Distinct visual pathways of threat retrieval in fear-conditioned faces

Abstract

Numerous studies have demonstrated rapid (< 100 ms) visuo-cortical differentiation of threat-associated faces. This may be due to low-spatial frequency (LSF) visual information originating from magnocellular pathways. Yet it remains unclear whether potentially magnocellular fear signals extend beyond evolutionarily prepared emotional faces and whether they are subject to short-term neuroplasticity. If so, spatial frequency characteristics should modulate processing of faces with newly acquired threat-relevance. Furthermore, it is unknown whether sub-bands of the visual spectrum are associated with autonomic arousal. Using a differential fear-conditioning paradigm, this study tested whether early visual attentional capture, indicated by the P1 event-related potential component, prioritizes LSF information of threat-associated faces with neutral expressions. Additionally, it was tested whether such effects would be paralleled by threat differentiation in the skin conductance response (SCR). For contingency aware participants, stimulus ratings confirmed successful fear conditioning and participants showed a selective left-hemispheric enhancement of the P1 in response to LSF threat-faces. By contrast, CS differentiation in the SCR was not modulated by spatial frequencies but by stimulus duration, with longer CS presentations resulting in larger SCR to threat compared to neutral faces. For contingency unaware participants, trial-by-trial amplitudes of P1 and SCR were positively correlated. Data support the notion that magnocellular-cortical pathways adapt quickly to novel threat-associations and facilitate rapid threat retrieval even for perceptually neutral faces. However, at least in the short term, these signals do not necessarily associate with anticipatory arousal in SCR. Impact statementOur electroencephalography (EEG) study provides evidence for distinct contributions of subcortical signals during early visual perception of fear-conditioned faces (P1 event-related potential) but not autonomic arousal (skin conductance response). Instead, skin conductance responses reflected conscious anticipatory arousal irrespective of the visual pathway. Together, these results reveal parallel but dissociable mechanisms of fear perception that are differentially sensitive to visual properties of threat-associated faces.