Lyon Neuroscience Research Center, CRNL; INSERM, U1028; CNRS, UMR5292; F-69000, France
University Lyon 1, Lyon, F-69000, France.
J Neurosci. 2022 Jan 19;42(3):474-486. doi: 10.1523/JNEUROSCI.0601-21.2021. Epub 2021 Nov 24.
Predictive coding accounts of brain functions profoundly influence current approaches to perceptual synthesis. However, a fundamental paradox has emerged, that may be very relevant for understanding hallucinations, psychosis, or cognitive inflexibility: in some situations, surprise or prediction error-related responses can decrease when predicted, and yet, they can increase when we know they are predictable. This paradox is resolved by recognizing that brain responses reflect precision-weighted prediction error. This presses us to disambiguate the contributions of precision and prediction error in electrophysiology. To meet this challenge for the first time, we appeal to a methodology that couples an original experimental paradigm with fine dynamic modeling. We examined brain responses in healthy human participants ( = 20; 10 female) to unexpected and expected surprising sounds, assuming that the latter yield a smaller prediction error but much more amplified by a larger precision weight. Importantly, addressing this modulation requires the modeling of trial-by-trial variations of brain responses, that we reconstructed within a fronto-temporal network by combining EEG and MEG. Our results reveal an adaptive learning of surprise with larger integration of past (relevant) information in the context of expected surprises. Within the auditory hierarchy, this adaptation was found tied down to specific connections and reveals in particular precision encoding through neuronal excitability. Strikingly, these fine processes are automated as sound sequences were unattended. These findings directly speak to applications in psychiatry, where specifically impaired precision weighting has been suggested to be at the heart of several conditions such as schizophrenia and autism. In perception as Bayesian inference and learning, context sensitivity expresses as the precision weighting of prediction errors. A subtle mechanism that is thought to lie at the heart of several psychiatric conditions. It is thus critical to identify its neurophysiological and computational underpinnings. We revisit the passive auditory oddball paradigm by manipulating sound predictability and use a twofold modeling approach to simultaneous EEG-MEG recordings: (1) trial-by-trial modeling of cortical responses reveals a context-sensitive perceptual learning process; (2) the dynamic causal modeling (DCM) of evoked responses uncovers the associated changes in synaptic efficacy. Predictability discloses a link between precision weighting and self-inhibition of superficial pyramidal (SP) cells, a result that paves the way to a fine description of healthy and pathologic perception.
预测编码对大脑功能的解释深刻地影响了当前对感知合成的研究方法。然而,一个基本的悖论出现了,这对于理解幻觉、精神分裂症或认知灵活性可能非常重要:在某些情况下,当被预测到时,与惊讶或预测误差相关的反应可能会减少,而当我们知道它们可以预测时,它们可能会增加。这个悖论通过认识到大脑反应反映了精度加权的预测误差而得到解决。这迫使我们在电生理学中区分精度和预测误差的贡献。为了首次应对这一挑战,我们呼吁采用一种将原始实验范式与精细动态建模相结合的方法。我们研究了健康人类参与者(n=20;10 名女性)对意外和预期的令人惊讶的声音的大脑反应,假设后者产生的预测误差较小,但由于精度权重更大而被放大了很多。重要的是,解决这种调制需要对大脑反应的逐次试验变化进行建模,我们通过结合 EEG 和 MEG 在额颞网络中重建了这种变化。我们的结果揭示了对惊讶的适应性学习,即在预期惊讶的情况下,对过去(相关)信息的更大整合。在听觉层次结构中,这种适应与特定的连接有关,特别是通过神经元兴奋性揭示了精度编码。引人注目的是,随着声音序列的不被注意,这些精细过程会自动进行。这些发现直接涉及精神病学中的应用,其中特定的精度加权受损被认为是精神分裂症和自闭症等几种疾病的核心。在作为贝叶斯推理和学习的感知中,上下文敏感性表现为预测误差的精度加权。这是一个微妙的机制,被认为是几种精神疾病的核心所在。因此,确定其神经生理学和计算基础至关重要。我们通过操纵声音的可预测性来重新审视被动听觉异常范式,并使用双重建模方法同时对 EEG-MEG 记录进行分析:(1)对皮质反应的逐次试验建模揭示了一种上下文敏感的感知学习过程;(2)对诱发反应的动态因果建模(DCM)揭示了相关的突触效能变化。可预测性揭示了精度加权与浅层锥体(SP)细胞的自我抑制之间的联系,这一结果为健康和病理感知的精细描述铺平了道路。