The Right Planum Temporale Is Involved in Stimulus-Driven, Auditory Attention – Evidence from Transcranial Magnetic Stimulation

It is well known that the planum temporale (PT) area in the posterior temporal lobe carries out spectro-temporal analysis of auditory stimuli, which is crucial for speech, for example. There are suggestions that the PT is also involved in auditory attention, specifically in the discrimination and selection of stimuli from the left and right ear. However, direct evidence is missing so far. To examine the role of the PT in auditory attention we asked fourteen participants to complete the Bergen Dichotic Listening Test. In this test two different consonant-vowel syllables (e.g., “ba” and “da”) are presented simultaneously, one to each ear, and participants are asked to verbally report the syllable they heard best or most clearly. Thus attentional selection of a syllable is stimulus-driven. Each participant completed the test three times: after their left and right PT (located with anatomical brain scans) had been stimulated with repetitive transcranial magnetic stimulation (rTMS), which transiently interferes with normal brain functioning in the stimulated sites, and after sham stimulation, where participants were led to believe they had been stimulated but no rTMS was applied (control). After sham stimulation the typical right ear advantage emerged, that is, participants reported relatively more right than left ear syllables, reflecting a left-hemispheric dominance for language. rTMS over the right but not left PT significantly reduced the right ear advantage. This was the result of participants reporting more left and fewer right ear syllables after right PT stimulation, suggesting there was a leftward shift in stimulus selection. Taken together, our findings point to a new function of the PT in addition to auditory perception: particularly the right PT is involved in stimulus selection and (stimulus-driven), auditory attention.

[1]  D. Kimura.  Functional Asymmetry of the Brain in Dichotic Listening , 1967 .

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

[3]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[4]  Kenneth Hugdahl,et al.  Dichotic listening reveals functional specificity in prefrontal cortex: an fMRI study , 2004, NeuroImage.

[5]  P. Rossini,et al.  Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. , 1994, Electroencephalography and clinical neurophysiology.

[6]  L. Jäncke,et al.  Focused and Nonfocused Attention in Verbal and Emotional Dichotic Listening: An FMRI Study , 2001, Brain and Language.

[7]  R. C. Oldfield.  THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

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

[9]  N. Geschwind,et al.  Dichotic Listening in Man after Section of Neocortical Commissures , 1968 .

[10]  René Westerhausen,et al.  Handedness, dichotic-listening ear advantage, and gender effects on planum temporale asymmetry—A volumetric investigation using structural magnetic resonance imaging , 2006, Neuropsychologia.

[11]  Kenneth Hugdahl,et al.  Sex differences in language asymmetry are age-dependent and small: A large-scale, consonant–vowel dichotic listening study with behavioral and fMRI data , 2013, Cortex.

[12]  B Milner,et al.  Lateralized Suppression of Dichotically Presented Digits after Commissural Section in Man , 1968, Science.

[13]  Kenneth Hugdahl,et al.  Processing of sub-syllabic speech units in the posterior temporal lobe: An fMRI study , 2005, NeuroImage.

[14]  A. Lundervold,et al.  Dichotic-listening performance and intracarotid injections of amobarbital in children and adolescents. Preoperative and postoperative comparisons. , 1997, Archives of neurology.

[15]  M. Studdert-Kennedy,et al.  Hemispheric specialization for speech perception. , 1970, The Journal of the Acoustical Society of America.

[16]  Karl J. Friston,et al.  The Role of the Thalamus in “Top Down” Modulation of Attention to Sound , 1996, NeuroImage.

[17]  A. Beaton,et al.  The Relation of Planum Temporale Asymmetry and Morphology of the Corpus Callosum to Handedness, Gender, and Dyslexia: A Review of the Evidence , 1997, Brain and Language.

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

[19]  Dani Byrd,et al.  Auditory Selective Attention: An fMRI Investigation , 1996, NeuroImage.

[20]  Kenneth Hugdahl,et al.  A new verbal reports fMRI dichotic listening paradigm for studies of hemispheric asymmetry , 2008, NeuroImage.

[21]  S. Ferber,et al.  Spatial awareness is a function of the temporal not the posterior parietal lobe , 2001, Nature.

[22]  Kenneth Hugdahl,et al.  A forced-attention dichotic listening fMRI study on 113 subjects , 2012, Brain and Language.

[23]  R. Cattelani,et al.  Hemispheric Prevalence Changes in Partial Epileptic Patients on Perceptual and Attentional Tasks , 1985, Epilepsia.

[24]  Kenneth Hugdahl,et al.  Functional relevance of interindividual differences in temporal lobe callosal pathways: a DTI tractography study. , 2009, Cerebral cortex.

[25]  Gregory P. Lee,et al.  Do dichotic word listening asymmetries predict side of temporal lobe seizure onset? , 1994, Epilepsy Research.

[26]  D. Broadbent.  The role of auditory localization in attention and memory span. , 1954, Journal of experimental psychology.

[27]  D. Perani,et al.  The anatomy of unilateral neglect after right-hemisphere stroke lesions. A clinical/CT-scan correlation study in man , 1986, Neuropsychologia.

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

[29]  Yasushi Miyashita,et al.  Functional Differentiation in the Human Auditory and Language Areas Revealed by a Dichotic Listening Task , 2000, NeuroImage.

[30]  E. Wassermann.  Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. , 1998, Electroencephalography and clinical neurophysiology.

[31]  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.

[32]  Responses to Dichotic Listening Tasks in Temporal Epileptics With or Without Clinically Evident Lesions , 1978, Cortex.

[33]  Alessandro Farnè,et al.  Neglect: A multisensory deficit? , 2012, Neuropsychologia.

[34]  N. Geschwind,et al.  Human Brain: Left-Right Asymmetries in Temporal Speech Region , 1968, Science.

[35]  Leonie de Visser,et al.  A critical review of sex differences in decision-making tasks: Focus on the Iowa Gambling Task , 2013, Behavioural Brain Research.

[36]  P. Birkett.  Measures of laterality and theories of hemispheric processes , 1977, Neuropsychologia.

[37]  Kenneth Hugdahl,et al.  Attention-related modulation of auditory-cortex responses to speech sounds during dichotic listening , 2012, Brain Research.

[38]  Karsten Specht,et al.  Functional segregation of the temporal lobes into highly differentiated subsystems for auditory perception: an auditory rapid event-related fMRI-task , 2003, NeuroImage.

[39]  Igor Schindler,et al.  An exploration of the role of the superior temporal gyrus in visual search and spatial perception using TMS , 2014 .

[40]  Kenneth Hugdahl,et al.  The effect of voice-onset-time on dichotic listening with consonant–vowel syllables , 2006, Neuropsychologia.

[41]  Seppo Kähkönen,et al.  The novelty value of the combined use of electroencephalography and transcranial magnetic stimulation for neuroscience research , 2006, Brain Research Reviews.

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

[43]  Alan Cowey,et al.  The Ferrier Lecture 2004 What can transcranial magnetic stimulation tell us about how the brain works? , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[44]  D. Broadbent.  Listening to one of two synchronous messages. , 1952, Journal of experimental psychology.

[45]  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.

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

[47]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[48]  V. Walsh,et al.  State-dependency in brain stimulation studies of perception and cognition , 2008, Trends in Cognitive Sciences.

[49]  Daniel S. O'Leary,et al.  A Positron Emission Tomography Study of Binaurally and Dichotically Presented Stimuli: Effects of Level of Language and Directed Attention , 1996, Brain and Language.

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

[51]  J. Rothwell,et al.  Preconditioning of Low-Frequency Repetitive Transcranial Magnetic Stimulation with Transcranial Direct Current Stimulation: Evidence for Homeostatic Plasticity in the Human Motor Cortex , 2004, The Journal of Neuroscience.

[52]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[53]  Stefan Pollmann,et al.  A Unified Structural-Attentional Framework for Dichotic Listening , 2010 .

[54]  K. Hugdahl,et al.  The “Forced-Attention Paradigm” in Dichotic Listening to CV-Syllables: A Comparison Between Adults and Children , 1986, Cortex.

[55]  J. Thiran,et al.  Distinct Pathways Involved in Sound Recognition and Localization: A Human fMRI Study , 2000, NeuroImage.

[56]  Marco Hirnstein,et al.  TMS over the left angular gyrus impairs the ability to discriminate left from right , 2011, Neuropsychologia.

[57]  S. Rossi,et al.  Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research , 2009, Clinical Neurophysiology.

[58]  D. Long,et al.  Transcranial Magnetic Stimulation: A Neurochronometrics of Mind , 2004 .

[59]  S. Pollmann,et al.  Splenial lesions lead to supramodal target detection deficits. , 2004, Neuropsychology.

[60]  J. Rauschecker,et al.  Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing , 2009, Nature Neuroscience.

[61]  R J Wise,et al.  Separate neural subsystems within 'Wernicke's area'. , 2001, Brain : a journal of neurology.