A visual generalization gradient of conceptual stimuli based on fear acquisition in visual and auditory modalities

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IntroductionFear learning is essential for human survival, as it enables individuals to adaptively respond to future threats based on prior experiences1. Through this mechanism, people can even avoid potentially dangerous situations they have not directly encountered—a phenomenon known as fear generalization2,3. Fear generalization refers to the extension of learned fear responses to stimuli or situations that are similar to the original threatening event3,4. Specifically, a conditioned fear response to a stimulus (CS+) that reliably predicts an unconditioned (aversive) stimulus (US) may generalize to stimuli (GSs) that share similarities with the CS+2,3,4. While fear generalization is a natural and adaptive process that aids in avoiding potential dangers, excessive or maladaptive fear generalization is thought to contribute to the development of anxiety-related disorders, including generalized anxiety disorder, post-traumatic stress disorder, and specific phobias5,6,7,8.Current research on fear generalization predominantly focuses on single sensory modality9,10,11,12,13, such as the visual or auditory sensory, with limited evidence supporting crossmodal fear generalization. For instance, one study presented participants with 10 rings of gradually increasing size (including CS+, CS−, and 8 intermediate-sized GS) to examine fear acquisition and generalization14. The results revealed that participants exhibited stronger fear responses to the CS+ ring and to rings of similar size, compared to the CS−, confirming the presence of fear generalization. Additionally, a visual search task demonstrated that after pairing colors from the blue-green spectrum (489–500 nm) with an electric shock, participants displayed heightened attention to color stimuli similar to the CS+ during the task15. This attentional bias increased as the color more closely resembled the CS+ and diminished as it deviated, illustrating a fear generalization gradient. However, numerous studies suggest that crossmodal information processing enhances individuals’ ability to identify and avoid potential threats more effectively16,17,18. For example, a person bitten by a dog may develop a fear not only of other dogs but also of the sound of barking. This phenomenon, in which fear generalizes across sensory modalities, reflects the transfer of fear responses between visual and auditory stimuli.A recent study investigated crossmodal fear generalization by using images of typewriters and telephones as the conditioned stimuli (vCS+) and the safety stimuli (vCS−), respectively, and their corresponding sounds (typewriter typing and telephone ringing) as generalization stimuli (aGS+ and aGS−)19; There were two groups in their study: a crossmodal group, which watched visual stimuli during the acquisition phase and heard auditory stimuli during the generalization phase, and a unimodal group, which watched visual stimuli in both phases. The crossmodal group showed significantly higher US expectancy ratings for aGS+ compared to aGS−. Notably, the unimodal group exhibited stronger responses to vCS+ than the crossmodal group did to aGS+. These findings provide the first direct evidence of crossmodal fear generalization, demonstrating that fear learned from visual stimuli can generalize to semantically consistent auditory stimuli. This study lays a foundation for further exploration into the mechanisms underlying crossmodal fear generalization and its implications for anxiety-related disorders. However, it should be noted that in the generalization phase of the study conducted by Gerdes et al., the experimental design included only two categories of stimuli (GS+, GS−). Additionally, the measurement of US expectancy rating was the sole assessment method employed during this phase. Thus, it remains unclear whether crossmodal generalization follows a stimulus gradient and what the neural correlates of crossmodal generalization are.Fear generalization extends beyond perceptually similar stimuli to include conceptual similarity as a critical factor13,14,15,20,21,22. For instance, after experiencing a traumatic car accident, an individual may develop fear not only toward other cars but also toward seemingly unrelated vehicles, such as cruise ships or airplanes. This phenomenon illustrates that fear is influenced by deeper conceptual similarity, in addition to perceptual resemblance23. Although these stimuli differ substantially in their sensory features, they are categorized as “vehicles” within the individual’s conceptual framework, thereby eliciting a generalized fear response. This type of fear generalization engages not only perceptual-level mechanisms but also higher-order cognitive processes, such as conceptual representation and analogical reasoning24,25. Research suggests that individuals facing fear-inducing stimuli frequently rely on conceptual thinking rather than solely on direct sensory input25,26. This cognitive mechanism is particularly relevant to understanding the development of anxiety-related emotional disorders. Patients with anxiety disorders often exhibit exaggerated fear responses to stimuli that are unrelated to the original traumatic event, likely due to excessive analogy and generalization of “similar” concepts26,27. Understanding the role of conceptual similarity in fear generalization provides important insights into the pathological mechanisms of anxiety disorders. Furthermore, it highlights the potential for developing novel therapeutic strategies focused on cognitive interventions and emotion regulation to address excessive fear generalization.In this context, theories of learning transfer and semantic consistency offer robust frameworks for understanding the role of conceptual stimuli in the crossmodal fear generalization15,28,29,30. Learning transfer is an essential evolutionary mechanism that allows organisms to apply acquired knowledge to novel situations, facilitating predictions of future events15,28. When stimuli across different sensory modalities share similarities in cognitive processing, they can enhance the transfer of learned associations29. For instance, Bratzke et al. demonstrated the effects of crossmodal transfer in a temporal discrimination task, showing that training with auditory stimuli improved temporal discrimination performance in the visual modality30. Similarly, in the study of fear generalization, it has been observed that fear responses can generalize not only to perceptually similar stimuli (e.g., those with similar shapes or sizes) but also to stimuli that are conceptually and semantically related28. These findings indicate that conceptually similar stimuli may facilitate crossmodal fear generalization between different sensory modalities, extending the understanding of how fear responses are transferred and generalized across sensory and conceptual domains.Neuroscientific studies have demonstrated that the amygdala, hippocampus, and prefrontal cortex (PFC) play central roles in fear learning and generalization31,32,33,34,35,36,37,38. Among these, the PFC is crucial for regulating fear emotions and inhibiting amygdala activity, thereby modulating the expression of fear responses39,40,41,42,43,44. Specifically, the medial PFC has been implicated in top-down regulation of fear, influencing both the expression and suppression of fear responses triggered by cues36,37. For instance, research on patients with mPFC dysfunction has revealed that, compared to healthy controls, these individuals exhibit significantly enhanced amygdala activation when exposed to threatening stimuli38. Moreover, previous research has also indicated that when the GS more closely resembles the CS+, it elicits a more pronounced activation of the mPFC45. In summary, existing research underscores the significant relationship between mPFC activity and both fear learning and generalization.Building on previous findings, we adopted a crossmodal conceptual fear generalization experimental design to investigate the presence of a crossmodal fear generalization gradient. First, we extended the visual generalization paradigm from the study by Gerdes et al. to include auditory generalization. Specifically, our crossmodal generalization design transitioned from auditory stimuli during the acquisition phase to visual stimuli during the generalization phase. In the unimodal group, visual stimuli were presented in both phases, whereas in the crossmodal group, auditory stimuli were used during the acquisition phase and visual stimuli during the generalization phase. Second, the GSs were designed to extend beyond modality to include conceptual generalization. The stimuli in the generalization phase were conceptually categorized as highly similar, moderately similar, or minimally similar to the CS+. This approach allowed us to explore generalization gradients both across modalities and conceptual dimensions. Finally, given the critical role of the mPFC in fear processing and regulation, we employed fNIRS to examine neural activities in this region. fNIRS is a non-invasive neuroimaging technique that measures changes in hemoglobin concentration in the brain, reflecting neural activity41. The advantage of the fNIRS is less sensitive to head motion and eliminates the potential auditory interference caused by scanner noise (e.g., fMRI) during fear acquisition42,43. In addition to employing fNIRS to assess frontal cortex activity, we measured US expectancy ratings and SCR as behavioral and physiological indicators of fear learning and generalization.Our study proposed two hypotheses: (1) Both the unimodal and crossmodal groups will successfully acquire and generalize fear, demonstrating a generalization gradient effect. Specifically, fear responses will increase as the conceptual similarity between the GSs and the CS+ increases19. (2) The HbO activities of the mPFC will show a growing trend as the conceptual similarity between the GSs and the CS+ increases45.ResultsUS expectancy ratingsThe main effect of stimulus type on US expectancy ratings was significant in the acquisition phase (F1, 79 = 1312.167, p