Hippocampal Memory Recovery After Acute Stress: A Behavioral, Morphological and Molecular Study

Felipe Ignacio Aguayo, Macarena Tejos-Bravo, Gabriela Díaz-Véliz, Aníbal Pacheco, Gonzalo García-Rojo, Wladimir Corrales, Felipe Antonio Olave, Esteban Aliaga, José L. Ulloa, Ana M. Avalos, Luciano Román-Albasini, Paulina S. Rojas, Jenny Lucy Fiedler

Resultado de la investigación: Article

Resumen

Several studies have shown that a single exposure to stress may improve or impair learning and memory processes, depending on the timing in which the stress event occurs with relation to the acquisition phase. However, to date there is no information about the molecular changes that occur at the synapse during the stress-induced memory modification and after a recovery period. In particular, there are no studies that have evaluated—at the same time—the temporality of stress and stress recovery period in hippocampal short-term memory and the effects on dendritic spine morphology, along with variations in N-methyl-D-aspartate (NMDA) and α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor subunits. The aim of our study was to take a multidimensional approach to investigate concomitant behavioral, morphological and molecular changes induced by a single restraint stress exposure (2.5 h) and a recovery period of 6 and 24 h in rats. We found that acute stress elicited a reduced preference to explore an object placed in a novel position (a hippocampal-dependent task). These changes were accompanied by increased activity of LIM kinase I (LIMK; an actin-remodeling protein) and increased levels of NR2A subunits of NMDA receptors. After 6 h of recovery from stress, rats showed similar preference to explore an object placed in a novel or familiar position, but density of immature spines increased in secondary CA1 apical dendrites, along with a transient rise in GluA2 AMPA receptor subunits. After 24 h of recovery from stress, the animals showed a preference to explore an object placed in a novel position, which was accompanied by a normalization of NMDA and AMPA receptor subunits to control values. Our data suggest that acute stress produces reversible molecular and behavioral changes 24 h after stress, allowing a full reestablishment of hippocampal-related memory. Further studies need to be conducted to deepen our understanding of these changes and their reciprocal interactions.Adaptive stress responses are a promising avenue to develop interventions aiming at restoring hippocampal function impaired by repetitive stress exposure.

Idioma originalEnglish
Número de artículo283
PublicaciónFrontiers in Molecular Neuroscience
Volumen11
DOI
EstadoPublished - 17 ago 2018

Huella dactilar

AMPA Receptors
N-Methyl-D-Aspartate Receptors
Lim Kinases
Dendritic Spines
N-Methylaspartate
Dendrites
Short-Term Memory
Synapses
Actins
Spine
Learning
Acids
Proteins

ASJC Scopus subject areas

  • Molecular Biology
  • Cellular and Molecular Neuroscience

Citar esto

Aguayo, F. I., Tejos-Bravo, M., Díaz-Véliz, G., Pacheco, A., García-Rojo, G., Corrales, W., ... Fiedler, J. L. (2018). Hippocampal Memory Recovery After Acute Stress: A Behavioral, Morphological and Molecular Study. Frontiers in Molecular Neuroscience, 11, [283]. https://doi.org/10.3389/fnmol.2018.00283
Aguayo, Felipe Ignacio ; Tejos-Bravo, Macarena ; Díaz-Véliz, Gabriela ; Pacheco, Aníbal ; García-Rojo, Gonzalo ; Corrales, Wladimir ; Olave, Felipe Antonio ; Aliaga, Esteban ; Ulloa, José L. ; Avalos, Ana M. ; Román-Albasini, Luciano ; Rojas, Paulina S. ; Fiedler, Jenny Lucy. / Hippocampal Memory Recovery After Acute Stress : A Behavioral, Morphological and Molecular Study. En: Frontiers in Molecular Neuroscience. 2018 ; Vol. 11.
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abstract = "Several studies have shown that a single exposure to stress may improve or impair learning and memory processes, depending on the timing in which the stress event occurs with relation to the acquisition phase. However, to date there is no information about the molecular changes that occur at the synapse during the stress-induced memory modification and after a recovery period. In particular, there are no studies that have evaluated—at the same time—the temporality of stress and stress recovery period in hippocampal short-term memory and the effects on dendritic spine morphology, along with variations in N-methyl-D-aspartate (NMDA) and α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor subunits. The aim of our study was to take a multidimensional approach to investigate concomitant behavioral, morphological and molecular changes induced by a single restraint stress exposure (2.5 h) and a recovery period of 6 and 24 h in rats. We found that acute stress elicited a reduced preference to explore an object placed in a novel position (a hippocampal-dependent task). These changes were accompanied by increased activity of LIM kinase I (LIMK; an actin-remodeling protein) and increased levels of NR2A subunits of NMDA receptors. After 6 h of recovery from stress, rats showed similar preference to explore an object placed in a novel or familiar position, but density of immature spines increased in secondary CA1 apical dendrites, along with a transient rise in GluA2 AMPA receptor subunits. After 24 h of recovery from stress, the animals showed a preference to explore an object placed in a novel position, which was accompanied by a normalization of NMDA and AMPA receptor subunits to control values. Our data suggest that acute stress produces reversible molecular and behavioral changes 24 h after stress, allowing a full reestablishment of hippocampal-related memory. Further studies need to be conducted to deepen our understanding of these changes and their reciprocal interactions.Adaptive stress responses are a promising avenue to develop interventions aiming at restoring hippocampal function impaired by repetitive stress exposure.",
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Aguayo, FI, Tejos-Bravo, M, Díaz-Véliz, G, Pacheco, A, García-Rojo, G, Corrales, W, Olave, FA, Aliaga, E, Ulloa, JL, Avalos, AM, Román-Albasini, L, Rojas, PS & Fiedler, JL 2018, 'Hippocampal Memory Recovery After Acute Stress: A Behavioral, Morphological and Molecular Study', Frontiers in Molecular Neuroscience, vol. 11, 283. https://doi.org/10.3389/fnmol.2018.00283

Hippocampal Memory Recovery After Acute Stress : A Behavioral, Morphological and Molecular Study. / Aguayo, Felipe Ignacio; Tejos-Bravo, Macarena; Díaz-Véliz, Gabriela; Pacheco, Aníbal; García-Rojo, Gonzalo; Corrales, Wladimir; Olave, Felipe Antonio; Aliaga, Esteban; Ulloa, José L.; Avalos, Ana M.; Román-Albasini, Luciano; Rojas, Paulina S.; Fiedler, Jenny Lucy.

En: Frontiers in Molecular Neuroscience, Vol. 11, 283, 17.08.2018.

Resultado de la investigación: Article

TY - JOUR

T1 - Hippocampal Memory Recovery After Acute Stress

T2 - A Behavioral, Morphological and Molecular Study

AU - Aguayo, Felipe Ignacio

AU - Tejos-Bravo, Macarena

AU - Díaz-Véliz, Gabriela

AU - Pacheco, Aníbal

AU - García-Rojo, Gonzalo

AU - Corrales, Wladimir

AU - Olave, Felipe Antonio

AU - Aliaga, Esteban

AU - Ulloa, José L.

AU - Avalos, Ana M.

AU - Román-Albasini, Luciano

AU - Rojas, Paulina S.

AU - Fiedler, Jenny Lucy

PY - 2018/8/17

Y1 - 2018/8/17

N2 - Several studies have shown that a single exposure to stress may improve or impair learning and memory processes, depending on the timing in which the stress event occurs with relation to the acquisition phase. However, to date there is no information about the molecular changes that occur at the synapse during the stress-induced memory modification and after a recovery period. In particular, there are no studies that have evaluated—at the same time—the temporality of stress and stress recovery period in hippocampal short-term memory and the effects on dendritic spine morphology, along with variations in N-methyl-D-aspartate (NMDA) and α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor subunits. The aim of our study was to take a multidimensional approach to investigate concomitant behavioral, morphological and molecular changes induced by a single restraint stress exposure (2.5 h) and a recovery period of 6 and 24 h in rats. We found that acute stress elicited a reduced preference to explore an object placed in a novel position (a hippocampal-dependent task). These changes were accompanied by increased activity of LIM kinase I (LIMK; an actin-remodeling protein) and increased levels of NR2A subunits of NMDA receptors. After 6 h of recovery from stress, rats showed similar preference to explore an object placed in a novel or familiar position, but density of immature spines increased in secondary CA1 apical dendrites, along with a transient rise in GluA2 AMPA receptor subunits. After 24 h of recovery from stress, the animals showed a preference to explore an object placed in a novel position, which was accompanied by a normalization of NMDA and AMPA receptor subunits to control values. Our data suggest that acute stress produces reversible molecular and behavioral changes 24 h after stress, allowing a full reestablishment of hippocampal-related memory. Further studies need to be conducted to deepen our understanding of these changes and their reciprocal interactions.Adaptive stress responses are a promising avenue to develop interventions aiming at restoring hippocampal function impaired by repetitive stress exposure.

AB - Several studies have shown that a single exposure to stress may improve or impair learning and memory processes, depending on the timing in which the stress event occurs with relation to the acquisition phase. However, to date there is no information about the molecular changes that occur at the synapse during the stress-induced memory modification and after a recovery period. In particular, there are no studies that have evaluated—at the same time—the temporality of stress and stress recovery period in hippocampal short-term memory and the effects on dendritic spine morphology, along with variations in N-methyl-D-aspartate (NMDA) and α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor subunits. The aim of our study was to take a multidimensional approach to investigate concomitant behavioral, morphological and molecular changes induced by a single restraint stress exposure (2.5 h) and a recovery period of 6 and 24 h in rats. We found that acute stress elicited a reduced preference to explore an object placed in a novel position (a hippocampal-dependent task). These changes were accompanied by increased activity of LIM kinase I (LIMK; an actin-remodeling protein) and increased levels of NR2A subunits of NMDA receptors. After 6 h of recovery from stress, rats showed similar preference to explore an object placed in a novel or familiar position, but density of immature spines increased in secondary CA1 apical dendrites, along with a transient rise in GluA2 AMPA receptor subunits. After 24 h of recovery from stress, the animals showed a preference to explore an object placed in a novel position, which was accompanied by a normalization of NMDA and AMPA receptor subunits to control values. Our data suggest that acute stress produces reversible molecular and behavioral changes 24 h after stress, allowing a full reestablishment of hippocampal-related memory. Further studies need to be conducted to deepen our understanding of these changes and their reciprocal interactions.Adaptive stress responses are a promising avenue to develop interventions aiming at restoring hippocampal function impaired by repetitive stress exposure.

KW - Actin dynamics

KW - Acute stress

KW - Dendritic spines

KW - Glutamate receptors

KW - Hippocampus

KW - Learning and memory

KW - LIMK

KW - RhoA/ROCK signaling pathway

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Aguayo FI, Tejos-Bravo M, Díaz-Véliz G, Pacheco A, García-Rojo G, Corrales W y otros. Hippocampal Memory Recovery After Acute Stress: A Behavioral, Morphological and Molecular Study. Frontiers in Molecular Neuroscience. 2018 ago 17;11. 283. https://doi.org/10.3389/fnmol.2018.00283