Biology subjects

Grahn, J. A.

Publications and source records attributed to Grahn, J. A..

7 recordsLinked to original sources

bioRxiv2026

Reward-driven emergence of auditory pattern encoding in the primate motor system

The ability to anticipate rhythmic patterns is fundamental to human experience, enabling music appreciation, speech comprehension, and dancing in sync to music. How the brain learns to use acoustic information to guide motor behavior remains a key question, with its neural underpinnings and evolutionary origins debated, especially in non-human primates. Reward contingencies improve monkeys ability to synchronize with musical beats with near-human accuracy. However, humans and certain birds spontaneously synchronize with musical beats. Behavioural work in monkeys suggests that the brains reward system can encode rhythmic patterns if sufficiently reinforced, known as the intrinsic reward hypothesis. To investigate the neural mechanism of how the reward gates rhythmic pattern learning, we recorded neural activity from the globus pallidus interna (GPi) of a rhesus macaque during passive listening to auditory patterns. We found that GPis ability to encode auditory patterns in a monkey is shaped by reward association. Specifically, during passive listening (Experiment 1), with reward only at the end of each trial, GPi showed at most a weak response to the auditory tone patterns that was not evident in single neurons or population responses, ruling out spontaneous entrainment of motor activity to auditory patterns. When each tone was simultaneously accompanied by a liquid reward (Experiment 2), GPi showed clear responses to the tone patterns. To test if the tone responses persisted, the reward contingency was subsequently removed (Experiment 3). Strikingly, although the reward was delivered only at the trials end as in Experiment 1, GPi neurons continued to track the occurrence of the tones. Besides GPi, we also recorded single-neuron activity across the primary somatosensory (S1), primary motor (M1), dorsal premotor (PMd), supplementary motor (SMA), pre-supplementary motor (preSMA) cortices, and the medial geniculate body (MGB) of the same animal in experiments 1 and 2. We found that during passive listening (Experiment 1) with a reward only at the end of each trial, primarily the MGB, not motor areas, responded to the auditory tone patterns, ruling out spontaneous entrainment of motor activity to auditory patterns across the primate motor system. When each tone was simultaneously accompanied by a liquid reward (Experiment 2), all areas except S1 showed clear responses to the tone patterns. These findings suggest that while basic sensory processing of tone patterns occurs in the MGB, the GPi exhibits reward-driven encoding of auditory patterns that persists after reward withdrawal. This reorganization of neural responsiveness shows that the capacity for auditory association can be elicited in the motor system through appropriate motivational contexts.

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bioRxiv2024

Isolating the effect of beat salience on rhythmic auditory stimulation outcomes

Rhythmic auditory stimulation (RAS) is an intervention for gait-disordered populations that involves synchronizing footsteps to regular auditory cues. Previous research has shown that high-groove music (music that induces the desire to move or dance to it) improves gait relative to low-groove music, but how this effect occurs is unclear. Greater beat salience in high-groove music may improve gait because salient beats are easier to synchronize with. Here, we manipulated beat salience by embedding metronome tones to emphasize beat onsets in both high- and low-groove music. We expected that, if beat salience drives gait improvements to high-groove music, then embedding metronome in low-groove music would elicit similar gait improvements (e.g. increased stride velocity). Here, we quantified gait synchronization in terms of period-matching (overall step rate to the cue pace) and phase-matching (individual step onsets to beat onsets). We tested a sample of healthy younger and older adults, with auditory cues matched to 10% faster than baseline. Low-groove music with embedded metronome, compared to without, elicited better period-matching; there were no differences between metronome conditions in high-groove music. These findings suggest gait improvements to high-groove music could be due to its high beat salience. On the other hand, embedded metronome did not improve phase-matching accuracy, but high-groove music did. This suggests that beat salience may not improve gait via easing step-to-beat synchronization, but rather through an overall increase in movement vigor.

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bioRxiv2023

Investigating the Causal Role of Motor Brain Areas in Rhythm Reproduction: A Transcranial Direct Current Stimulation Study

Humans have an intrinsic tendency to move to music. However, our understanding of the neural mechanisms underlying the music-movement connection remains limited, and most studies have used correlational methods. Here, we used transcranial direct current stimulation (tDCS) to investigate the causal role of four brain regions commonly involved in movement timing and beat perception: the supplementary motor area (SMA), left and right premotor cortices (PMC), and the right cerebellum. On three different days, subjects received anodal, cathodal, or sham stimulation while reproducing strong-beat, weak-beat, and non-beat rhythms via finger tapping. Each subject only received stimulation in one of the four brain regions. As the SMA appears to play a primary role in beat perception, while the premotor cortex and cerebellum appear to have a more general role in timing, we predicted that the SMA stimulation would affect reproduction of rhythms with a beat, whereas premotor and cerebellar stimulation would affect reproduction of sequences with no beat. As expected, reproduction accuracy depended on beat strength; strong-beat rhythms were more accurately reproduced than weak and non-beat rhythms. Unexpectedly, tDCS had no effect on reproduction accuracy in any brain region. Thus, we found no evidence that modulating brain excitability in SMA, PMC, or cerebellum altered accuracy of rhythm reproduction. We discuss the implications of these results and future perspectives for this research.

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bioRxiv2023

Neural Representations of Beat and Rhythm in Motor and Association Regions

Humans perceive a pulse, or beat, underlying musical rhythm. Beat strength correlates with activity in the basal ganglia and SMA, suggesting these regions support beat perception. However, the basal ganglia and SMA make up a general timing network active during rhythm and timing perception, regardless of beat. Therefore, activity in these regions may represent basic rhythmic features, in addition to beat. Using RSA, we characterized the neural representation of rhythm in the basal ganglia, SMA, and across the whole brain. During fMRI, participants heard 12 rhythms - 4 strong-beat, 4 weak-beat, and 4 non-beat. Multi-voxel activity patterns for each rhythm, and for the mean of each condition, were tested for uniqueness. Activity patterns in beat-sensitive regions should alter as a function of beat strength, eliciting greater dissimilarities between rhythms with different beat strength than between rhythms with similar beat strength. Indeed, mean activity patterns in the putamen and SMA were significantly dissimilar for strong-beat and non-beat conditions, and dissimilarity between activity patterns across all 12 rhythms correlated with beat strength models, not basic rhythmic features. Whole-brain analyses also identified beat-sensitivity in the IFG, and inferior parietal cortex. These findings build upon univariate work suggesting that motor and association regions are beat-sensitive.

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bioRxiv2021

Finding and Keeping the Beat: Neural Mechanisms Differ as Beat Perception Unfolds

Perception of a regular beat is essential to our ability to synchronize movements to music in an anticipatory fashion. Beat perception requires multiple, distinct neural functions, corresponding to the perceptual stages that occur over time, including 1) detection that regularity is present (beat finding), 2) prediction of future regular events to enable anticipation (beat continuation), and 3) dynamic adjustment of predictions as the rhythmic stimulus changes (beat adjustment). The striatum has been shown to be crucial for beat perception generally, although it is unclear how, or whether, distinct regions of the striatum contribute to these different stages of beat perception. Here, we used fMRI to investigate the activity of striatal subregions during the different stages of beat perception. Participants listened to pairs of rhythms (polyrhythms) whose temporal structure induced distinct perceptual stages--finding, continuation, and adjustment of the beat. Dorsal putamen was preferentially active during beat finding, whereas the ventral putamen was preferentially active during beat adjustment. We also observed that anterior insula activity was sensitive to metrical structure (greater when polyrhythms were metrically incongruent than when they were congruent). These data implicate the dorsal putamen in the detection of regularity, possibly by detection of coincidences between cortical oscillations, and the ventral putamen in the adjustment of regularity perception, possibly by integration of prediction errors in ongoing beat predictions. Additionally, activity in the supramarginal and superior temporal gyri correlated with beat tapping performance, and activity in the superior temporal gyrus correlated with beat perception (performance on the Beat Alignment Test).

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bioRxiv2019

Investigation of working memory networks for verbal and rhythmic stimuli

Auditory working memory is often conceived of as a unitary capacity, with memory for different auditory materials (syllables, pitches, rhythms) thought to rely on similar neural mechanisms. One spontaneous behavior observed in working memory studies is chunking. For example, individuals often recount digit sequences in groups, or chunks, of 3 to 4 digits, and this chunking improves performance. Chunking may also operate in musical rhythm, with beats acting as chunk boundaries for tones in rhythmic sequences. Similar to chunking, beat-based structure in rhythms also improves performance. Thus, beat processing may rely on the same mechanisms that underlie chunking of verbal material. The current fMRI study examined whether beat perception is a type of chunking, measuring brain responses to chunked and unchunked letter sequences relative to beat-based and nonbeat-based rhythmic sequences. Participants completed a sequence discrimination task, and comparisons between stimulus encoding, maintenance, and discrimination were made for both rhythmic and verbal sequences. Overall, rhythm and verbal working memory networks overlapped substantially. When comparing rhythmic and verbal conditions, rhythms activated basal ganglia, supplementary motor area, and anterior insula, compared to letter strings, during encoding and discrimination. Letter strings compared to rhythms activated bilateral auditory cortex during encoding, and parietal cortex, precuneus, and middle frontal gyri during discrimination. Importantly, there was a significant interaction in the basal ganglia during encoding: activation for beat-based rhythms was greater than for nonbeat-based rhythms, but verbal chunked and unchunked conditions did not differ. The significant interaction indicates that beat perception is not simply a case of chunking, suggesting a dissociation between beat processing and grouping mechanisms that warrants further exploration.

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bioRxiv2019

The Effect of Aging, Parkinson’s Disease, and Exogenous Dopamine on the Neural Response Associated with Auditory Regularity Processing

Processing regular patterns in auditory scenes is important for navigating complex environments. Electroencephalography (EEG) studies find enhancement of sustained brain activity, correlating with the emergence of a regular pattern in sounds. How aging, aging-related diseases such as Parkinsons disease (PD), and treatment of PD affect this fundamental function remain unknown. We addressed this knowledge gap. Healthy younger and older adults, and PD patients listened to sounds that contained or were devoid of regular patterns. Healthy older adults and PD patients were tested twice--on and off dopaminergic medication in counterbalanced order. Regularity-evoked, sustained EEG activity was reduced in older, compared to younger adults. PD patients and older controls had comparable attenuation of the sustained response. Dopaminergic therapy further weakened the sustained response in both groups. These findings suggest that fundamental regularity processing is impacted by aging-related neural changes but not those underlying PD. The finding that dopaminergic therapy attenuates rather than improves the sustained response coheres with the dopamine overdose response and implicates brain regions receiving dopamine from the ventral tegmental area in regularity processing.

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