Mode of functional connectivity in amygdala pathways dissociates level of awareness for signals of fear - PubMed (original) (raw)

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Mode of functional connectivity in amygdala pathways dissociates level of awareness for signals of fear

Leanne M Williams et al. J Neurosci. 2006.

Abstract

Many of the same regions of the human brain are activated during conscious attention to signals of fear and in the absence of awareness for these signals. The neural mechanisms that dissociate level of awareness from activation in these regions remain unknown. Using functional magnetic resonance imaging with connectivity analysis in healthy human subjects, we demonstrate that level of awareness for signals of fear depends on mode of functional connectivity in amygdala pathways rather than discrete patterns of activation in these pathways. Awareness for fear relied on negative connectivity within both cortical and subcortical pathways to the amygdala, suggesting that reentrant feedback may be necessary to afford such awareness. In contrast, responses to fear in the absence of awareness were supported by positive connections in a direct subcortical pathway to the amygdala, consistent with the view that excitatory feedforward connections along this pathway may be sufficient for automatic responses to "unseen" fear.

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Figures

Figure 1.

Figure 1.

Skin conductance responses elicited by fear relative to neutral under conscious and nonconscious perception conditions. The amplitude of SCRs is shown in microsiemens. Fear elicited enhanced SCRs relative to neutral under both awareness conditions.

Figure 2.

Figure 2.

Statistical parameter maps for the regions of interest activated in response to conscious fear (left) (vs neutral) and nonconscious fear (right) (vs neutral). For conscious fear, significant (p < 0.05, small-volume corrected) activations were observed in the amygdala, thalamus (including LGN), anterior cingulate (dorsal and ventral portions), and visual cortices, both striate and extrastriate (including fusiform and inferior occipital gyri). Activations were also observed in the superior colliculus and hypothalamus regions of the brainstem. For nonconscious fear, significant (p < 0.05, small-volume corrected) activity was observed in the bilateral amygdala and brainstem regions consistent with the superior colliculus and hypothalamus. Activity was also observed in the thalamic pulvinar (rather than LGN), in the ventral (but not dorsal) anterior cingulate, and in the extrastriate (right inferior occipital gyrus) but not striate visual cortex. Coordinates for these regions of significant activation are presented in Table 1. A, Amygdala; V1, striate visual cortex; SC, superior colliculus of the brainstem; Pulv, pulvinar of the thalamus; Th, thalamus; Hy, hypothalamus; dMPFC, dorsal MPFC; vMPFC, ventral MPFC.

Figure 3.

Figure 3.

Statistical parameter maps for the conjunction of activation in regions of interest to both conscious and nonconscious fear (vs neutral). In conjunction, these conditions showed significant (p < 0.05, small-volume corrected) activations in the amygdala, thalamus (encompassing regions consistent with LGN and pulvinar), brainstem, and extrastriate GOi and Gf regions. Small regions of common, trend-level activation were also observed in a dorsal portion of the MPFC and ACC. There were no corresponding clusters of common activity in the ventral prefrontal or striate visual cortices. A, Amygdala; dMPFC, dorsal MPFC; Hy, hypothalamus; Pulv, pulvinar of the thalamus; SC, superior colliculus of the brainstem; Th, thalamus.

Figure 4.

Figure 4.

Psychophysiological interaction analyses showing the functional connectivity between the amygdala and the regions of interest during conscious fear (A) and nonconscious fear (B) relative to neutral. Red arrows represent positive functional connectivity between the amygdala and regions of interest, and blue arrows represent negative connectivity. Conscious fear (A) was distinguished by negative functional connectivity in a cortical (striate–thalamic LGN) amygdala pathway, with links to both left and right amygdala. Negative connectivity was also observed between the bilateral amygdala and other cortical regions (extrastriate and dorsal medial prefrontal), as well as the subcortical brainstem region. Conscious fear elicited positive functional connectivity between the bilateral amygdala and dorsal ACC. The right amygdala in particular also covaried positively with the ventral ACC, extrastriate, and periaqueductal gray regions of the brainstem (data not shown). Nonconscious fear (B), in contrast, elicited positive functional connectivity in a subcortical (brainstem–thalamic pulvinar) amygdala pathway, localized to the right amygdala. Positive relationships were also observed between the bilateral amygdala and rostral regions of the medial prefrontal and ACC. For nonconscious fear, the right amygdala showed negative relationships with additional cortical regions: the extrastriate and ventral medial prefrontal cortices (data not shown). A, Amygdala; B, brainstem; dACC, dorsal ACC; dMPFC, dorsal MPFC; vMPFC, ventral MPFC.

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