FMRI investigation of cross-modal interactions in beat perception: Audition primes vision, but not vice versa

How we measure time and integrate temporal cues from different sensory modalities are fundamental questions in neuroscience. Sensitivity to a “beat” (such as that routinely perceived in music) differs substantially between auditory and visual modalities. Here we examined beat sensitivity in each modality, and examined cross-modal influences, using functional magnetic resonance imaging (fMRI) to characterize brain activity during perception of auditory and visual rhythms. In separate fMRI sessions, participants listened to auditory sequences or watched visual sequences. The order of auditory and visual sequence presentation was counterbalanced so that cross-modal order effects could be investigated. Participants judged whether sequences were speeding up or slowing down, and the pattern of tempo judgments was used to derive a measure of sensitivity to an implied beat. As expected, participants were less sensitive to an implied beat in visual sequences than in auditory sequences. However, visual sequences produced a stronger sense of beat when preceded by auditory sequences with identical temporal structure. Moreover, increases in brain activity were observed in the bilateral putamen for visual sequences preceded by auditory sequences when compared to visual sequences without prior auditory exposure. No such order-dependent differences (behavioral or neural) were found for the auditory sequences. The results provide further evidence for the role of the basal ganglia in internal generation of the beat and suggest that an internal auditory rhythm representation may be activated during visual rhythm perception.

[1]  R. Parncutt A Perceptual Model of Pulse Salience and Metrical Accent in Musical Rhythms , 1994 .

[2]  J. Devin McAuley,et al.  Duration Discrimination in Crossmodal Sequences , 2009, Perception.

[3]  W. Penny,et al.  Random-Effects Analysis , 2002 .

[4]  A. Glenberg,et al.  Modality effects in the coding and reproduction of rhythms. , 1989, Memory & cognition.

[5]  S. Grondin,et al.  Discriminating time intervals presented in sequences marked by visual signals , 2001, Perception & psychophysics.

[6]  Norimichi Kitagawa,et al.  Audio-visual integration in temporal perception. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[7]  F. Vidal,et al.  Activation of the supplementary motor area and of attentional networks during temporal processing , 2002, Experimental Brain Research.

[8]  Giacomo Koch,et al.  Role of the cerebellum in externally paced rhythmic finger movements. , 2007, Journal of neurophysiology.

[9]  Arthur M. Glenberg,et al.  Modality effects in the coding reproduction of rhythms , 1989 .

[10]  Menachem Jona,et al.  Temporal coding in rhythm tasks revealed by modality effects , 1991, Memory & cognition.

[11]  R. Zatorre,et al.  When the brain plays music: auditory–motor interactions in music perception and production , 2007, Nature Reviews Neuroscience.

[12]  J. Devin McAuley,et al.  Neural bases of individual differences in beat perception , 2009, NeuroImage.

[13]  J A Obeso,et al.  Temporal discrimination is abnormal in Parkinson's disease. , 1992, Brain : a journal of neurology.

[14]  R B Ivry,et al.  Dissociable contributions of the prefrontal and neocerebellar cortex to time perception. , 1998, Brain research. Cognitive brain research.

[15]  Randolph Blake,et al.  Hearing What the Eyes See , 2005, Psychological science.

[16]  Karl J. Friston,et al.  A neural substrate for musical hallucinosis , 1997 .

[17]  M. Thaut,et al.  Neural Basis of Rhythmic Timing Networks in the Human Brain , 2003, Annals of the New York Academy of Sciences.

[18]  Peter Ford Dominey,et al.  Motor imagery of a lateralized sequential task is asymmetrically slowed in hemi-Parkinson's patients , 1995, Neuropsychologia.

[19]  André Dufour,et al.  Evidence of beat perception via purely tactile stimulation , 2008, Brain Research.

[20]  S Lehéricy,et al.  Basal ganglia and supplementary motor area subtend duration perception: an fMRI study , 2003, NeuroImage.

[21]  R. Zatorre,et al.  When that tune runs through your head: a PET investigation of auditory imagery for familiar melodies. , 1999, Cerebral cortex.

[22]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[23]  J. Coull fMRI studies of temporal attention: allocating attention within, or towards, time. , 2004, Brain research. Cognitive brain research.

[24]  G. Recanzone Auditory influences on visual temporal rate perception. , 2003, Journal of neurophysiology.

[25]  Caroline Palmer,et al.  Accent structures in music performance. , 1993 .

[26]  Doris-Eva Bamiou,et al.  The insula (Island of Reil) and its role in auditory processing Literature review , 2003, Brain Research Reviews.

[27]  Karl J. Friston,et al.  The Functional Neuroanatomy of Temporal Discrimination , 2004, The Journal of Neuroscience.

[28]  J. Devin McAuley,et al.  Modeling effects of rhythmic context on perceived duration: a comparison of interval and entrainment approaches to short-interval timing. , 2003, Journal of experimental psychology. Human perception and performance.

[29]  J. Gibbon,et al.  Coupled Temporal Memories in Parkinson's Disease: A Dopamine-Related Dysfunction , 1998, Journal of Cognitive Neuroscience.

[30]  J. Devin McAuley,et al.  Modality effects in rhythm processing: Auditory encoding of visual rhythms is neither obligatory nor automatic , 2010, Attention, perception & psychophysics.

[31]  Peter Vuust,et al.  It don't mean a thing… Keeping the rhythm during polyrhythmic tension, activates language areas (BA47) , 2006, NeuroImage.

[32]  W. Meck,et al.  Cortico-striatal circuits and interval timing: coincidence detection of oscillatory processes. , 2004, Brain research. Cognitive brain research.

[33]  D. V. von Cramon,et al.  Interval and ordinal properties of sequences are associated with distinct premotor areas. , 2001, Cerebral cortex.

[34]  J. Devin McAuley,et al.  Effect of deviations from temporal expectations on tempo discrimination of isochronous tone sequences. , 1998, Journal of experimental psychology. Human perception and performance.

[35]  D. Harrington,et al.  Temporal processing in the basal ganglia. , 1998, Neuropsychology.

[36]  Alan C. Evans,et al.  Cerebellar Contributions to Motor Timing: A PET Study of Auditory and Visual Rhythm Reproduction , 1998, Journal of Cognitive Neuroscience.

[37]  H. Zelaznik,et al.  The Cerebellum and Event Timing , 2002, Annals of the New York Academy of Sciences.

[38]  Robert H. Gault,et al.  An Empirical Comparison of Audition, Vision, and Touch in the Discrimination of Temporal Patterns and Ability to Reproduce them , 1938 .

[39]  Richard lvry,et al.  Cerebellar timing systems. , 1997 .

[40]  Fred L. Steinberg,et al.  Functional MRI reveals the existence of modality and coordination-dependent timing networks , 2005, NeuroImage.

[41]  G. Aschersleben,et al.  Temporal ventriloquism: crossmodal interaction on the time dimension. 1. Evidence from auditory-visual temporal order judgment. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[42]  S. Keele,et al.  Timing Functions of The Cerebellum , 1989, Journal of Cognitive Neuroscience.

[43]  Rhythms and responses. , 1985 .

[44]  Hans Forssberg,et al.  Listening to rhythms activates motor and premotor cortices , 2009, Cortex.

[45]  R Fendrich,et al.  The temporal cross-capture of audition and vision , 2001, Perception & psychophysics.

[46]  Catalin V. Buhusi,et al.  What makes us tick? Functional and neural mechanisms of interval timing , 2005, Nature Reviews Neuroscience.

[47]  R. Zatorre,et al.  Listening to musical rhythms recruits motor regions of the brain. , 2008, Cerebral cortex.

[48]  Jen-Chuen Hsieh,et al.  Common neural mechanisms for explicit timing in the sub-second range , 2009, Neuroreport.

[49]  Richard S. J. Frackowiak,et al.  The structural components of music perception. A functional anatomical study. , 1997, Brain : a journal of neurology.

[50]  A. Friederici,et al.  Time Perception and Motor Timing: A Common Cortical and Subcortical Basis Revealed by fMRI , 2000, NeuroImage.

[51]  C. Drake,et al.  The development of rhythmic attending in auditory sequences: attunement, referent period, focal attending , 2000, Cognition.

[52]  R. Ivry Cerebellar timing systems. , 1997, International review of neurobiology.

[53]  Roland R. Lee,et al.  Does the representation of time depend on the cerebellum? Effect of cerebellar stroke. , 2003, Brain : a journal of neurology.

[54]  Rodrigo Quian Quiroga,et al.  Rhythmic training decreases latency-jitter of omission evoked potentials (OEPs) in humans , 2004, Neuroscience Letters.

[55]  Aniruddh D. Patel,et al.  The influence of metricality and modality on synchronization with a beat , 2005, Experimental Brain Research.

[56]  Örjan Blom,et al.  The dorsal auditory pathway is involved in performance of both visual and auditory rhythms , 2009, NeuroImage.

[57]  T SHIPLEY,et al.  Auditory Flutter-Driving of Visual Flicker , 1964, Science.

[58]  S. Grondin,et al.  Judging the relative duration of multimodal short empty time intervals , 1991, Perception & psychophysics.

[59]  Norimichi Kitagawa,et al.  Hearing visual motion in depth , 2002, Nature.

[60]  Stephen M. Rao,et al.  The evolution of brain activation during temporal processing , 2001, Nature Neuroscience.

[61]  E. Large On synchronizing movements to music , 2000 .

[62]  G Hickok,et al.  Functional Anatomy of Speech Perception and Speech Production: Psycholinguistic Implications , 2001, Journal of psycholinguistic research.

[63]  D. Burr,et al.  Auditory dominance over vision in the perception of interval duration , 2009, Experimental Brain Research.

[64]  Nathaniel S. Miller,et al.  The time of our lives: life span development of timing and event tracking. , 2006, Journal of experimental psychology. General.

[65]  Bruno H. Repp,et al.  Auditory dominance in temporal processing: new evidence from synchronization with simultaneous visual and auditory sequences. , 2002, Journal of experimental psychology. Human perception and performance.

[66]  S. Goldstone,et al.  Studies of Auditory-Visual Differences in Human Time Judgment: 2. More Transmitted Information with Sounds than Lights , 1974, Perceptual and motor skills.

[67]  Christian Gaser,et al.  Processing of temporal information and the basal ganglia: new evidence from fMRI , 2003, Experimental Brain Research.

[68]  John Gibbon,et al.  Separating Storage from Retrieval Dysfunction of Temporal Memory in Parkinson's Disease , 2002, Journal of Cognitive Neuroscience.

[69]  R. Miall,et al.  Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging , 2003, Current Opinion in Neurobiology.

[70]  M. Grube,et al.  Dissociation of duration-based and beat-based auditory timing in cerebellar degeneration , 2010, Proceedings of the National Academy of Sciences.

[71]  Matthew Brett,et al.  Rhythm and Beat Perception in Motor Areas of the Brain , 2007, Journal of Cognitive Neuroscience.

[72]  J. Devin McAuley,et al.  Listening strategy for auditory rhythms modulates neural correlates of expectancy and cognitive processing. , 2011, Psychophysiology.

[73]  W. D. Penny,et al.  Random-Effects Analysis , 2002 .

[74]  M. Brett,et al.  Impairment of beat-based rhythm discrimination in Parkinson's disease , 2009, Cortex.

[75]  Peter Essens,et al.  Perception of Temporal Patterns , 1985 .

[76]  G. Logan,et al.  Modality differences in short-term memory for rhythms , 2000, Memory & cognition.

[77]  John F. Kolen,et al.  Resonance and the Perception of Musical Meter , 1994, Connect. Sci..

[78]  D. Harrington,et al.  Neural Underpinnings of Temporal Processing: Α Review of Focal Lesion, Pharmacological, and Functional Imaging Research , 1999, Reviews in the neurosciences.

[79]  G. E. Alexander,et al.  Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. , 1990, Progress in brain research.

[80]  Nathaniel S. Miller,et al.  Detecting changes in timing: Evidence for two modes of listening , 2006 .

[81]  M. Nicolelis,et al.  Interval timing and the encoding of signal duration by ensembles of cortical and striatal neurons. , 2003, Behavioral neuroscience.

[82]  P A Kolers,et al.  Rhythms and responses. , 1985, Journal of experimental psychology. Human perception and performance.

[83]  L. D. Goodfellow,et al.  An Empirical Comparison of Audition, Vision, and Touch in the Discrimination of Short Intervals of Time , 1934 .

[84]  Jessica A. Grahn,et al.  Feeling the Beat: Premotor and Striatal Interactions in Musicians and Nonmusicians during Beat Perception , 2009, The Journal of Neuroscience.

[85]  Jane S. Paulsen,et al.  fMRI biomarker of early neuronal dysfunction in presymptomatic Huntington's Disease. , 2004, AJNR. American journal of neuroradiology.