Social aversive generalization learning sharpens the tuning of visuocortical neurons to facial identity cues

Abstract

Defensive system activation promotes heightened perception of threat signals, and excessive attention to threat signals has been discussed as a contributory factor in the etiology of anxiety disorders. However, a mechanistic account of attentional modulation during fear-relevant processes, especially during fear generalization remains elusive. To test the hypothesis that social fear generalization prompts sharpened tuning in the visuocortical representation of social threat cues, 67 healthy participants underwent differential fear conditioning, followed by a generalization test in which participants viewed faces varying in similarity with the threat-associated face. We found that generalization of social threat sharpens visuocortical tuning of social threat cues, whereas ratings of fearfulness showed generalization, linearly decreasing with decreasing similarity to the threat-associated face. Moreover, individuals who reported greater anxiety in social situations also showed heightened sharpened tuning of visuocortical neurons to facial identity cues, indicating the behavioral relevance of visuocortical tuning during generalization learning.

Aversive Conditioning of Spatial Position Sharpens Neural Population-level Tuning in Visual Cortex and Selectively Reduces Alpha-band Activity

“…Within the visual system, suppression mechanisms are thought to contribute to transforming broadly tuned excitatory outputs from lateral geniculate nucleus (LGN) relay cells into the more narrowly feature selective responses observed in visual cortex (Shapley, Hawken, & Xing, 2007; Isaacson & Scanziani, 2011; Angelucci et al, 2017; but see Priebe & Ferster, 2008). The difference-of-gaussian pattern of visuocortical response changes across the range of tested spatial positions observed here closely mirrors responses to orientated gratings (McTeague, Gruss, & Keil, 2015) and faces (Stegmann, Ahrens, Pauli, Keil, & Wieser, 2020) parametrically varied in similarity to conditioned threat cues. The finding that altered tuning of the ssVEP emerges within visual cortex whether the low-level visual feature predicting an upcoming aversive event is a particular orientation or a specific visual field location points to response sharpening as a common mechanism that is operating at this early stage of the associative learning process.…”

Associative learning shapes visual discrimination in a web-based classical conditioning task

“…First, the JND is only a point measure of discrimination acuity, thus obscuring potential nongradual effects on visual discrimination along the perceptual continuum. These nongradual effects have already been identified, for example, for visuocortical activation patterns during aversive generalization learning paradigms using grating stimuli 10 , 25 or faces 18 . In this line of studies, visuocortical activity as an index of sensory engagement increased with increasing similarity to the threat-related stimulus for all except for the most similar generalization stimuli, which elicited decreased activity.…”

“…Mirroring the organization of visual receptive fields, threat-related sensory amplification has been reported for visual stimuli differing in orientation 10,11 , spatial frequency 12 , location 13 , and color 14 . However, enhanced visuocortical responses have also been observed for more complex visual stimuli, like geometric symbols 15,16 , pictures of virtual rooms 17 and facial identities 18,19 .…”

Acute stress leaves fear generalization in healthy individuals intact

“…Specifically, studies repeatedly associated activation in the anterior insula (aI), the dorsomedial prefrontal cortex, and the bilateral inferior parietal lobe with fear excitation, whereas activation of the bilateral ventral hippocampus, the ventromedial prefrontal cortex (vmPFC) and the precuneus cortex is associated with fear inhibition (Dunsmoor, Prince, Murty, Kragel, & LaBar, 2011;Greenberg, Carlson, Cha, Hajcak, & Mujica-Parodi, 2013;Lissek, Bradford, et al, 2014;Onat & Büchel, 2015). In line with behavioral studies that showed that fear generalization can be independent of perception (Bennett, Vervoort, Boddez, Hermans, & Baeyens, 2015;Dunsmoor, Martin, & LaBar, 2012;Dunsmoor & Murphy, 2014), studies investigating the neural mechanisms showed partly sharpened fear generalization on a neural level compared to the behavioral level, indicating that processes other than perception add to fear generalization (Onat & Büchel, 2015;Stegmann, Ahrens, Pauli, Keil, & Wieser, 2020).…”