No 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.

There is considerable interest in understanding the ontogeny and phylogeny of the human language system, yet, neurobiological work at the interface of both fields is absent. Syntactic processes in language build on sensory processing and sequencing capabilities on the side of the receiver. While we better understand language-related ontogenetic changes in the human brain, it remains a mystery how neurobiological processes at specific human development stages compare with those in phylogenetically closely related species. To address this knowledge gap, we measured EEG event-related potentials (ERPs) in two macaque monkeys using a paradigm developed to evaluate human infant and adult brain potentials associated with the processing of non-adjacent ordering relationships in sequences of syllable triplets. Frequent standard triplet sequences were interspersed with infrequent voice pitch or non-adjacent rule deviants. Monkey ERPs show early pitch and rule deviant mismatch responses that are strikingly similar to those previously reported in human infants. This stands in contrast to adults’ later ERP responses for rule deviants. The results reveal how non-adjacent sequence ordering relationships are processed in the primate brain and provide evidence for evolutionarily conserved neurophysiological effects, some of which are remarkably like those seen at an early human developmental stage.

HighlightsFirst combined EEG and Artificial Grammar (AG) learning study in nonhuman animals.Early and late frontal potentials modulated in response to violations of the AG sequencing relationships in the primate brain.Informative similarities and differences are noted in relation to reported human EEG potentials associated with AG learning.