Distinct Pathways Involved in Sound Recognition and Localization: A Human fMRI Study

Evidence from psychophysical studies in normal and brain-damaged subjects suggests that auditory information relevant to recognition and localization are processed by distinct neuronal populations. We report here on anatomical segregation of these populations. Brain activation associated with performance in sound identification and localization was investigated in 18 normal subjects using fMRI. Three conditions were used: (i) comparison of spatial stimuli simulated with interaural time differences; (ii) identification of environmental sounds; and (iii) rest. Conditions (i) and (ii) required acknowledgment of predefined targets by pressing a button. After coregistering, images were normalized and smoothed. Activation patterns were analyzed using SPM99 for individual subjects and for the whole group. Sound recognition and localization activated, as compared to rest, inferior colliculus, medial geniculate body, Heschl gyrus, and parts of the temporal, parietal, and frontal convexity bilaterally. The activation pattern on the fronto-temporo-parietal convexity differed in the two conditions. Middle temporal gyrus and precuneus bilaterally and the posterior part of left inferior frontal gyrus were more activated by recognition than by localization. Lower part of inferior parietal lobule and posterior parts of middle and inferior frontal gyri were more activated, bilaterally, by localization than by recognition. Regions selectively activated by sound recognition, but not those selectively activated by localization, were significantly larger in women. Passive listening paradigm revealed segregated pathways on superior temporal gyrus and inferior parietal lobule. Thus, anatomically distinct networks are involved in sound recognition and sound localization.

[1]  L P SANCHEZ-LONGO,et al.  Clinical Significance of Impairment of Sound Localization , 1958, Neurology.

[2]  A. Benton,et al.  AUDITORY AGNOSIA WITHOUT APHASIA. , 1965, Archives of neurology.

[3]  Gerald H. Klingon,et al.  Localization in auditory space , 1966, Neurology.

[4]  H. Spinnler,et al.  Impaired Recognition of Meaningful Sounds in Aphasia , 1966 .

[5]  H Spinnler,et al.  Contrasting behavior of right and left hemisphere-damaged patients on a discriminative and a semantic task of auditory recognition. , 1969, Cortex; a journal devoted to the study of the nervous system and behavior.

[6]  L Weiskrantz,et al.  Disruptions of auditory sequence discrimination by unilateral and bilateral cortical ablations of superior temporal gyrus in the monkey. , 1970, Experimental neurology.

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

[8]  J. Jerger,et al.  Auditory disorder following bilateral temporal lobe insult: report of a case. , 1972, The Journal of speech and hearing disorders.

[9]  M. Albert,et al.  A case study of auditory agnosia: linguistic and non-linguistic processing. , 1999, Cortex; a journal devoted to the study of the nervous system and behavior.

[10]  M. Albert,et al.  A Case Study of auditory Agnosia: Linguistic and Non-Linguistic Processing , 1972 .

[11]  Lawrence Weiskrantz,et al.  Auditory sequence discrimanation in macaca mulatta: The role of the superior temporal cortex , 1976, Neuropsychologia.

[12]  J. A. Altman,et al.  Effects of unilateral disorder of the brain hemisphere function in man on directional hearing , 1979, Neuropsychologia.

[13]  S. Bentin,et al.  Reduction in Regional Cerebral Blood Flow During Normal Aging in Man , 1980, Stroke.

[14]  K. H. Pribram,et al.  Auditory spatial deficits in the personal and extrapersonal frames of reference due to cortical lesions , 1981, Neuropsychologia.

[15]  L. Vignolo,et al.  Auditory agnosia. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[16]  L. Vignolo,et al.  The neuropsychology of cognitive function - Auditory agnosia , 1982 .

[17]  E. Yund,et al.  Central auditory processing III. The “cocktail party” effect and anterior temporal lobectomy , 1983, Brain and Language.

[18]  James H. Halsey,et al.  rCBF For Middle-Aged Males and Females During Right-Left Discrimination , 1983, Cortex.

[19]  Leslie G. Ungerleider,et al.  Object vision and spatial vision: two cortical pathways , 1983, Trends in Neurosciences.

[20]  P. Pohl Central auditory processing , 1983 .

[21]  Reduction in regional cerebral blood flow during normal aging is not limited to elderly subjects. , 1984, Monographs in neural sciences.

[22]  E. Bisiach,et al.  Disorders of perceived auditory lateralization after lesions of the right hemisphere. , 1984, Brain : a journal of neurology.

[23]  R. L. Rogers,et al.  Cerebral blood flow changes in benign aging and cerebrovascular disease , 1984, Neurology.

[24]  H. Heffner,et al.  Temporal lobe lesions and perception of species-specific vocalizations by macaques. , 1984, Science.

[25]  Mortimer Mishkin,et al.  Visual recognition impairment follows ventromedial but not dorsolateral prefrontal lesions in monkeys , 1986, Behavioural Brain Research.

[26]  H. Heffner,et al.  Effect of unilateral and bilateral auditory cortex lesions on the discrimination of vocalizations by Japanese macaques. , 1986, Journal of neurophysiology.

[27]  Michael E. Phelps,et al.  Cerebral glucose metabolic rates in normal human females versus normal males , 1987, Psychiatry Research.

[28]  R. Schmieder,et al.  Disparate cardiovascular findings in men and women with essential hypertension. , 1987, Annals of internal medicine.

[29]  A. Alavi,et al.  The Effect of Anxiety on Cortical Cerebral Blood Flow and Metabolism , 1987, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[30]  M D Ginsberg,et al.  Sensitivity of Cerebral Glucose Metabolism to Age, Gender, Brain Volume, Brain Atrophy, and Cerebrovascular Risk Factors , 1988, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[31]  G. Rodriguez,et al.  Sex Differences in Regional Cerebral Blood Flow , 1988, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[32]  M. Mendez,et al.  Cortical auditory disorders: clinical and psychoacoustic features. , 1988, Journal of neurology, neurosurgery, and psychiatry.

[33]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[34]  H. Buchtel,et al.  Auditory agnosia: Apperceptive or associative disorder? , 1989, Brain and Language.

[35]  R. Gur,et al.  Gender differences in regional cerebral blood flow. , 1990, Schizophrenia bulletin.

[36]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

[37]  Toshikatsu Fujii,et al.  Auditory Sound Agnosia without Aphasia Following a Right Temporal Lobe Lesion , 1990, Cortex.

[38]  C. Gross,et al.  Auditory association cortex lesions impair auditory short-term memory in monkeys. , 1990, Science.

[39]  Leslie G. Ungerleider,et al.  Dissociation of object and spatial visual processing pathways in human extrastriate cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[40]  M. Brouchon,et al.  Head turning versus manual pointing to auditory targets in normal subjects and in subjects with right parietal damage , 1992, Brain and Cognition.

[41]  M. Corbetta,et al.  A PET study of visuospatial attention , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  Karl J. Friston,et al.  Functional mapping of brain areas implicated in auditory--verbal memory function. , 1993, Brain : a journal of neurology.

[43]  D. M. Green,et al.  A panoramic code for sound location by cortical neurons. , 1994, Science.

[44]  D. Benson,et al.  Non-verbal environmental sound recognition after unilateral hemispheric stroke. , 1994, Brain : a journal of neurology.

[45]  R. S. J. Frackowiak,et al.  Human cortical areas selectively activated by apparent sound movement , 1994, Current Biology.

[46]  J. Villemure,et al.  Sound localization in hemispherectomized patients , 1994, Neuropsychologia.

[47]  Leslie G. Ungerleider,et al.  ‘What’ and ‘where’ in the human brain , 1994, Current Opinion in Neurobiology.

[48]  J. Rauschecker,et al.  Processing of complex sounds in the macaque nonprimary auditory cortex. , 1995, Science.

[49]  P M Grasby,et al.  Brain systems for encoding and retrieval of auditory-verbal memory. An in vivo study in humans. , 1995, Brain : a journal of neurology.

[50]  V B Mountcastle,et al.  The parietal system and some higher brain functions. , 1995, Cerebral cortex.

[51]  R J Zatorre,et al.  Preserved auditory spatial localization following cerebral hemispherectomy. , 1995, Brain : a journal of neurology.

[52]  A Engelien,et al.  The functional anatomy of recovery from auditory agnosia. A PET study of sound categorization in a neurological patient and normal controls. , 1995, Brain : a journal of neurology.

[53]  R. Andersen,et al.  Eye-centered, head-centered, and intermediate coding of remembered sound locations in area LIP. , 1996, Journal of neurophysiology.

[54]  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.

[55]  Stephanie Clarke,et al.  Non-verbal auditory recognition in normal subjects and brain-damaged patients: Evidence for parallel processing , 1996, Neuropsychologia.

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

[57]  Alan C. Evans,et al.  Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: a positron emission tomography study. , 1996, Cerebral cortex.

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

[59]  T. Paus Location and function of the human frontal eye-field: A selective review , 1996, Neuropsychologia.

[60]  Alan C. Evans,et al.  Planning and Spatial Working Memory: a Positron Emission Tomography Study in Humans , 1996, The European journal of neuroscience.

[61]  Volker Hömberg,et al.  Sound localization in egocentric space following hemispheric lesions , 1996, Neuropsychologia.

[62]  C Witton,et al.  Spatial and temporal auditory processing deficits following right hemisphere infarction. A psychophysical study. , 1997, Brain : a journal of neurology.

[63]  T. Kumagai,et al.  Human cortico‐hippocampal activity related to auditory discrimination revealed by neuromagmetic field , 1997, Neuroreport.

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

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

[66]  Karl J. Friston,et al.  How the brain learns to see objects and faces in an impoverished context , 1997, Nature.

[67]  A. Owen The Functional Organization of Working Memory Processes Within Human Lateral Frontal Cortex: The Contribution of Functional Neuroimaging , 1997, The European journal of neuroscience.

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

[69]  J. Rauschecker Processing of complex sounds in the auditory cortex of cat, monkey, and man. , 1997, Acta oto-laryngologica. Supplementum.

[70]  Timothy D. Griffiths,et al.  Spatial and temporal auditory processing deficits following right hemisphere infarction , 1997 .

[71]  S. Clarke,et al.  Distinct short‐term memory systems for sound content and sound localization , 1998, Neuroreport.

[72]  A. Nobre,et al.  Where and When to Pay Attention: The Neural Systems for Directing Attention to Spatial Locations and to Time Intervals as Revealed by Both PET and fMRI , 1998, The Journal of Neuroscience.

[73]  C D Frith,et al.  The functional roles of prefrontal cortex in episodic memory. II. Retrieval. , 1998, Brain : a journal of neurology.

[74]  J J Jaeger,et al.  Sex differences in brain regions activated by grammatical and reading tasks , 1998, Neuroreport.

[75]  Alan C. Evans,et al.  Event-related fMRI of the auditory cortex. , 1998, NeuroImage.

[76]  C. Frith,et al.  Differential Activation of Right Superior Parietal Cortex and Intraparietal Sulcus by Spatial and Nonspatial Attention , 1998, NeuroImage.

[77]  T. Shallice,et al.  The functional roles of prefrontal cortex in episodic memory. I. Encoding. , 1998, Brain : a journal of neurology.

[78]  C. Fischer,et al.  [Auditory perception disorders due to bilateral cortical lesions. An electrophysiology study]. , 1998, Revue neurologique.

[79]  Richard S. J. Frackowiak,et al.  Right parietal cortex is involved in the perception of sound movement in humans , 1998, Nature Neuroscience.

[80]  M. Petrides,et al.  Functional organization of spatial and nonspatial working memory processing within the human lateral frontal cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[82]  S. Clarke,et al.  Compartments within human primary auditory cortex: evidence from cytochrome oxidase and acetylcholinesterase staining , 1998, The European journal of neuroscience.

[83]  R. Benedict,et al.  Functional neuroimaging of attention in the auditory modality , 1998, Neuroreport.

[84]  R. Bowtell,et al.  “sparse” temporal sampling in auditory fMRI , 1999, Human brain mapping.

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

[86]  R. Burkard,et al.  The functional anatomy of the normal human auditory system: responses to 0.5 and 4.0 kHz tones at varied intensities. , 1999, Cerebral cortex.

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

[88]  Jon H. Kaas,et al.  'What' and 'where' processing in auditory cortex , 1999, Nature Neuroscience.

[89]  J. Kaas,et al.  Prefrontal connections of the parabelt auditory cortex in macaque monkeys , 1999, Brain Research.

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

[91]  J. Lauter Central auditory processing , 1999 .

[92]  G H Glover,et al.  Gender Differences in Cerebral Blood Flow and Oxygenation Response during Focal Physiologic Neural Activity , 1999, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[93]  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.

[94]  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.

[95]  J. Rauschecker,et al.  A PET study of human auditory spatial processing , 1999, Neuroscience Letters.

[96]  R. Weisskoff,et al.  Quantitative assessment of auditory cortex responses induced by imager acoustic noise , 1999, Human brain mapping.

[97]  J. Rauschecker,et al.  Modality-specific frontal and parietal areas for auditory and visual spatial localization in humans , 1999, Nature Neuroscience.

[98]  C R Genovese,et al.  Cortical networks subserving pursuit and saccadic eye movements in humans: An FMRI study , 1999, Human brain mapping.

[99]  J. Thiran,et al.  Distinct pathways involved in sound recognition and localization: A human fMRI study , 2000, NeuroImage.

[100]  Raquel E Gur,et al.  Sex differences in brain-behavior relationships between verbal episodic memory and resting regional cerebral blood flow , 2000, Neuropsychologia.

[101]  R. Meuli,et al.  Auditory agnosia and auditory spatial deficits following left hemispheric lesions: evidence for distinct processing pathways , 2000, Neuropsychologia.

[102]  B. Turetsky,et al.  An fMRI Study of Sex Differences in Regional Activation to a Verbal and a Spatial Task , 2000, Brain and Language.

[103]  What and where in human audition: Distinct cortical processing pathways revealed by fMRI , 2000 .

[104]  A Rees,et al.  Human brain areas involved in the analysis of auditory movement , 2000, Human brain mapping.

[105]  Mark Hallett,et al.  Gender Difference in Premotor Activity during Active Tactile Discrimination , 2000, NeuroImage.

[106]  Jean-Philippe Thiran,et al.  Optimisation of stimuli and acquisition technique for fMRI of the auditory system , 2000, NeuroImage.

[107]  J. Rauschecker,et al.  Mechanisms and streams for processing of "what" and "where" in auditory cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.