Elastic Attention: Enhanced, then Sharpened Response to Auditory Input as Attentional Load Increases

A long debate in selective attention research is whether attention enhances sensory response or sharpens neural tuning by suppressing response to non-target input. In fact, both processes may occur as a function of load: an uncertain listener might use a broad attentional filter to enhance responses to all inputs (i.e., vigilance), yet employ sharpened tuning to focus on hard to discriminate targets. The present work used the greater signal gain, anatomical precision, and laterality separation of intracranial electrophysiological recordings (electrocorticograms) to investigate these competing effects. Data were recorded from acoustically-responsive cortex in the perisylvian region of a single hemisphere in five neurosurgery patients. Patients performed a dichotic listening task in which they alternately attended toward, away from, or completely ignored (silent reading) tones presented to designated ears at varying presentation rates. Comparisons between the grand-averaged event-related potential (ERP) waveforms show a striking change in the effect of selective auditory attention with attentional load. At slower presentation rates (low-load), ERPs were overall enhanced in response to both input channels and regardless of attended ear, including a significant enhancement of ipsilateral input. This result supports a broadly enhancing model of attention under low perceptual load conditions. At the fastest rate, however, only responses to attended inputs contralateral to grid location remained enhanced. This result supports an increasing suppression, or “sharpening,” of neural responses to non-targets with increasing attentional load. These data provide support for an elastic model of attention in which attentional scope narrows with increasing load.

[1]  Michael F. Neelon,et al.  The effects of auditory attention measured from human electrocorticograms , 2006, Clinical Neurophysiology.

[2]  Catherine Fischer,et al.  The role of the temporal pole in auditory processing. , 2002, Epileptic disorders : international epilepsy journal with videotape.

[3]  Lutz Jäncke,et al.  Attention modulates activity in the primary and the secondary auditory cortex: a functional magnetic resonance imaging study in human subjects , 1999, Neuroscience Letters.

[4]  J. Majkowski,et al.  Latency of averaged evoked potentials to contralateral and ipsilateral auditory stimulation in normal subjects. , 1971, Brain research.

[5]  L. Collet,et al.  Effect of stimulus frequency and stimulation site on the N1m response of the human auditory cortex , 2004, Hearing Research.

[6]  S. Sisodiya,et al.  The role of the interhemispheric pathway in hearing , 2007, Brain Research Reviews.

[7]  S. David,et al.  Auditory attention : focusing the searchlight on sound , 2007 .

[8]  T. Cizadlo,et al.  Auditory and visual attention assessed with PET , 1997, Human brain mapping.

[9]  Pascal Barone,et al.  Physiology of Thalamus and Cortex , 1992 .

[10]  S A Hillyard,et al.  Selective attention and the auditory vertex potential. I. Effects of stimulus delivery rate. , 1976, Electroencephalography and clinical neurophysiology.

[11]  Nilli Lavie Capacity limits in selective attention: Behavioral evidence and implications for neural activity , 2001 .

[12]  S. Debener,et al.  Late auditory evoked potentials asymmetry revisited , 2007, Clinical Neurophysiology.

[13]  Stefan Pollmann,et al.  Dichotic listening in patients with splenial and nonsplenial callosal lesions. , 2002, Neuropsychology.

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

[15]  N. Lavie Distracted and confused?: Selective attention under load , 2005, Trends in Cognitive Sciences.

[16]  M. Mishkin,et al.  Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex , 1999, Nature Neuroscience.

[17]  J. Wolpaw,et al.  The influence of stimulus intensity, contralateral masking and handedness on the temporal N1 and the T complex components of the auditory N1 wave, by John F. Connolly. , 1994, Electroencephalography and clinical neurophysiology.

[18]  M. Pinsk,et al.  Push-pull mechanism of selective attention in human extrastriate cortex. , 2004, Journal of neurophysiology.

[19]  R P Lesser,et al.  Recording of auditory evoked potentials in man using chronic subdural electrodes. , 1984, Brain : a journal of neurology.

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

[21]  R. Srinivasan Methods to Improve the Spatial Resolution of EEG , 1999 .

[22]  Olivier Bertrand,et al.  Listening in Silence Activates Auditory Areas: A Functional Magnetic Resonance Imaging Study , 2006, The Journal of Neuroscience.

[23]  S. Hillyard,et al.  Modulation of early auditory processing during selective listening to rapidly presented tones. , 1991, Electroencephalography and clinical neurophysiology.

[24]  K. Hugdahl,et al.  Attentional Effects in Dichotic Listening , 1995, Brain and Language.

[25]  Mikko Sams,et al.  Modulation of auditory cortex activation by sound presentation rate and attention , 2005, Human brain mapping.

[26]  Contra- and ipsilateral auditory stimuli produce different activation patterns at the human auditory cortex , 1988, Pflügers Archiv.

[27]  L. M. Warner,et al.  The Neural Mechanisms for Minimizing Cross-Modal Distraction , 2004, The Journal of Neuroscience.

[28]  B. Renault,et al.  Functional Anatomy of Human Auditory Attention Studied with PET , 1997, NeuroImage.

[29]  Régine Kolinsky,et al.  Attention-Dependent Changes of Activation and Connectivity in Dichotic Listening , 2002, NeuroImage.

[30]  Stefan Treue,et al.  Feature-based attention influences motion processing gain in macaque visual cortex , 1999, Nature.

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

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

[33]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[34]  R. Näätänen,et al.  Strongly focused attention and auditory event-related potentials , 1994, Biological Psychology.

[35]  Henning Scheich,et al.  Learning-induced plasticity in animal and human auditory cortex , 2005, Current Opinion in Neurobiology.

[36]  J. E. Hind,et al.  Auditory cortex on the human posterior superior temporal gyrus , 2000, The Journal of comparative neurology.

[37]  J. Maunsell,et al.  The role of attention in visual processing. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

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

[40]  J. Kaas,et al.  Auditory processing in primate cerebral cortex , 1999, Current Opinion in Neurobiology.

[41]  John C Middlebrooks,et al.  Spatial sensitivity in the dorsal zone (area DZ) of cat auditory cortex. , 2005, Journal of neurophysiology.

[42]  C D Frith,et al.  Modulating irrelevant motion perception by varying attentional load in an unrelated task. , 1997, Science.

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

[44]  M. Scherg,et al.  Intracerebral Sources of Human Auditory-Evoked Potentials , 1999, Audiology and Neurotology.

[45]  Michael F. Neelon,et al.  The effects of attentional load on auditory ERPs recorded from human cortex , 2006, Brain Research.

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

[47]  M. Tervaniemi,et al.  Selective tuning of the left and right auditory cortices during spatially directed attention. , 1999, Brain research. Cognitive brain research.

[48]  P. Chauvel,et al.  Neuromagnetic source localization of auditory evoked fields and intracerebral evoked potentials: a comparison of data in the same patients , 2001, Clinical Neurophysiology.

[49]  Kenneth Hugdahl,et al.  The role of the corpus callosum in dichotic listening: a combined morphological and diffusion tensor imaging study. , 2006, Neuropsychology.

[50]  S. Grossberg The Attentive Brain , 1995 .

[51]  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.

[52]  S. Hillyard,et al.  Cross-modal selective attention effects on retinal, myogenic, brainstem, and cerebral evoked potentials. , 1990, Psychophysiology.

[53]  J. Maunsell,et al.  Effects of task difficulty and target likelihood in area V4 of macaque monkeys. , 2006, Journal of neurophysiology.

[54]  Gerwin Schalk,et al.  Can Electrocorticography (ECoG) Support Robust and Powerful Brain–Computer Interfaces? , 2010, Front. Neuroeng..

[55]  K. Hugdahl,et al.  Dichotic listening with forced attention in patients with temporal lobe epilepsy: significance of left hemisphere cognitive dysfunction. , 2006, Scandinavian journal of psychology.

[56]  The Role of Attention in Visual Processing , 1991 .

[57]  J. Fell,et al.  Lateralized auditory spatial perception and the contralaterality of cortical processing as studied with functional magnetic resonance imaging and magnetoencephalography , 1999, Human brain mapping.

[58]  J. Schnupp,et al.  Cortical Plasticity: Learning from Cortical Reorganisation , 2002, Current Biology.

[59]  Kenneth Hugdahl,et al.  The corpus callosum in dichotic listening studies of hemispheric asymmetry: A review of clinical and experimental evidence , 2008, Neuroscience & Biobehavioral Reviews.

[60]  A R Palmer,et al.  Modulation and task effects in auditory processing measured using fMRI , 2000, Human brain mapping.