Pathways for fear perception: Modulation of amygdala activity by thalamo-cortical systems

Neuroscience Institute of Schizophrenia and Allied Disorders (NISAD), Darlinghurst, NSW, Australia.
NeuroImage (Impact Factor: 6.36). 06/2005; 26(1):141-8. DOI: 10.1016/j.neuroimage.2005.01.049
Source: PubMed

ABSTRACT Effective perception of fear signals is crucial for human survival and the importance of the amygdala in this process is well documented. Animal, lesion and neuroimaging studies indicate that incoming sensory signals of fear travel from thalamus to amygdala via two neural pathways: a direct subcortical route and an indirect pathway via the sensory cortex. Other lines of research have demonstrated prefrontal modulation of the amygdala. However, no study to date has examined the prefrontal modulation of the thalamo-cortico-amygdala pathways in vivo. We used psychophysiological and physiophysiological interactions to examine the functional connectivity within thalamus, amygdala and sensory (inferior occipital, fusiform) cortices, and the modulation of these networks by the anterior cingulate cortex (ACC). Functional magnetic resonance imaging (fMRI) data were acquired for 28 healthy control subjects during a fear perception task, with neutral as the 'baseline' control condition. Main effect analysis, using a region of interest (ROI) approach, confirmed that these regions are part of a distributed neural system for fear perception. Psychophysiological interactions revealed an inverse functional connectivity between occipito-temporal visual regions and the left amygdala, but a positive connectivity between these visual region and the right amygdala, suggesting that there is a hemispheric specialization in the transfer of fear signals from sensory cortices to amygdala. Physiophysiological interactions revealed a dorsal-ventral division in ACC modulation of the thalamus-sensory cortex pathway. While the dorsal ACC showed a positive modulation of this pathway, the ventral ACC exhibited an inverse relationship. In addition, both the dorsal and ventral ACC showed an inverse interaction with the direct thalamus-amygdala pathway. These findings suggest that thalamo-amygdala and cortical regions are involved in a dynamic interplay, with functional differentiation in both lateralized and ventral/dorsal gradients. Breakdowns in these interactions may give rise to affect-related symptoms seen in a range of neuropsychiatric disorders.

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Available from: Leanne M Williams, Feb 24, 2015
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    • "Based on its putative role in fear conditioning, a seed was placed in right amygdala [MNI [22] [26] [212]; coordinates obtained from Das et al., 2005] to examine functional connectivity from and to this region. A set of regions was found to drive neural responses in amygdala across experimental phases for both CS1 and CS2 (habituation CS1: size 5 62, habituation CS2: size 5 24, conditioning CS1: 45, conditioning CS2: 136, extinction CS1: size 5 73, extinction CS2: size 5 84). "
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    ABSTRACT: Despite a strong focus on the role of the amygdala in fear conditioning, recent works point to a more distributed network supporting fear conditioning. We aimed to elucidate interactions between subcortical and cortical regions in fear conditioning in humans. To do this, we used two fearful faces as conditioned stimuli (CS) and an electrical stimulation at the left hand, paired with one of the CS, as unconditioned stimulus (US). The luminance of the CS was rhythmically modulated leading to "entrainment" of brain oscillations at a predefined modulation frequency. Steady-state responses (SSR) were recorded by MEG. In addition to occipital regions, spectral analysis of SSR revealed increased power during fear conditioning particularly for thalamus and cerebellum contralateral to the upcoming US. Using thalamus and amygdala as seed-regions, directed functional connectivity was calculated to capture the modulation of interactions that underlie fear conditioning. Importantly, this analysis showed that the thalamus drives the fusiform area during fear conditioning, while amygdala captures the more general effect of fearful faces perception. This study confirms ideas from the animal literature, and demonstrates for the first time the central role of the thalamus in fear conditioning in humans. Hum Brain Mapp, 2015. © 2015 Wiley Periodicals, Inc. © 2015 Wiley Periodicals, Inc.
    Human Brain Mapping 08/2015; DOI:10.1002/hbm.22940 · 5.97 Impact Factor
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    • "Studies also found that the connectivity between different subregions of the MPFC and amygdala may make diverse effects on emotion function. For example, when people did a fear perception task, there was a dorsal-ventral division in ACC modulation of the thalamus-sensory cortex pathway, with a positive modulation of this pathway from dorsal ACC and a negative one from the ventral ACC (Das et al., 2005). In addition, Satterthwaite et al. (2011) demonstrated that the amygdala responded preferentially to threatening (fearful or angry) faces and had increased connectivity during threat trials with the OFC. "
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    ABSTRACT: The Default Mode Network (DMN) has been found to be involved in various domains of cognitive and social processing. The present article will review brain connectivity results related to the DMN in the fields of social understanding of others: emotion perception, empathy, theory of mind, and morality. Most of the reviewed studies focused on healthy subjects with no neurological and psychiatric disease, but some studies on patients with autism and psychopathy will also be discussed. Common results show that the medial prefrontal cortex (MPFC) plays a key role in the social understanding of others, and the subregions of the MPFC contribute differently to this function according to their roles in different subsystems of the DMN. At the bottom, the ventral MPFC in the medial temporal lobe (MTL) subsystem and its connections with emotion regions are mainly associated with emotion engagement during social interactions. Above, the anterior MPFC (aMPFC) in the cortical midline structures (CMS) and its connections with posterior and anterior cingulate cortex contribute mostly to making self-other distinctions. At the top, the dorsal MPFC (dMPFC) in the dMPFC subsystem and its connection with the temporo-parietal junction (TPJ) are primarily related to the understanding of other's mental states. As behaviors become more complex, the related regions in frontal cortex are located higher. This reflects the transfer of information processing from automatic to cognitive processes with the increase of the complexity of social interaction. Besides the MPFC and TPJ, the connectivities of posterior cingulate cortex (PCC) also show some changes during tasks from the four social fields. These results indicate that the DMN is indispensable in the social understanding of others.
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    • "Although without performing tractography it is difficult to precisely identify the specific thalamic nuclei and cortical regions connected by the affected tracts, based on the rostro-caudal location of this cluster the fibers affected likely connect the thalamus with occipital or temporal cortices [96]. Interestingly, thalamo-cortical systems modulate amygdala activity, and are involved in the perception of fear [122]. Cortico-thalamic circuits are implicated in the pathogenesis of mood disorders [123]. "
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    Biology of Mood and Anxiety Disorders 12/2013; 3(1):21. DOI:10.1186/2045-5380-3-21
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