Time perception of visual events is intertwined with conscious and emotional experiences, yet it remains unknown whether such temporal distortion effect depends on explicit awareness of emotional cues. In this dissertation, we focused on invisible conditioned fear and combined psychophysics, intra-cranial electroencephalography recording (iEEG) and functional magnetic resonance imaging (fMRI) to unlock the cognitive and neural mechanisms through which the invisible conditioned fear may take effect in sub-second time perception.
In study 1，conditioned fear was created by repetitively pairing aversive electrical shocks to one of two sets of luminance gratings with orthogonal orientations. Following the conditioning phase, counter-phase chromatic gratings with the conditioned (CS+) and nonconditioned (CS一)orientations were rendered invisible through flickering at a frequency above the critical flicker fusion (CFF) threshold. In a temporal duration discrimination task, the invisible CS+ flicker was perceived significantly longer than the invisible CS一flicker. Magnitude of this temporal dilation effect doubled when the physical duration of stimulus presented increased from 250ms to SOOms. We roughly explored the extinguishing time course of this effect and found it fading swiftly to nonsignificant within 30 minutes. Asymmetric allocation of attentional sources may not explain the effect, since a control experiment found no difference between the invisible CS+ and CS一flickers in attentional capture. When only one part of the CS+ and CS-flickers were presented and thus all visual features of the gratings to be timed were explicitly visible, however, the temporal dilation effect disappeared. Oppositely, another kind of temporal dilation effect induced by increase of visual saliency of neutral textures was observed in the visible condition only, it disappeared completely when these neutral textures were flickering above CFF threshold and thus rendered invisible.This double dissociation, dependent on visual awareness between conditioned fear and neutral visual saliency, suggests a specific timing mechanism adapted for conditioned fear outside the scope of visual awareness.
In study 2，we studied the neural mechanisms underlying the temporal dilation effect induced by invisible conditioned fear. At first, it cannot be mediated by locally enhanced neural energy in the visual areas: chromatic flickers, though evokes larger neural energy selectively in the visual cortex, failed to dilate time perception relative to the static presentation of its perceptual counterpart. Secondly, this effect was closely related to the amygdala, a hub region for fear processing in the human brain. Intracranial electroencephalography (iEEG) data, recorded from electrodes implanted precisely in the human amygdala of six volunteer epilepsy patients, revealed that,during the temporal duration discrimination task, invisible CS+ flicker evoked local field potential significantly larger than that of the CS一In line with the behavioral findings, when the CS+ and CS一gratings to be timed were explicitly visible, no differential responses were observed in amygdala in vivo. At last, by using functional magnetic resonance imaging (fMRI), we explored in the whole brain what additional regions, together with amygdala, may account for the temporal dilation effect. During a revised oddball timing task, BOLD responses lateralized in the right hemisphere in the amygdala and core regions involved in timing, namely the insula, supplementary motor area (SMA) and inferior frontal gyrus (IFG), were significantly larger for invisible CS+ flicker than that for CS一flicker. These effects of significant BOLD enhancement were selectively tied to the invisible condition, which were nonsignificant while the visible CS+ and CS一were to be timed. Inter-individual correlation analysis revealed that larger BOLD enhancement in these four regions predicted more temporal dilation effect induced by invisible conditioned fear. Dynamic causal modeling analyses revealed that stronger feedforward modulation from the right amygdala to the IFG and Insula, induced by invisible CS+ relative to CS一，was associated with larger temporal dilation effect. These associations were not significant for the connectivity modulation backwards to the amygdala.
Taken together, invisible conditioned fear may significantly dilate perceived temporal duration. This effect may depend on a timing mechanism specifically adapted for conditioned fear outside the scope of visual awareness. More specifically,feedforward rather than feedback connectivity from the amygdala to the insula and IFG in the right hemisphere may mediate the temporal dilation effect induced by invisible conditioned fear.