Temporal integration of sequential auditory events: silent period in sound pattern activates human planum temporale

Temporal integration is a fundamental process that the brain carries out to construct coherent percepts from serial sensory events. This process critically depends on the formation of memory traces reconciling past with present events and is particularly important in the auditory domain where sensory information is received both serially and in parallel. It has been suggested that buffers for transient auditory memory traces reside in the auditory cortex. However, previous studies investigating "echoic memory" did not distinguish between brain response to novel auditory stimulus characteristics on the level of basic sound processing and a higher level involving matching of present with stored information. Here we used functional magnetic resonance imaging in combination with a regular pattern of sounds repeated every 100 ms and deviant interspersed stimuli of 100-ms duration, which were either brief presentations of louder sounds or brief periods of silence, to probe the formation of auditory memory traces. To avoid interaction with scanner noise, the auditory stimulation sequence was implemented into the image acquisition scheme. Compared to increased loudness events, silent periods produced specific neural activation in the right planum temporale and temporoparietal junction. Our findings suggest that this area posterior to the auditory cortex plays a critical role in integrating sequential auditory events and is involved in the formation of short-term auditory memory traces. This function of the planum temporale appears to be fundamental in the segregation of simultaneous sound sources.

[1]  R. Turner,et al.  Detecting Latency Differences in Event-Related BOLD Responses: Application to Words versus Nonwords and Initial versus Repeated Face Presentations , 2002, NeuroImage.

[2]  Alan C. Evans,et al.  Quantifying variability in the planum temporale: a probability map. , 1999, Cerebral cortex.

[3]  R Hari,et al.  Cerebral magnetic responses to noise bursts and pauses of different durations. , 1989, Audiology : official organ of the International Society of Audiology.

[4]  P Finkenzeller,et al.  Evoked responses as a function of external and stored information. , 1968, Electroencephalography and clinical neurophysiology.

[5]  H. Yabe,et al.  Temporal window of integration revealed by MMN to sound omission , 1997, Neuroreport.

[6]  I. Johnsrude,et al.  Spectral and temporal processing in human auditory cortex. , 2002, Cerebral cortex.

[7]  E. Schröger,et al.  Differential Contribution of Frontal and Temporal Cortices to Auditory Change Detection: fMRI and ERP Results , 2002, NeuroImage.

[8]  E R John,et al.  Information Delivery and the Sensory Evoked Potential , 1967, Science.

[9]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[10]  J. Downar,et al.  A multimodal cortical network for the detection of changes in the sensory environment , 2000, Nature Neuroscience.

[11]  W. Roth,et al.  ERPs for infrequent omissions and inclusions of stimulus elements. , 1994, Psychophysiology.

[12]  M. Hasselmo,et al.  Graded persistent activity in entorhinal cortex neurons , 2002, Nature.

[13]  R. Näätänen The role of attention in auditory information processing as revealed by event-related potentials and other brain measures of cognitive function , 1990, Behavioral and Brain Sciences.

[14]  I. Winkler,et al.  Mismatch negativity is unaffected by top-down predictive information , 2001, Neuroreport.

[15]  P. Goldman-Rakic Cellular basis of working memory , 1995, Neuron.

[16]  Karl J. Friston,et al.  Multisubject fMRI Studies and Conjunction Analyses , 1999, NeuroImage.

[17]  R. Näätänen Attention and brain function , 1992 .

[18]  J. Mäkelä,et al.  Human auditory cortex is activated by omissions of auditory stimuli , 1997, Brain Research.

[19]  K. Reinikainen,et al.  Right hemisphere dominance of different mismatch negativities. , 1991, Electroencephalography and clinical neurophysiology.

[20]  Robert J. Zatorre,et al.  Spatial Localization after Excision of Human Auditory Cortex , 2001, The Journal of Neuroscience.

[21]  Karl J. Friston,et al.  Event‐related f MRI , 1997, Human brain mapping.

[22]  A. Galaburda,et al.  Cytoarchitectonic organization of the human auditory cortex , 1980, The Journal of comparative neurology.

[23]  R. Zatorre,et al.  Functional specificity in the right human auditory cortex for perceiving pitch direction. , 2000, Brain : a journal of neurology.

[24]  J. Rauschecker,et al.  Functional Specialization in Rhesus Monkey Auditory Cortex , 2001, Science.

[25]  W. Ritter,et al.  The scalp topography of potentials associated with missing visual or auditory stimuli. , 1976, Electroencephalography and clinical neurophysiology.

[26]  R. Ilmoniemi,et al.  Temporal window of integration of auditory information in the human brain. , 1998, Psychophysiology.

[27]  K. Reinikainen,et al.  Attentive novelty detection in humans is governed by pre-attentive sensory memory , 1994, Nature.

[28]  R. Ilmoniemi,et al.  Language-specific phoneme representations revealed by electric and magnetic brain responses , 1997, Nature.

[29]  I. Winkler,et al.  The concept of auditory stimulus representation in cognitive neuroscience. , 1999, Psychological bulletin.

[30]  N. Cowan On short and long auditory stores. , 1984, Psychological bulletin.

[31]  S. Clarke,et al.  Cytochrome Oxidase, Acetylcholinesterase, and NADPH-Diaphorase Staining in Human Supratemporal and Insular Cortex: Evidence for Multiple Auditory Areas , 1997, NeuroImage.

[32]  W. Ritter,et al.  Predictability of stimulus deviance and the mismatch negativity , 1998, Neuroreport.

[33]  Á. Pascual-Leone,et al.  Fast Backprojections from the Motion to the Primary Visual Area Necessary for Visual Awareness , 2001, Science.

[34]  K. Alho,et al.  Lateralized automatic auditory processing of phonetic versus musical information: A PET study , 2000, Human brain mapping.

[35]  John G. Neuhoff,et al.  Neural Processing of Auditory Looming in the Human Brain , 2002, Current Biology.

[36]  R. Näätänen,et al.  Temporal integration of auditory information in sensory memory as reflected by the mismatch negativity , 1994, Biological Psychology.

[37]  L. Barrett‐Lennard,et al.  Graded persistent activity in entorhinal cortex neurons , 2002 .

[38]  Terence W. Picton,et al.  Temporal integration in the human auditory cortex as represented by the development of the steady-state magnetic field , 2002, Hearing Research.

[39]  M. Scherg,et al.  A Source Analysis of the Late Human Auditory Evoked Potentials , 1989, Journal of Cognitive Neuroscience.

[40]  P. Bandettini,et al.  Functional MRI of brain activation induced by scanner acoustic noise , 1998, Magnetic resonance in medicine.

[41]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[42]  Laura Busse,et al.  The ERP omitted stimulus response to “no-stim” events and its implications for fast-rate event-related fMRI designs , 2003, NeuroImage.

[43]  I. Winkler,et al.  Organizing sound sequences in the human brain: the interplay of auditory streaming and temporal integration 1 1 Published on the World Wide Web on 27 February 2001. , 2001, Brain Research.

[44]  J. Kaas,et al.  Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans , 2001, The Journal of comparative neurology.

[45]  I. Winkler,et al.  ‘Primitive intelligence’ in the auditory cortex , 2001, Trends in Neurosciences.

[46]  Hans-Jochen Heinze,et al.  A movement-sensitive area in auditory cortex , 1999, Nature.

[47]  C. Schroeder,et al.  Role of cortical N-methyl-D-aspartate receptors in auditory sensory memory and mismatch negativity generation: implications for schizophrenia. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[48]  T. Griffiths,et al.  The planum temporale as a computational hub , 2002, Trends in Neurosciences.

[49]  Albert S. Bregman,et al.  The Auditory Scene. (Book Reviews: Auditory Scene Analysis. The Perceptual Organization of Sound.) , 1990 .

[50]  R. Hari,et al.  Omissions of Auditory Stimuli May Activate Frontal Cortex , 1989, The European journal of neuroscience.

[51]  T. Sejnowski,et al.  Single-Trial Variability in Event-Related BOLD Signals , 2002, NeuroImage.

[52]  John G. Neuhoff,et al.  Spatiotemporal Pattern of Neural Processing in the Human Auditory Cortex , 2002, Science.

[53]  Wolfgang Grodd,et al.  Mismatch responses to randomized gradient switching noise as reflected by fMRI and whole‐head magnetoencephalography , 2002, Human brain mapping.

[54]  K Scheffler,et al.  The MR tomograph as a sound generator: fMRI tool for the investigation of the auditory cortex , 1998, Magnetic resonance in medicine.

[55]  Karl J. Friston,et al.  Cognitive Conjunction: A New Approach to Brain Activation Experiments , 1997, NeuroImage.

[56]  L. Schiebinger,et al.  Commentary on Risto Naatanen (1990). The role of attention in auditory information processing as revealed by event-related potentials and other brain measures of cognitive fenctiono BBS 13s201-2888 , 1991 .

[57]  T. M. Darcey,et al.  Responses of Human Auditory Association Cortex to the Omission of an Expected Acoustic Event , 2001, NeuroImage.

[58]  J. Rauschecker,et al.  Perception of Sound-Source Motion by the Human Brain , 2002, Neuron.

[59]  R. Goebel,et al.  The functional neuroanatomy of target detection: an fMRI study of visual and auditory oddball tasks. , 1999, Cerebral cortex.

[60]  A R Palmer,et al.  Time‐course of the auditory BOLD response to scanner noise , 2000, Magnetic resonance in medicine.