Emotional and cognitive information processing: Relations to behavioral performance and hippocampal long-term potentiation in vivo during a spatial water maze training in rats

Abstract

Emotionality as well as cognitive abilities contribute to the acquisition and retrieval of memories as well as to the consolidation of long-term potentiation (LTP), a cellular model of memory formation. However, little is known about the timescale and relative contribution of these processes. Therefore, we tested the effects of weak water maze training, containing both emotional and cognitive demands, on LTP in the hippocampal dentate gyrus. The population spike amplitude (PSA)-LTP was prolonged in all rats irrespective of whether they memorized the platform position or not, whereas the field excitatory postsynaptic potential (fEPSP)-LTP was impaired in good learners and enhanced in poor learners. We then dissociated the behavioral performance of rats during the water maze task by principal component analysis and by means of stress hormone concentrations into underlying "emotional" and "cognitive" factors. PSA-LTP was associated with "emotional" and fEPSP-LTP with "cognitive" behavior. PSA-LTP was depotentiated after the blockade of corticosterone binding mineralocorticoid receptors (MRs) in trained animals, while fEPSP-LTP was unaffected. These results suggest that synaptic processing and encoding of emotional information in the hippocampal dentate gyrus is realized fast and further information transfer is detectable by the reinforcement of PSA-LTP, whereas that of cognitive memories is long lasting.Memory is formed and stored quickly when supported by concurrent emotional experience, whereas the formation of cognitive memories requires repeated training and occurs at a longer timescale (Fanselow 2000;Shors 2001;Sapolsky 2003;Frank et al. 2004). Long-term potentiation (LTP), a cellular model of memory formation, can be dissociated into a short-lived, protein synthesis-independent form (early LTP) and a prolonged, protein synthesis-dependent form (late LTP). The electrically induced early form can be reinforced (consolidated) into the late form by emotional or cognitive stimuli temporally related to the time point of LTP induction (Seidenbecher et al. 1997; Frey 2003, 2004).As emotional and cognitive memories are stored at different timescales, the effective time windows for LTP consolidation induced by emotional and cognitive stimuli may also vary. In the literature LTP and its modulation by memory processes is mostly measured as the field excitatory postsynaptic potential (fEPSP), i.e., the efficacy of synaptic communication between neurons. However, if emotional memories are quickly established, fEPSP-LTP may be affected only during a very short time period after the emotional stimulus. This is supported by recent in vitro findings (Fonseca et al. 2006) which show that the induction and maintenance (30 min to 1 h) of an early fEPSP-LTP can also, in dependence on neuronal activity, be protein synthesis dependent. Thus, during emotional demands with high neuronal activity the memory network may be established rapidly by such mechanisms. An already established memory network may, over time, be better detectable...

A novel control condition for spatial learning in the Morris water maze

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Efecto del estrés en la adquisición y consolidación de la memoria de reconocimiento de objetos en ratas

“…Existen estudios que relacionan la presentación de estresores como la restricción, cercanos a la fase de la adquisición con la expresión diferencial de receptores a glucocorticoides bajos y receptores a mineralocorticoides altos en hipocampo, que pueden generar alteración en el procesamiento de la información 47 . En nuestros resultados es probable que el efecto de la R se sume al estrés producido durante el entrenamiento en RO y que ambos modifiquen la codificación de la información emocional en las estructuras cerebrales involucradas durante la adquisición 48 .…”

Expression of c-Fos in the rat retrosplenial cortex during instrumental re-learning of appetitive bar-pressing depends on the number of stages of previous training

“…Moreover, not all animals in each group acquired Task 2, so their activity during the last session had different levels of success, but still the effect of previous training history on Fos expression seemed to be greater. Individual behavioral differences are of great interest and have been broadly discussed in animal learning studies (Sandi and Touyarot, 2006; Lehner et al, 2008, 2009; Schulz and Korz, 2010; Gökçek-Saraç et al, 2012), but their relations to neuronal functioning (including Fos expression) peculiarities are still to be determined in further experiments.…”