Changes in brain rhythms and connectivity tracking fear acquisition and reversal

Abstract

Fear conditioning is used to investigate the neural bases of threat and anxiety, and to understand their flexible modifications when the environment changes. This study aims to examine the temporal evolution of brain rhythms using electroencephalographic signals recorded in healthy volunteers during a protocol of Pavlovian fear conditioning and reversal. Power changes and Granger connectivity in theta, alpha, and gamma bands are investigated from neuroelectrical activity reconstructed on the cortex. Results show a significant increase in theta power in the left (contralateral to electrical shock) portion of the midcingulate cortex during fear acquisition, and a significant decrease in alpha power in a broad network over the left posterior-frontal and parietal cortex. These changes occur since the initial trials for theta power, but require more trials (3/4) to develop for alpha, and are also present during reversal, despite being less pronounced. In both bands, relevant changes in connectivity are mainly evident in the last block of reversal, just when power differences attenuate. No significant changes in the gamma band were detected. We conclude that the increased theta rhythm in the cingulate cortex subserves fear acquisition and is transmitted to other cortical regions via increased functional connectivity allowing a fast theta synchronization, whereas the decrease in alpha power can represent a partial activation of motor and somatosensory areas contralateral to the shock side in the presence of a dangerous stimulus. In addition, connectivity changes at the end of reversal may reflect long-term alterations in synapses necessary to reverse the previously acquired contingencies.

Cellular Processes and Synaptic Interactions in Nuclei of the Amygdala

“…Plastic changes involve cortical representations and the refinement of contextual input as part of circuit modulation. Theta oscillatory activity across several brain regions has been found to be critical in this regard [31,[84][85][86][87], e.g., in relation to long-term fear memory, modulation of synchronized oscillations in the hippocampal-prefrontal-amygdala circuit in contextual fear, and changes in brain rhythms and connectivity tracking fear acquisition and reversal. Projection neurons of the lateral amygdala exhibit resonant/oscillatory behavior of their membrane potential and provide a cellular correlate of coherent theta activity in amygdalo-hippocampal pathways (see Figure 1).…”

“…Synaptic plasticity observed in these networks has been proposed to rely on correlated activity, e.g., input-specific long-term depression of thalamo-amygdaloid signals and consolidation of long-term potentiation in the dentate gyrus. Moreover, increased theta rhythm in the cingulate cortex was found to subserve fear acquisition and is transmitted to other cortical regions via increased functional connectivity, which allows for fast theta rhythm synchronization [87].…”