Mode of Functional Connectivity in Amygdala Pathways Dissociates Level of Awareness for Signals of Fear

Westmead Hospital, Sydney, New South Wales, Australia
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 10/2006; 26(36):9264-71. DOI: 10.1523/JNEUROSCI.1016-06.2006
Source: PubMed


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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Available from: Leanne M Williams, Feb 08, 2015
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    • "With regard to the processing of emotional aspects of scenes, there is some evidence suggesting that the pulvinar and superior colliculus act as a pathway to amygdala during the preattentive processing of fearful faces (Morris et al., 1998, 2001; Tamietto and de Gelder, 2010; Williams et al., 2006), however the meaning of these effects are controversial (Cowey, 2004; Pessoa and Adolphs, 2010; Pessoa and Ungerleider, 2004), and intracranial studies in the primate (Nakamura et al., 1994; Nishijo et al., 2007; Sugase et al.,1999) and human (Oya et al., 2002; Krolak-Salmon et al., 2004; Pourtois et al., 2010) report emotional discrimination in the amygdala much later than would be expected via a purely subcortical route. Other evidence in humans suggests that while the pulvinar is unlikely to contain the processing power necessary to discriminate complex visual information (Grieve et al., 2000; Petersen et al., 1985), it may be involved indirectly in the emotional evaluation process (Ward et al., 2005; Padmala et al., 2010) perhaps reflecting the enhanced visual attention to motivationally relevant features of visual stimuli. "
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    ABSTRACT: Emotional scene perception is associated with enhanced activity in ventral occipitotemporal cortex and amygdala. While a growing body of research supports the perspective that emotional perception is organized via amygdala feedback to rostral ventral visual cortex, the contributions of high-order thalamic structures strongly associated with visual attention, specifically the mediodorsal nucleus and pulvinar, have not been well investigated. Here we sample the activity of amygdala, MDN, pulvinar, and extrastriate ventral visual regions with fMRI as a group of participants view a mixed series of pleasant, neutral, and unpleasant natural scenes, balanced for basic perceptual characteristics. The results demonstrate that all regions showed enhanced activity during emotionally arousing relative to neutral scene perception. Consistent with recent research, the latency of emotional discrimination across subcortical and visual cortical regions suggests a role for the amygdala in the early evaluation of scene emotion. These data support the perspective that higher order visual thalamic structures are sensitive to the emotional value of complex scene stimuli, and may serve in concert with amygdala and fusiform gyrus to modulate visual attention toward motivationally relevant cues.
    Brain Research 08/2014; 1587(1). DOI:10.1016/j.brainres.2014.08.061 · 2.84 Impact Factor
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    • "Previous work has also shown that both disgusted and fearful expressions can be perceived independently of awareness (e.g., Smith, in press). Using various methods to render stimuli invisible, neuroimaging studies demonstrated that the amygdala is involved in the non-conscious processing of emotional faces (e.g., Whalen et al., 1998; Morris et al., 1999; Pasley et al., 2004; Williams et al., 2004, 2006; Jiang and He, 2006; but see Phillips et al., 2004). Scarce studies found support for an involvement of the insula in the non-conscious processing of emotional stimuli (e.g., Sabatini et al., 2009; but see, Anderson et al., 2003, and Phillips et al., 2004, for results that speak against automatic facial expression processing in the insula). "
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    ABSTRACT: Previous studies have shown that complex visual stimuli, such as emotional facial expressions, can influence brain activity independently of the observers’ awareness. Little is known yet, however, about the “informational correlates” of consciousness—i.e., which low-level information correlates with brain activation during conscious vs. non-conscious perception. Here, we investigated this question in the spatial frequency (SF) domain. We examined which SFs in disgusted and fearful facial expressions modulate activation in the insula and amygdala over time and as a function of awareness, using a combination of intracranial event-related potentials (ERPs), SF Bubbles (Willenbockel et al., 2010a), and Continuous Flash Suppression (CFS; Tsuchiya and Koch, 2005). Patients implanted with electrodes for epilepsy monitoring viewed face photographs (13° x 7°) that were randomly SF filtered trial-by-trial. In the conscious condition, the faces were visible; in the non-conscious condition, they were rendered invisible using CFS. Data were analyzed by performing multiple linear regressions on the SF filters from each trial and the transformed ERP amplitudes across time. The resulting classification images suggest that many SFs are involved in the conscious and non-conscious perception of emotional expressions, with those between 6 and 10 cycles per face width being particularly important early on. The results also revealed qualitative differences between the awareness conditions for both regions. Non-conscious processing relied on low SFs more and was faster than conscious processing. Overall, our findings are consistent with the idea that different pathways are employed for the processing of emotional stimuli under different degrees of awareness. The present study represents a first step to mapping with a high temporal resolution how SF information “flows” through the emotion-processing network and to shedding light on the informational correlates of consciousness in general.
    Frontiers in Psychology 07/2012; 3:237. DOI:10.3389/fpsyg.2012.00237 · 2.80 Impact Factor
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    • "More specifically, these abnormalities include deficits in emotion perception (Chan et al. 2010) and emotion control (Henry et al. 2007). Previous imaging studies have revealed aberrant functional responses of brain areas strongly associated with emotion processing, in particular : the amygdala, implicated in processing of emotionally aversive stimuli (Breiter et al. 1996 ; Morris et al. 1996 ; LaBar et al. 1998 ; Yang et al. 2002 ; Suslow et al. 2006 ; Adolphs, 2008, 2010 ; Blasi et al. 2009a); the prefrontal cortex (PFC), involved in cognitive evaluation of stimuli and modulation of emotional responses (Hariri et al. 2003 ; Ochsner & Gross, 2005 ; Tessitore et al. 2005 ; Williams et al. 2006) ; and the striatum (Gur et al. 2002 ; Williams et al. 2004 ; Das et al. 2007 ; Li et al. 2010), important for avoidance learning (Jensen et al. 2003 ; Menon et al. 2007), avoidance responses to threatening stimuli (Schlund et al. 2010) and learning behavioural actions allowing control over fearful responses (Delgado et al. 2009). This literature consistently suggests abnormal physiology associated with emotion processing in patients with schizophrenia . "
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    ABSTRACT: BACKGROUND: Emotion dysregulation is a key feature of schizophrenia, a brain disorder strongly associated with genetic risk and aberrant dopamine signalling. Dopamine is inactivated by catechol-O-methyltransferase (COMT), whose gene contains a functional polymorphism (COMT Val158Met) associated with differential activity of the enzyme and with brain physiology of emotion processing. The aim of the present study was to investigate whether genetic risk for schizophrenia and COMT Val158Met genotype interact on brain activity during implicit and explicit emotion processing.MethodA total of 25 patients with schizophrenia, 23 healthy siblings of patients and 24 comparison subjects genotyped for COMT Val158Met underwent functional magnetic resonance imaging during implicit and explicit processing of facial stimuli with negative emotional valence. RESULTS: We found a main effect of diagnosis in the right amygdala, with decreased activity in patients and siblings compared with control subjects. Furthermore, a genotype×diagnosis interaction was found in the left middle frontal gyrus, such that the effect of genetic risk for schizophrenia was evident in the context of the Val/Val genotype only, i.e. the phenotype of reduced activity was present especially in Val/Val patients and siblings. Finally, a complete inversion of the COMT effect between patients and healthy subjects was found in the left striatum during explicit processing. CONCLUSIONS: Overall, these results suggest complex interactions between genetically determined dopamine signalling and risk for schizophrenia on brain activity in the prefrontal cortex during emotion processing. On the other hand, the effects in the striatum may represent state-related epiphenomena of the disorder itself.
    Psychological Medicine 05/2012; 43(2):1-14. DOI:10.1017/S0033291712001134 · 5.94 Impact Factor
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