Sequence learning modulates neural responses and oscillatory coupling in human and monkey auditory cortex

Abstract

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.

Neuronal Encoding in a High-Level Auditory Area: From Sequential Order of Elements to Grammatical Structure

“…Sensitivity to the sequential order in which sounds occur could be a functional property that characterizes high-level auditory regions. However, very few studies have examined neuronal responses to changes in the ordering relationships of elements within sequences by recording single-unit activity in the auditory cortex of mammalian species (Weinberger and McKenna, 1988;McKenna et al, 1989;Kikuchi et al, 2017).…”

Non-linear Auto-Regressive Models for Cross-Frequency Coupling in Neural Time Series

“…In humans, theta (4−8 Hz)/gamma (80−150 Hz) PAC was described in human auditory cortex during speech perception [Canolty et al, 2006]. In more recent work, theta/gamma PAC was reported during the processing of auditory sequences in both humans and monkeys [Kikuchi et al, 2017], during working memory maintenance in human hippocampus [Axmacher et al, 2010], and during serial memory recall using non-invasive human magnetoencephalography (MEG) [Heusser et al, 2016]. PAC has been proposed to support the maintenance of information and to play an important role in long distance communication between different neural populations, considering that slow oscillations can propagate at larger scales than fast ones [Jensen and Colgin, 2007, Khan et al, 2013, Lisman and Jensen, 2013, Bonnefond et al, 2017.…”

Interaction of music and emotional stimuli in modulating working memory in macaque monkeys

“…Our study aims at examining the effects of music in macaque monkeys because of the great similarity in brain architecture between humans and monkeys (Mansouri, Koechlin, Rosa, & Buckley, ; Petrides, Tomaiuolo, Yeterian, & Pandya, ), the ability of monkeys in processing abstract rules and concepts and their enriched social behavior (Kikuchi et al, ; Mansouri, Buckley, Fehring, & Tanaka, ; Mansouri, Egner, & Buckley, ; Mansouri, Tanaka, & Buckley, ; Miller, Nieder, Freedman, & Wallis, ).…”