn Mem 2006; 13:241-244.
Maren S, Fanselow MS. Synaptic plasticity in the basolateral induced by amygdala hippocampal formation stimulation in viva. J Neurosci 1995; 15(11):7546-7564.
Bauer EP, Schafe GE, LeDoux JE. NMDA Receptors and L-type voltage-gated calcium channels contribute to long-term potentiation and different components of fear memory formation in the lateral amygdala. J Neurosci 2002; 22(12):5239-5249.
Vaas R. Neurobiología del miedo. Mente y cerebro 2002; 1:56-63.
Kalisch R, Holt B, Petrovic P, De Martino B, Klöppel S, Büchel C, et al. The NMDA agonist D-cycloserine facilitates fear memory consolidation in humans. Cereb Cortex 2009; 19:187-196.
Wood MA, Kaplan MP, Park A, Blanchard EJ, Oliveira AMM, Lombardi TL, et al. Transgenic mice expressing a truncated form of CREB-binding protein (CBP) exhibit deficits in hippocampal synaptic plasticity and memory storage. Learn Mem 2005; 12:111-119.
English JD, Sweatt JD. Activation of p42 mitogenactivated protein kinase in hippocampal long term potentiation. J Biol Chem 1996; 271:24329-24332.
Vecsey CG, Hawk JD, Lattal KM, Stein JM, Fabian SA, Attner MA, et al. Histone Deacetylase inhibitors enhance memory and synaptic plasticity via CREB: CBP-Dependent transcriptional activation. J Neurosci 2007; 27(23):6128-6140.
Ryu J, Futai K, Feliu M, Weinberg R, Sheng M. Constitutively active Rap2 transgenic mice display fewer dendritic spines, reduced extracellular signal-regulated kinase signaling, enhanced long-term depression, and impaired spatial learning and fear extinction. J Neurosci 2008; 28(33):8178-8188.
Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R. Driving AMPA receptors into synapses by LTP and CaMKII: Requirement for GluR1 and PDZ domain interaction. Science 2000; 287:2262-2267.
Gresack JE, Schafe GE, Orr PT, Frick KM. Sex differences in contextual fear conditioning are associated with differential ventral hippocampal extracellular signal-regulated kinase activation. Neuroscience 2009; 159(2):451-67.
Schafe GE, Doyère V, LeDoux JE. Tracking the fear engram: The lateral amygdala is an essential locus of fear memory storage. J Neurosci 2005; 25(43):10010-10015.
Hebert AE, Dash PK. Plasticity in the entorhinal cortex suppresses memory for contextual fear. J Neurosci 2004; 24(45):10111-10116.
Levenson JM, O’Riordan KJ, Brown KD, Trinh MA, Molfese DL, Sweatt JD. Regulation of histone acetylation during memory formation in the hippocampus. J Biol Chem 2004; 279(39):40545-40559.
Chwang WB, Arthur JS, Schumacher A, Sweatt JD. The nuclear kinase mitogen- and stress-activated protein kinase 1 regulates hippocampal chromatin remodeling in memory formation. J Neurosci 2007; 27(46):12732-12742.
Pan BX, Vautier F, Ito W, Bolshakov VY, Morozov A. Enhanced cortico- amygdala efficacy and suppressed fear in absence of Rap1. J Neurosci 2008; 28(9):2089-2098.
Rodrigues SM, Schafe GE, LeDoux JE. Intra-amygdala blockade of the NR2B subunit of the NMDA receptor disrupts the acquisition but not the expression of fear conditioning. J Neurosci 2001; 21(17):6889-6896.
Fu Z, Lee SH, Simonetta A, Hansen J, Sheng M, Pak DTS. Differential roles of Rap1 and Rap2 small GTPases in neurite retraction and synapse elimination in hippocampal spiny neurons. J Neurochem 2007; 100(1):118-131.
Serrano P, Friedman EL, Kenney J, Taubenfeld SM, Zimmerman JM, Hanna J, et al. PKMζ Maintains spatial, instrumental, and classically conditioned long-term memories. PLoS Biology 2008; 6:2698-2706.
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