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Two Prediction Error Systems in the Nonlemniscal Inferior Colliculus: "Spectral" and "Nonspectral"
Journal of Neuroscience ( IF 4.4 ) Pub Date : 2024-06-05 , DOI: 10.1523/jneurosci.1420-23.2024
Guillermo V. Carbajal , Lorena Casado-Román , Manuel S. Malmierca

According to the predictive processing framework, perception emerges from the reciprocal exchange of predictions and prediction errors (PEs) between hierarchically organized neural circuits. The nonlemniscal division of the inferior colliculus (IC) is the earliest source of auditory PE signals, but their neuronal generators, properties, and functional relevance have remained mostly undefined. We recorded single-unit mismatch responses to auditory oddball stimulation at different intensities, together with activity evoked by two sequences of alternating tones to control frequency-specific effects. Our results reveal a differential treatment of the unpredictable "many-standards" control and the predictable "cascade" control by lemniscal and nonlemniscal IC neurons that is not present in the auditory thalamus or cortex. Furthermore, we found that frequency response areas of nonlemniscal IC neurons reflect their role in subcortical predictive processing, distinguishing three hierarchical levels: (1) nonlemniscal neurons with sharply tuned receptive fields exhibit mild repetition suppression without signaling PEs, thereby constituting the input level of the local predictive processing circuitry. (2) Neurons with broadly tuned receptive fields form the main, "spectral" PE signaling system, which provides dynamic gain compensation to near-threshold unexpected sounds. This early enhancement of saliency reliant on spectral features was not observed in the auditory thalamus or cortex. (3) Untuned neurons form an accessory, "nonspectral" PE signaling system, which reports all surprising auditory deviances in a robust and consistent manner, resembling nonlemniscal neurons in the auditory cortex. These nonlemniscal IC neurons show unstructured and unstable receptive fields that could result from inhibitory input controlled by corticofugal projections conveying top-down predictions.



中文翻译:


非脑膜下丘的两个预测误差系统:“光谱”和“非光谱”



根据预测处理框架,感知产生于分层组织的神经回路之间的预测和预测误差(PE)的相互交换。下丘 (IC) 的非丘系区是听觉 PE 信号的最早来源,但它们的神经元发生器、特性和功能相关性大多仍未定义。我们记录了对不同强度的听觉奇怪刺激的单单元失配反应,以及由两个交替音调序列引起的活动,以控制特定频率的效果。我们的结果揭示了对不可预测的“多标准”控制和可预测的“级联”控制的区别对待,这些控制是由丘系和非丘系 IC 神经元进行的,而这些神经元不存在于听觉丘脑或皮层中。此外,我们发现非丘系 IC 神经元的频率响应区域反映了它们在皮层下预测处理中的作用,区分了三个层次级别:(1)具有急剧调整的感受野的非丘系神经元在没有信号 PE 的情况下表现出轻微的重复抑制,从而构成了本地预测处理电路。 (2) 具有广泛调谐感受野的神经元形成主要的“频谱”PE 信号系统,该系统为接近阈值的意外声音提供动态增益补偿。在听觉丘脑或皮层中没有观察到这种依赖于频谱特征的早期显着性增强。 (3) 未调谐的神经元形成一个辅助的“非频谱”PE 信号系统,该系统以稳健且一致的方式报告所有令人惊讶的听觉异常,类似于听觉皮层中的非丘系神经元。 这些非丘系 IC 神经元表现出非结构化且不稳定的感受野,这可能是由传达自上而下预测的皮质投射控制的抑制输入引起的。

更新日期:2024-06-06
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