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The Journal of Neuroscience, September 6, 2006, 26(36):9264-9271; doi:10.1523/JNEUROSCI.1016-06.2006

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Behavioral/Systems/Cognitive
Mode of Functional Connectivity in Amygdala Pathways Dissociates Level of Awareness for Signals of Fear

Leanne M. Williams,^1,2 Pritha Das,^1,3 Belinda J. Liddell,¹ Andrew H. Kemp,^1,2 Christopher J. Rennie,^1,4 and Evian Gordon^1,2,5

¹The Brain Dynamics Centre, Westmead Millenium Institute and University of Sydney, ²Psychological Medicine, Western Clinical School, University of Sydney, Westmead Hospital, Westmead, Sydney, New South Wales, 2145, Australia, ³Neuroscience Institute of Schizophrenia and Allied Disorders, Darlinghurst, New South Wales, 2010, Australia, ⁴Diagnostic Physics, Westmead Hospital, Westmead, Sydney, New South Wales, 2145, Australia, and ⁵Brain Resource International Database, Brain Resource Company, Ultimo, New South Wales, 2007, Australia

Correspondence should be addressed to Assoc. Prof. Leanne M. Williams, Brain Dynamics Centre, Westmead Millenium Institute, Westmead Hospital, Westmead, New South Wales, 2145, Australia. Email: lea{at}psych.usyd.edu.au

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.

Key words: functional brain imaging; connectivity; amygdala; medial prefrontal cortex; amygdala; emotion

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Received March 8, 2006; revised July 12, 2006; accepted July 17, 2006.

Correspondence should be addressed to Assoc. Prof. Leanne M. Williams, Brain Dynamics Centre, Westmead Millenium Institute, Westmead Hospital, Westmead, New South Wales, 2145, Australia. Email: lea{at}psych.usyd.edu.au

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