The stimulus manipulations were successful in modulating the participants' perception of the beat (). High ratings of beat perception occurred even in the absence of external accents (Unaccented Beat condition), corroborating other work showing that internal subjective accents are generated when listening to unaccented isochronous rhythms (Temperley, 1963
; Brochard et al., 2003
). Moreover, the ratings indicate that these internal accents were as effective as external duration accents at inducing beat perception.
The putamen, pallidum, and caudate responded more to beat rhythms than nonbeat rhythms (). Only the basal ganglia (the putamen most robustly) responded to beat presence per se
, showing activity increases for all beat conditions compared to nonbeat conditions. Interestingly, putamen activation did not parallel the behavioral beat ratings. Participants rated beat presence as Volume Beat > Unaccented Beat > Duration Beat, whereas putamen activity was Unaccented Beat > Duration Beat > Volume Beat. Why might this be the case? A critical difference between conditions is the requirement for internal beat generation - this is unnecessary in the Volume Beat condition, and essential in Unaccented Beat condition. Internal generation may modulate the basal ganglia response, with beat perception driving activity to a certain degree, but internal generation driving it as well. Importantly, the putamen response was not merely due to temporal complexity, as complexity was matched in the Unaccented and Volume Beat conditions. Also, it is unlikely that the response was influenced by potential differences in the perceived beat rate between conditions. Other studies have searched for correlations between basal ganglia activity and tapping or vocalization rates and found none (Jenkins et al., 1997
; Riecker et al., 2003
; Lutz et al., 2005
; Riecker et al., 2006
). Here also, basal ganglia activity did not significantly correlate with stimulus rate. However, as we did not specifically manipulate beat rate independently of stimulus rate, this remains to be fully tested.
Turning to other rhythm-responsive areas, greater activity was generally shown for the most unpredictable, temporally complex condition, the Volume Nonbeat condition, in which all tone onsets and accents are unpredictable (). In these regions, including dorsal premotor cortex, prefrontal cortex, inferior parietal lobule, and cerebellum, activity is associated with temporal complexity in motor tasks (Catalan et al., 1998
; Lewis et al., 2004
; Chen et al., 2008a
). Their activation in a purely perceptual task suggests functional overlap between neural networks involved in the perception of temporal complexity and the organization and sequencing of temporally complex movements (Penhune et al., 1998
Perhaps more surprisingly, several areas (right supramarginal and middle frontal gyri, bilateral insula) responded strongly to the ‘simplest’ condition—the Unaccented Beat condition. For this condition, some participants reported that, in addition to a regular beat, they perceived more complex patterns of accents, giving rise to a rhythmic pattern similar to the duration condition. Thus, even though the stimuli are quite simple, what subjects ‘do’ with their perception may not be so simple. The Volume Beat condition is also simple, but external accents force a particular interpretation of the sequence.
The consequences of the putamen's role in beat perception are suggested by the analyses of connectivity. Beat perception led to increased cortico-subcortical coupling of the putamen with bilateral SMA and PMC regardless of how the beat was determined (). One interpretation of this increased coupling is that the putamen encodes information about beat timing that facilitates cortical motor areas in precise control of movement timing, required, for example, when movements are made in time with beats.
In contrast to cortico-subcortical coupling, the cortico-cortical coupling amongst the SMA, PMC and auditory cortex did
depend on accent type: greater coupling was observed for the Duration Beat than the Volume Beat condition. Moreover, the increase in coupling depended on musical training. Only for musicians was coupling between bilateral SMA and STG significant (). These differences in coupling between musicians and non-musicians are seen despite the lack of significant differences using traditional analyses of regional activation. This is consistent with other work showing that connectivity measures may be more sensitive than regional analyses (Rowe et al., 2007
; Sonty et al., 2007
). Recent work has investigated auditory-motor connectivity during tapping tasks in which participants to synchronize to rhythms (Chen et al., 2006
). During tapping, auditory-motor connectivity was increased as volume accents were increased, likely due to the greater influence of the auditory accent structure on participants' motor response (Chen et al., 2006
). In a subsequent study, auditory-motor connectivity increased with musical training (Chen et al., 2008a
), although tapping accuracy and regional activation levels also differed. Here we show that during a purely perceptual task, and without differences in regional activity, auditory-motor connectivity can be altered by musical training.
The difference in coupling between musicians and non-musicians was paralleled by the difference in behavioral ratings: musicians rated the Duration Beat condition as having more of a beat than non-musicians did, whereas the two groups rated the Volume Beat condition similarly. Arguably, the Duration Beat condition is most similar to the type of rhythms musicians spend extensive time learning and performing, thus musicians' ability to organize (‘chunk’) and anticipate onsets may be superior to that of non-musicians (Smith, 1983
). This ability may influence expectations about what will be heard later in the sequence (e.g., expecting onsets to coincide with predicted beats in the Duration Beat condition). In the brain, this could be mediated by top-down influence from motor areas to auditory cortex. In contrast, anticipation of future onsets in the Volume Beat condition is trivial for both musicians and non-musicians, thus no connectivity differences between the groups occur.
Whether musically trained or not, beat perception occurs spontaneously in most people without great effort. Cognitive theories of beat perception propose that the beat in music is indicated by several accent types: volume, duration, melodic, harmonic, timbral, etc. When attempting to find a beat in a sequence, people generate hypotheses about the beat location based on the perceived accents (Drake and Botte, 1993
; Toivanen and Snyder, 2003
; Hannon et al., 2004
), and predict that future accented events will occur ‘on the beat’. Successful prediction leads to enhanced processing of stimulus features (Jones et al., 2002
). The basal ganglia have been implicated in prediction of events (Doya, 2000
; Tanji, 2001
; Schultz, 2006
). When accents occur in unpredicted locations (not on the beat), then the listener's current predictions will be incorrect, causing a prediction error that leads to adjusted future hypotheses (Dickinson and Schultz, 2000
; Davidson and Wolpert, 2003
). This prediction error and continual updating of an internal model of events may explain the large degree of activation seen for the Volume Nonbeat conditions in both experiments: strongly accented events, which are normally indicative of a beat, were occurring at unpredictable times. The salient but unpredictable volume accents could cue participants to search for a beat to a greater degree than less salient duration accents.
We propose that the role of the basal ganglia in rhythm perception, as in other domains, is prediction: when a detectable structure is present in the rhythm, predictions can be made about the timing of future onsets. Successful predictions can enhance the speed of perceptual organization of the sequence, reducing working memory load. With EEG, increases in induced gamma-band activity are observed in anticipation of expected beat locations (Snyder and Large, 2005
; Zanto et al., 2006
). Taken together, these results suggest a strong relationship between anticipation or prediction and beat perception. These results also link to models of musical expectancy (for example, Large and Jones, 1999
), suggesting that prediction may a key process in the perception of musical rhythm.
The results are also of clinical significance, as the basal ganglia are compromised in Parkinson's disease. Parkinson's disease patients have decreased striatal dopamine release, affecting excitatory input to the putamen (Lewis et al. 2003). Studies in patients with Parkinson's disease have shown deficits in timing tasks (Artieda et al., 1992
; O'Boyle et al., 1996
; Harrington et al., 1998
). In addition, Parkinson's disease patients have selective deficits in discriminating rhythms that have a weakly-indicated beat structure (Grahn and Brett, 2009
), such as Duration Beat rhythms, but they are unimpaired in discriminating control nonbeat rhythms. Rhythmic signals with a strong external beat ameliorate gait problems in Parkinson's disease and Huntington's disease (McIntosh et al., 1997
; Thaut et al., 2001a
; Thaut et al., 2001b
). Thus, rhythmic cueing therapy may depend on common neural systems underlying rhythm perception and movement, including the putamen.
In conclusion, the basal ganglia show a specific response to the beat during rhythm perception, regardless of musical training or how the beat is indicated. We suggest that a cortico-subcortical network including the putamen, SMA, and PMC is engaged for the analysis of temporal sequences and prediction or generation of putative beats, especially under conditions that require internal generation of the beat. In these conditions, the coupling among cortical motor and auditory areas is facilitated for musically trained individuals.