Attention-driven auditory cortex short-term plasticity helps segregate relevant sounds from noise

How can we concentrate on relevant sounds in noisy environments? A “gain model” suggests that auditory attention simply amplifies relevant and suppresses irrelevant afferent inputs. However, it is unclear whether this suffices when attended and ignored features overlap to stimulate the same neuronal receptive fields. A “tuning model” suggests that, in addition to gain, attention modulates feature selectivity of auditory neurons. We recorded magnetoencephalography, EEG, and functional MRI (fMRI) while subjects attended to tones delivered to one ear and ignored opposite-ear inputs. The attended ear was switched every 30 s to quantify how quickly the effects evolve. To produce overlapping inputs, the tones were presented alone vs. during white-noise masking notch-filtered ±1/6 octaves around the tone center frequencies. Amplitude modulation (39 vs. 41 Hz in opposite ears) was applied for “frequency tagging” of attention effects on maskers. Noise masking reduced early (50–150 ms; N1) auditory responses to unattended tones. In support of the tuning model, selective attention canceled out this attenuating effect but did not modulate the gain of 50–150 ms activity to nonmasked tones or steady-state responses to the maskers themselves. These tuning effects originated at nonprimary auditory cortices, purportedly occupied by neurons that, without attention, have wider frequency tuning than ±1/6 octaves. The attentional tuning evolved rapidly, during the first few seconds after attention switching, and correlated with behavioral discrimination performance. In conclusion, a simple gain model alone cannot explain auditory selective attention. In nonprimary auditory cortices, attention-driven short-term plasticity retunes neurons to segregate relevant sounds from noise.

[1]  B. Shinn-Cunningham,et al.  Task-modulated “what” and “where” pathways in human auditory cortex , 2006, Proceedings of the National Academy of Sciences.

[2]  C. Pantev,et al.  Attention Improves Population-Level Frequency Tuning in Human Auditory Cortex , 2007, The Journal of Neuroscience.

[3]  R. Zatorre,et al.  Shifting and focusing auditory spatial attention. , 1995, Journal of experimental psychology. Human perception and performance.

[4]  A. Dale,et al.  Distributed current estimates using cortical orientation constraints , 2006, Human brain mapping.

[5]  C. Pantev,et al.  Frequency-specific modulation of population-level frequency tuning in human auditory cortex , 2009, BMC Neuroscience.

[6]  G. Recanzone,et al.  Frequency and intensity response properties of single neurons in the auditory cortex of the behaving macaque monkey. , 2000, Journal of neurophysiology.

[7]  Alan C. Evans,et al.  Auditory Attention to Space and Frequency Activates Similar Cerebral Systems , 1999, NeuroImage.

[8]  Jun Yan,et al.  Corticofugal Modulation of Initial Sound Processing in the Brain , 2008, The Journal of Neuroscience.

[9]  Brian R Glasberg,et al.  Derivation of auditory filter shapes from notched-noise data , 1990, Hearing Research.

[10]  E. Halgren,et al.  Dynamic Statistical Parametric Mapping Combining fMRI and MEG for High-Resolution Imaging of Cortical Activity , 2000, Neuron.

[11]  F. Bloom,et al.  Modulation of early sensory processing in human auditory cortex during auditory selective attention. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[13]  T. Womelsdorf,et al.  Dynamic shifts of visual receptive fields in cortical area MT by spatial attention , 2006, Nature Neuroscience.

[14]  Kenneth Hugdahl,et al.  Identification of attention and cognitive control networks in a parametric auditory fMRI study , 2010, Neuropsychologia.

[15]  Teemu Rinne,et al.  Functional Maps of Human Auditory Cortex: Effects of Acoustic Features and Attention , 2009, PloS one.

[16]  J Mazziotta,et al.  A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[17]  Mark W. Woolrich,et al.  Bayesian analysis of neuroimaging data in FSL , 2009, NeuroImage.

[18]  I. Fried,et al.  Ultra-fine frequency tuning revealed in single neurons of human auditory cortex , 2008, Nature.

[19]  Roger B. H. Tootell,et al.  The advantage of combining MEG and EEG: Comparison to fMRI in focally stimulated visual cortex , 2007, NeuroImage.

[20]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[21]  K Alho,et al.  Selective attention in auditory processing as reflected by event-related brain potentials. , 1992, Psychophysiology.

[22]  S. Hillyard,et al.  Electrical Signs of Selective Attention in the Human Brain , 1973, Science.

[23]  Joonyeol Lee,et al.  A Normalization Model of Attentional Modulation of Single Unit Responses , 2009, PloS one.

[24]  J. Belliveau,et al.  Short-term plasticity in auditory cognition , 2007, Trends in Neurosciences.

[25]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

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

[27]  Mikko Sams,et al.  Selective Attention Increases Both Gain and Feature Selectivity of the Human Auditory Cortex , 2007, PloS one.

[28]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[29]  S. David,et al.  Does attention play a role in dynamic receptive field adaptation to changing acoustic salience in A1? , 2007, Hearing Research.

[30]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[31]  Lutz Jäncke,et al.  Focused attention in a simple dichotic listening task: an fMRI experiment. , 2003, Brain research. Cognitive brain research.

[32]  C Alain,et al.  Selectively attending to auditory objects. , 2000, Frontiers in bioscience : a journal and virtual library.

[33]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[34]  S. Hillyard,et al.  Temporal dynamics of selective attention during dichotic listening. , 2009, Cerebral cortex.

[35]  Risto N t nen Attention and brain function , 1992 .

[36]  N. Kraus,et al.  Musical Experience Limits the Degradative Effects of Background Noise on the Neural Processing of Sound , 2009, The Journal of Neuroscience.

[37]  Mounya Elhilali,et al.  Task Difficulty and Performance Induce Diverse Adaptive Patterns in Gain and Shape of Primary Auditory Cortical Receptive Fields , 2009, Neuron.

[38]  John W Belliveau,et al.  Monte Carlo simulation studies of EEG and MEG localization accuracy , 2002, Human brain mapping.

[39]  E. Wojciulik,et al.  Attention increases neural selectivity in the human lateral occipital complex , 2004, Nature Neuroscience.

[40]  A K Liu,et al.  Spatiotemporal imaging of human brain activity using functional MRI constrained magnetoencephalography data: Monte Carlo simulations. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[41]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[42]  S. Hillyard,et al.  Endogenous brain potentials associated with selective auditory attention. , 1980, Electroencephalography and clinical neurophysiology.

[43]  Riitta Salmelin,et al.  Evidence of sharp frequency tuning in the human auditory cortex , 1994, Hearing Research.

[44]  A. Dale,et al.  Improved Localizadon of Cortical Activity by Combining EEG and MEG with MRI Cortical Surface Reconstruction: A Linear Approach , 1993, Journal of Cognitive Neuroscience.

[45]  J. Fritz,et al.  Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex , 2003, Nature Neuroscience.

[46]  Sabine Kastner,et al.  Beyond a relay nucleus: neuroimaging views on the human LGN. , 2006, Progress in brain research.

[47]  E. Yund,et al.  Attentional modulation of human auditory cortex , 2004, Nature Neuroscience.

[48]  S. Hillyard,et al.  Selective attention and the auditory vertex potential. Effects of signal intensity and masking noise. , 1976, Electroencephalography and clinical neurophysiology.

[49]  J. Rauschecker Parallel Processing in the Auditory Cortex of Primates , 1998, Audiology and Neurotology.

[50]  E. Vogel,et al.  Sensory gain control (amplification) as a mechanism of selective attention: electrophysiological and neuroimaging evidence. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[51]  N. Logothetis The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[52]  J. Rauschecker,et al.  Attention‐related modulation of activity in primary and secondary auditory cortex , 1997, Neuroreport.