Rhythm sensitivity in macaque monkeys

Abstract

This study provides evidence that monkeys are rhythm sensitive. We composed isochronous tone sequences consisting of repeating triplets of two short tones and one long tone which humans perceive as repeating triplets of two weak and one strong beat. This regular sequence was compared to an irregular sequence with the same number of randomly arranged short and long tones with no such beat structure. To search for indication of rhythm sensitivity we employed an oddball paradigm in which occasional duration deviants were introduced in the sequences. In a pilot study on humans we showed that subjects more easily detected these deviants when they occurred in a regular sequence. In the monkeys we searched for spontaneous behaviors the animals executed concomitant with the deviants. We found that monkeys more frequently exhibited changes of gaze and facial expressions to the deviants when they occurred in the regular sequence compared to the irregular sequence. In addition we recorded neuronal firing and local field potentials from 175 sites of the primary auditory cortex during sequence presentation. We found that both types of neuronal signals differentiated regular from irregular sequences. Both signals were stronger in regular sequences and occurred after the onset of the long tones, i.e., at the position of the strong beat. Local field potential responses were also significantly larger for the durational deviants in regular sequences, yet in a later time window. We speculate that these temporal pattern-selective mechanisms with a focus on strong beats and their deviants underlie the perception of rhythm in the chosen sequences.

Hierarchy of prediction errors for auditory events in human temporal and frontal cortex

“…We did not find sensitivity to periodic structure in auditory cortex contacts, such as it was shown for the rat or macaque auditory cortex (37,38). Yaron et al (37) found neurons responding differently to fully predictable and unpredictable standards and deviants.…”

Finding the beat: a neural perspective across humans and non-human primates

“…However, the authors found that the sensitivity for deviant detection is more developed in humans than monkeys. Humans detect deviants with high accuracy not only for the isochronous tone sequences but also in more complex sequences (with an additional sound with a different timbre), whereas monkeys do not show sensitivity to deviants under these conditions [62]. Overall, these findings suggest that monkeys have some capabilities for beat perception, particularly when the stimuli are isochronous, corroborating the hypothesis that the complex entrainment abilities of humans have evolved gradually across primates, and with a primordial beat-based mechanism already present in macaques [7].…”

Predictive cues for auditory stream formation in humans and monkeys

“…It has been hypothesised that an increase in precision is associated with an increase in subthreshold excitability of neural networks encoding the predicted stimulus (Prabhu et al ., ; van Elswijk et al ., ; Aggelopoulos, ), increasing the signal‐to‐noise ratio of neuronal responses to sensory stimuli. This hypothesis is compatible with the principles of active inference by which attention, by increasing the gain of sensory feedback, optimises precision (Brown et al ., ) and is consonant with the recent finding of an increase in the MEG field strength RMS by tone sequences of predictable patterns of tone frequencies (Barascud et al., ) and also agrees with our previous observation (Selezneva et al ., ) that neuronal responses to the long stimuli are enhanced in a temporally predictable sequence of stimuli.…”

“…Previous observations on the effects of repeating patterns of stimuli on auditory stream formation made by us (Selezneva et al ., ) or others (Schroeder & Lakatos, ; Arnal & Giraud, ) have been made for periodic (isochronous) stimulus sequences and were explained by way of an entrainment of brain oscillations with the periodic stimulation. In this view, the oscillatory nature of up‐ and down‐regulation of neuronal activity (Castro‐Alamancos, ) has been considered to provide the prediction, or the internal forward model, about the timing of the upcoming stimuli, relative to which the auditory system computes the relationship with the stimulation at the predicted time.…”

“…Specifically, the monkey experiment tested the null hypothesis that the responses to the long tone under the two factors isochrony and regularity were not different, using a design suited to a repeated measures anova . As we already knew from the previous experiment (Selezneva et al ., ) that the regular sequence caused a response enhancement, the question more specifically, as explained in the Introduction, was whether it was isochrony or regularity (or both) that caused this enhancement. Another aspect of the hypothesis, already established in the previous experiment, was that an increase in the prediction confidence of a stimulus (increase in precision ) caused a facilitation in response to the expected stimulus.…”