Neural Correlates of Temporal Complexity and Synchrony during Audiovisual Correspondence Detection

Visual Abstract Abstract We often perceive real-life objects as multisensory cues through space and time. A key challenge for audiovisual integration is to match neural signals that not only originate from different sensory modalities but also that typically reach the observer at slightly different times. In humans, complex, unpredictable audiovisual streams lead to higher levels of perceptual coherence than predictable, rhythmic streams. In addition, perceptual coherence for complex signals seems less affected by increased asynchrony between visual and auditory modalities than for simple signals. Here, we used functional magnetic resonance imaging to determine the human neural correlates of audiovisual signals with different levels of temporal complexity and synchrony. Our study demonstrated that greater perceptual asynchrony and lower signal complexity impaired performance in an audiovisual coherence-matching task. Differences in asynchrony and complexity were also underpinned by a partially different set of brain regions. In particular, our results suggest that, while regions in the dorsolateral prefrontal cortex (DLPFC) were modulated by differences in memory load due to stimulus asynchrony, areas traditionally thought to be involved in speech production and recognition, such as the inferior frontal and superior temporal cortex, were modulated by the temporal complexity of the audiovisual signals. Our results, therefore, indicate specific processing roles for different subregions of the fronto-temporal cortex during audiovisual coherence detection.

[1]  T. Goldberg,et al.  Dissociating the effects of Sternberg working memory demands in prefrontal cortex , 2007, Psychiatry Research: Neuroimaging.

[2]  Rachel N. Denison,et al.  Temporal Structure and Complexity Affect Audio-Visual Correspondence Detection , 2013, Front. Psychology.

[3]  J. Bower,et al.  Consensus Paper: The Role of the Cerebellum in Perceptual Processes , 2014, The Cerebellum.

[4]  L. Kempe Handbook of Physiology. Section I. The Nervous System , 1982 .

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

[6]  Walter Schneider,et al.  The cognitive control network: Integrated cortical regions with dissociable functions , 2007, NeuroImage.

[7]  Joel R. Meyer,et al.  Modality independence of word comprehension , 2002, Human brain mapping.

[8]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[9]  Mark W Greenlee,et al.  Neural correlates of coherent audiovisual motion perception. , 2007, Cerebral cortex.

[10]  R Todd Constable,et al.  Image distortion correction in EPI: Comparison of field mapping with point spread function mapping , 2002, Magnetic resonance in medicine.

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

[12]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[13]  J. Duncan The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour , 2010, Trends in Cognitive Sciences.

[14]  P. Goldman-Rakic,et al.  Segregation of working memory functions within the dorsolateral prefrontal cortex , 2000, Experimental Brain Research.

[15]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[16]  Adrian K. C. Lee,et al.  Auditory selective attention is enhanced by a task-irrelevant temporally coherent visual stimulus in human listeners , 2015, eLife.

[17]  M Zaitsev,et al.  Error reduction and parameter optimization of the TAPIR method for fast T1 mapping , 2003, Magnetic resonance in medicine.

[18]  W. Singer,et al.  Capture of Auditory Motion by Vision Is Represented by an Activation Shift from Auditory to Visual Motion Cortex , 2008, The Journal of Neuroscience.

[19]  Peter Thier,et al.  Dissociable Roles of the Superior Temporal Sulcus and the Intraparietal Sulcus in Joint Attention: A Functional Magnetic Resonance Imaging Study , 2008, Journal of Cognitive Neuroscience.

[20]  Nancy Kanwisher,et al.  Broad domain generality in focal regions of frontal and parietal cortex , 2013, Proceedings of the National Academy of Sciences.

[21]  J. Kaiser,et al.  Multisensory Object Perception in the Primate Brain , 2010 .

[22]  Mark W. Greenlee,et al.  Neural Correlates of Coherent Audiovisual Motion Perception , 2007 .

[23]  C. Spence,et al.  Audiovisual Temporal Integration for Complex Speech, Object-Action, Animal Call, and Musical Stimuli , 2010 .

[24]  S. Koelsch Significance of Broca's Area and Ventral Premotor Cortex for Music-Syntactic Processing , 2006, Cortex.

[25]  Justin L. Vincent,et al.  Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

[26]  Alan Kingstone,et al.  Cross-modal dynamic capture: congruency effects in the perception of motion across sensory modalities. , 2004, Journal of experimental psychology. Human perception and performance.

[27]  A. Nobre,et al.  Orienting attention in time: behavioural and neuroanatomical distinction between exogenous and endogenous shifts , 2000, Neuropsychologia.

[28]  O. Hikosaka,et al.  Switching from automatic to controlled action by monkey medial frontal cortex , 2007, Nature Neuroscience.

[29]  D. Manoach,et al.  Prefrontal cortex fMRI signal changes are correlated with working memory load , 1997, Neuroreport.

[30]  M. Hallett,et al.  Neural Correlates of Auditory–Visual Stimulus Onset Asynchrony Detection , 2001, The Journal of Neuroscience.

[31]  Jonathan D. Cohen,et al.  Dissociating working memory from task difficulty in human prefrontal cortex , 1997, Neuropsychologia.

[32]  G. Calvert Crossmodal processing in the human brain: insights from functional neuroimaging studies. , 2001, Cerebral cortex.

[33]  L. Craighero,et al.  Broca's Area in Language, Action, and Music , 2009, Annals of the New York Academy of Sciences.

[34]  Mikko Sams,et al.  Processing of audiovisual speech in Broca's area , 2005, NeuroImage.

[35]  E E Smith,et al.  Components of verbal working memory: evidence from neuroimaging. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[36]  M. Husain,et al.  Control of Visuotemporal Attention by Inferior Parietal and Superior Temporal Cortex , 2002, Current Biology.

[37]  Rhodri Cusack,et al.  The Intraparietal Sulcus and Perceptual Organization , 2005, Journal of Cognitive Neuroscience.

[38]  Kathryn M. McMillan,et al.  N‐back working memory paradigm: A meta‐analysis of normative functional neuroimaging studies , 2005, Human brain mapping.