Dissociated theta phase synchronization in amygdalo- hippocampal circuits during various stages of fear memory
ABSTRACT The amygdala and the hippocampus are critically involved in the formation and retention of fear memories. However, their precise contribution to, and their interplay during, fear memory formation are not fully understood. In the present study we investigated network activities in the amygdalo-hippocampal system of freely behaving mice at different stages of fear memory consolidation and retention. Our data show enhanced theta phase synchronization in this pathway during the retrieval of fear memory at long-term (24 h post-training), but not short-term (2 min, 30 min and 2 h post-training) stages, following both contextual and auditory cued conditioning. However, retrieval of remotely conditioned fear (30 days post-training) failed to induce an increase in synchronization despite there still being memory retention. Thus, our data indicate that the amygdalo-hippocampal interaction reflects a dynamic interaction of ensemble activities related to various stages of fear memory consolidation and/or retention, and support the notion that recent and remote memories are organized through different network principles.
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ABSTRACT: eLife digest For the brain to function correctly, the activities of multiple regions must be coordinated. This coordination is thought to be carried out by waves of electrical activity in the brain. One of the most prominent signals within these waves is called the theta rhythm. The theta rhythm is thought to help coordinate neural activity between the regions of the brain that are involved in learning and memory. However, theta rhythms also appear when subjects encounter emotional stimuli, which suggests that they might have a role in social cognition. Consistent with this idea, theta rhythms are reduced in individuals with autism spectrum disorders, but the exact nature of the relationship between theta rhythms and social behavior has remained unclear. Tendler and Wagner have now addressed this question directly by implanting electrodes into five brain regions that are active when rats engage in social interactions. Exposing a rat to a social stimulus, such as an unfamiliar visitor rat, caused the intensity of theta rhythms to increase in this network. This change was temporary, with the theta rhythms gradually returning to normal as the novelty of the visitor wore off. An increase in the intensity of theta rhythms also occurred in the same network when the rats encountered a fearful stimulus, such as a tone that had previously signaled the delivery of a mild electric shock. Notably, however, the fearful stimulus led to an increase in low frequency theta rhythms, whereas the social stimulus led to an increase in high frequency theta rhythms. These results suggest that social and fearful stimuli give rise to two different forms of alertness or arousal, which are reflected by the two types of theta rhythms in this network within the brain. Tendler and Wagner also suggest that the distinct frequencies of theta rhythms might be used to support different forms of communication between various regions of the brain, depending on the emotional value of the stimuli (for example, are they social or fearful stimuli?) encountered by the animal. This means that emotional states might be dictating cognitive processes such as learning and memory. DOI: http://dx.doi.org/10.7554/eLife.03614.002eLife Sciences 02/2015; 4. DOI:10.7554/eLife.03614 · 8.52 Impact Factor
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ABSTRACT: Prediction error signals are fundamental to learning. Here, in mice, we show that aversive prediction signals are found in the hemodynamic responses and theta oscillations recorded from the basolateral amygdala. During fear conditioning, amygdala responses evoked by footshock progressively decreased, whereas responses evoked by the auditory cue that predicted footshock concomitantly increased. Unexpected footshock evoked larger amygdala responses than expected footshock. The magnitude of the amygdala response to the footshock predicted behavioral responses the following day. The omission of expected footshock led to a decrease below baseline in the amygdala response suggesting a negative aversive prediction error signal. Thus, in mice, amygdala activity conforms to temporal difference models of aversive learning.The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 07/2014; 34(27):9024-33. DOI:10.1523/JNEUROSCI.4465-13.2014 · 6.75 Impact Factor
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ABSTRACT: Numerous studies have found evidence for corticolimbic theta band electroencephalographic (EEG) oscillations in the neural processing of visual stimuli perceived as threatening. However, varying temporal and topographical patterns have emerged, possibly due to varying arousal levels of the stimuli. In addition, recent studies suggest neural oscillations in delta, theta, alpha, and beta-band frequencies play a functional role in information processing in the brain. This study implemented a data-driven PCA based analysis investigating the spatiotemporal dynamics of electroencephalographic delta, theta, alpha, and beta-band frequencies during an implicit visual threat processing task. While controlling for the arousal dimension (the intensity of emotional activation), we found several spatial and temporal differences for threatening compared to nonthreatening visual images. We detected an early posterior increase in theta power followed by a later frontal increase in theta power, greatest for the threatening condition. There was also a consistent left lateralized beta desynchronization for the threatening condition. Our results provide support for a dynamic corticolimbic network, with theta and beta band activity indexing processes pivotal in visual threat processing.Brain and Cognition 09/2014; 91C:54-61. DOI:10.1016/j.bandc.2014.08.003 · 2.68 Impact Factor