Sequence learning modulates neural responses and oscillatory coupling in human and monkey auditory cortex.
Sequence learning modulates neural responses and oscillatory coupling in human and monkey auditory cortex.
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DOI：
10.1371/journal.pbio.2000219
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发表时间：
2017-04
期刊：
影响因子：
9.8
通讯作者：
Petkov CI
中科院分区：
文献类型：
--
作者：
Kikuchi Y;Attaheri A;Wilson B;Rhone AE;Nourski KV;Gander PE;Kovach CK;Kawasaki H;Griffiths TD;Howard MA 3rd;Petkov CI
学习序列中感觉事件之间的复杂排序关系是动物感知和人类交流的基础。虽然已知有节奏的感觉事件可以以不同的频率引起脑振荡，但对学习和先前的序列关系经验如何影响新皮层振荡和神经元反应的了解甚少。我们使用了一种内隐序列学习范式（一种“人工语法”），在这种范式中，人类和猴子被暴露在一系列无意义的单词中，这些单词之间的顺序关系是不确定的。然后，我们直接记录了这两个物种的听觉皮层对新的法律的序列或违反特定顺序关系的序列的神经反应。猴子和人类对无意义单词序列的神经振荡显示出惊人的相似的层次嵌套低频相位和高伽马振幅耦合，建立了这种形式的振荡耦合-以前与人类听觉皮层的语音处理相关-作为进化保守的生物过程。此外，学习的排序关系调节观察到的形式的神经振荡耦合在这两个物种，时间上不同的神经振荡效应，似乎协调神经元的反应在猴子。这项研究确定了保守的听觉皮层神经签名参与监测学习排序操作，明显的瞬态耦合和神经元响应的调制时间结构的感觉输入。虽然自然环境不断变化，但某些事件可以预测其他事件的未来发生。学习排序关系对于动物感知和人类交流至关重要，但这种学习和先前的经验如何影响大脑仍然知之甚少。我们开始了解单词之间的学习关系如何改变人类和猴子的神经元反应。使用内隐学习范式，我们将人类受试者和猴子暴露于遵循某些基于规则的排序关系（“人工语法”）的无意义语音序列。然后，我们直接记录了这两个物种的听觉皮层对序列的神经反应，这些序列要么与人工语法一致，要么在序列中的元素之间创建了非法的顺序转换。我们发现，学习排序关系调节神经反应的多样性（其中一些以类似的方式协调）在两个物种的神经元群体的规模。我们在猴子身上的实验也揭示了这种神经处理的规模与单个神经元有关，单个神经元是大脑中的基本处理单元。这项研究揭示了听觉皮层的保守神经元特征，这些特征参与监测学习的排序操作，这些操作机械地告知并扩展了大脑如何预测感官世界的想法。
Learning complex ordering relationships between sensory events in a sequence is fundamental for animal perception and human communication. While it is known that rhythmic sensory events can entrain brain oscillations at different frequencies, how learning and prior experience with sequencing relationships affect neocortical oscillations and neuronal responses is poorly understood. We used an implicit sequence learning paradigm (an “artificial grammar”) in which humans and monkeys were exposed to sequences of nonsense words with regularities in the ordering relationships between the words. We then recorded neural responses directly from the auditory cortex in both species in response to novel legal sequences or ones violating specific ordering relationships. Neural oscillations in both monkeys and humans in response to the nonsense word sequences show strikingly similar hierarchically nested low-frequency phase and high-gamma amplitude coupling, establishing this form of oscillatory coupling—previously associated with speech processing in the human auditory cortex—as an evolutionarily conserved biological process. Moreover, learned ordering relationships modulate the observed form of neural oscillatory coupling in both species, with temporally distinct neural oscillatory effects that appear to coordinate neuronal responses in the monkeys. This study identifies the conserved auditory cortical neural signatures involved in monitoring learned sequencing operations, evident as modulations of transient coupling and neuronal responses to temporally structured sensory input. While natural environments constantly change, certain events can predict the future occurrence of others. Learning ordering relationships is vital for animal perception and human communication, yet how such learning and prior experience affect the brain remains poorly understood. We set out to understand how learning relationships between words modifies neuronal responses in both humans and monkeys. Using an implicit learning paradigm, we exposed human subjects and monkeys to sequences of nonsense speech sounds that followed certain rule-based ordering relationships (an “artificial grammar”). We then recorded neural responses directly from the auditory cortex in both species in response to sequences that were either consistent with the artificial grammar or created illegal ordering transitions between elements in a sequence. We found that learned ordering relationships modulate a diversity of neural responses (some of which coordinate in similar ways) at the scale of populations of neurons in both species. Our experiments in monkeys also revealed that this scale of neural processing is related to single neurons, the fundamental processing unit in the brain. This study reveals the conserved neuronal signatures of the auditory cortex involved in monitoring learned sequencing operations, which mechanistically inform and extend ideas on how the brain predicts the sensory world.