Distinct Visual Pathways of Threat Retrieval in Fear-Conditioned Faces

Many have demonstrated rapid (< 100 ms) visuo-cortical differentiation of threat-associated faces. This may go back to low-spatial frequency (LSF) visual information originating from magnocellular pathways. Yet it remains unknown whether potentially magnocellular fear signals extend beyond evolutionarily prepared emotional faces. If so, spatial frequency characteristics should modulate visual processing of faces with newly acquired threat-relevance. Furthermore, it is unclear whether sub-bands of the visual spectrum are associated with autonomic arousal. Using a differential fear-conditioning paradigm (n = 68), this study tested whether early visual attentional capture, indicated by the P1 event-related potential component, face encoding, indicated by the N1 component, and autonomic arousal, indicated by skin conductance responses (SCR), prioritizes LSF information of threat-associated faces with neutral expressions during fear retrieval. Additionally, correlations tested whether the same subcortical system underlies the P1 and SCR. Stimulus ratings and N1 amplitudes confirmed successful fear acquisition. During fear retrieval, the P1 showed a selective left-hemispheric enhancement in response to LSF threat-faces. By contrast, the N1 was sensitive to spatial frequency but not fear-relevance. CS-differentiation in the SCR was not modulated by spatial frequency but longer CS presentations resulting in larger fear differentiation. Amplitudes of P1 and SCR were positively correlated only for safety faces. Data support the notion that magnocellular-cortical pathways adapt quickly to novel threat-associations and facilitate rapid threat retrieval in early visual attention, but not face encoding, even for perceptually neutral faces. At least in the present paradigm, subcortical fear pathways do not associate with anticipatory arousal in SCR.