Abstract
SummaryRodent research delineates how the basolateral amygdala (BLA) and central amygdala (CeA) control defensive behaviors, but translation of these findings to humans is needed. Here, we compare humans with natural-selective bilateral BLA lesions to rats with a chemogenetically silenced BLA. We find, across species, an essential role for the BLA in the selection of active escape over passive freezing during exposure to imminent yet escapable threat (Timm). In response to Timm, BLA-damaged humans showed increased startle potentiation and BLA-silenced rats demonstrated increased startle potentiation, freezing, and reduced escape behavior as compared to controls. Neuroimaging in humans suggested that the BLA reduces passive defensive responses by inhibiting the brainstem via the CeA. Indeed, Timm conditioning potentiated BLA projections onto an inhibitory CeA pathway, and pharmacological activation of this pathway rescued deficient Timm responses in BLA-silenced rats. Our data reveal how the BLA, via the CeA, adaptively regulates escape behavior from imminent threat and that this mechanism is evolutionary conserved across rodents and humans.
Highlights
The amygdala is an almond-shaped group of nuclei in the temporal lobe that is crucial for defensive behaviors in all mammals, including humans (Davis and Whalen, 2001; Phelps and LeDoux, 2005)
Using an MRI probability-mapping method described by Eickhoff et al (2005), we were able to quantify the overlap of each calcification with cytoarchitectonic structure-probability maps of the amygdala sub-regions developed by Amunts et al (2005)
In line with our previous findings in this group (Terburg et al, 2012), in each of the five Urbach-Wiethe disease (UWD) subjects, we found bilateral calcifications that were localized to the basolateral amygdala (BLA) without affecting the central amygdala (CeA) (Figure 1; Video S1)
Summary
The amygdala is an almond-shaped group of nuclei in the temporal lobe that is crucial for defensive behaviors in all mammals, including humans (Davis and Whalen, 2001; Phelps and LeDoux, 2005). Using structural and functional neuroimaging methods in affected individuals, we recently demonstrated that, in this group, there is a focal bilateral neurodegeneration that is restricted to within the BLA without affecting CeA (Terburg et al, 2012). This group of individuals could contribute significantly to crossspecies translation of functions of the different nuclei in the amygdala
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