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, suggesting that anxiety may improve the visual system’s discrimination of threatening social stimuli.

Aversive Conditioning of Spatial Position Sharpens Neural Population-Level Tuning in Visual Cortex and Selectively Alters Alpha-Band Activity

“…Furthermore, sharpened visuocortical responses to aversively paired screen locations developed within minutes of exposure to the noxious noise stimulus, transitioning to generally elevated ssVEP responses undifferentiated by proximity to the CS 1 in the second half of acquisition trials. The DOG pattern of visuocortical response change across the range of tested spatial positions observed here closely mirrors responses to oriented gratings (McTeague et al, 2015) and faces (Stegmann et al, 2020) parametrically varied in similarity to conditioned threat cues. The finding that altered tuning of the ssVEP emerges whether the lowlevel 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 operating at this early stage of the associative learning process.…”

Social buffering of human fear is shaped by gender, social concern, and the presence of real vs virtual agents

“…However, not all humans are equally sociable. In some individuals, the presence of another person induces concern and anxiety, paralleled by an increase in autonomic fear and hormonal stress responses [ 19 – 21 ]. The sensitivity to anxiety in social situations has been defined as an independent dimension of human anxiety, known as social concern [ 22 – 25 ].…”

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 lowlevel 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.…”