Department of Psychology, Florida State University, Tallahassee, Florida 32306
Department of Psychology, Florida State University, Tallahassee, Florida 32306.
J Neurosci. 2021 Apr 7;41(14):3222-3233. doi: 10.1523/JNEUROSCI.2325-20.2021. Epub 2021 Feb 23.
Growing animal data evince a critical role of the sensory cortex in the long-term storage of aversive conditioning, following acquisition and consolidation in the amygdala. Whether and how this function is conserved in the human sensory cortex is nonetheless unclear. We interrogated this question in a human aversive conditioning study using multidimensional assessments of conditioning and long-term (15 d) retention. Conditioned stimuli (CSs; Gabor patches) were calibrated to differentially activate the parvocellular (P) and magnocellular (M) visual pathways, further elucidating cortical versus subcortical mechanisms. Full-blown conditioning and long-term retention emerged for M-biased CS (vs limited effects for P-biased CS), especially among anxious individuals, in all four dimensions assessed: threat appraisal (threat ratings), physiological arousal (skin conductance response), perceptual learning [discrimination sensitivity (') and response speed], and cortical plasticity [visual evoked potentials (VEPs) and cortical current density]. Interestingly, while behavioral, physiological, and VEP effects were comparable at immediate and delayed assessments, the cortical substrates evolved markedly over time, transferring from high-order cortices [inferotemporal/fusiform cortex and orbitofrontal cortex (OFC)] immediately to the primary and secondary visual cortex after the delay. In sum, the contrast between P- and M-biased conditioning confirms privileged conditioning acquisition via the subcortical pathway while the immediate cortical plasticity lends credence to the triadic amygdala-OFC-fusiform network thought to underlie threat processing. Importantly, long-term retention of conditioning in the basic sensory cortices supports the conserved role of the human sensory cortex in the long-term storage of aversive conditioning. A growing network of neural substrates has been identified in threat learning and memory. The sensory cortex plays a key role in long-term threat memory in animals, but such a function in humans remains unclear. To explore this problem, we conducted multidimensional assessments of immediate and delayed (15 d) effects of human aversive conditioning. Behavioral, physiological, and scalp electrophysiological data demonstrated conditioning effects and long-term retention. High-density EEG intracranial source analysis further revealed the cortical underpinnings, implicating high-order cortices immediately and primary and secondary visual cortices after the long delay. Therefore, while high-order cortices support aversive conditioning acquisition (i.e., threat learning), the human sensory cortex (akin to the animal homolog) underpins long-term storage of conditioning (i.e., long-term threat memory).
动物研究数据表明，在杏仁核中获得和巩固之后，感觉皮层在长期储存厌恶条件反射中起着关键作用。然而，这种功能在人类感觉皮层中是否以及如何得到保留尚不清楚。我们在一项人类厌恶条件反射研究中使用条件反射和长期（15 天）保留的多维评估来研究这个问题。条件刺激（CS；Gabor 补丁）被校准为以不同方式激活小细胞（P）和大细胞（M）视觉通路，进一步阐明了皮质与皮质下机制。对于 M 偏向 CS（相比之下，P 偏向 CS 的效果有限），出现了完全的条件反射和长期保留，尤其是在所有四个评估维度上：威胁评估（威胁评分）、生理唤醒（皮肤电导反应）、知觉学习[辨别敏感性（'）和反应速度]和皮质可塑性[视觉诱发电位（VEPs）和皮质电流密度]。有趣的是，虽然行为、生理和 VEP 效应在即时和延迟评估中是可比的，但皮质基质随时间的推移发生了显著变化，从高级皮质（颞下/梭状回和眶额皮质（OFC））立即转移到延迟后的初级和次级视觉皮质。总之，P-和 M-偏向条件反射的对比证实了通过皮质下途径获得优先条件反射的能力，而即时皮质可塑性则证明了被认为是威胁处理基础的三突触杏仁核-OFC-梭状回网络的存在。重要的是，在基本感觉皮质中保留条件反射支持人类感觉皮质在长期储存厌恶条件反射中的保守作用。在威胁学习和记忆中已经确定了一个不断增长的神经基质网络。感觉皮层在动物的长期威胁记忆中起着关键作用，但在人类中这种功能尚不清楚。为了探讨这个问题，我们对人类厌恶条件反射的即时和延迟（15 天）效果进行了多维评估。行为、生理和头皮脑电图数据表明存在条件反射效应和长期保留。高密度 EEG 颅内源分析进一步揭示了皮质基础，表明高级皮质立即和长时间延迟后的初级和次级视觉皮质。因此，虽然高级皮质支持厌恶条件反射的获得（即威胁学习），但人类感觉皮层（类似于动物同源物）支持条件反射的长期储存（即长期威胁记忆）。
