Auditory perception vs. recognition: representation of complex communication sounds in the mouse auditory cortical fields

Details of brain areas for acoustical Gestalt perception and the recognition of species‐specific vocalizations are not known. Here we show how spectral properties and the recognition of the acoustical Gestalt of wriggling calls of mouse pups based on a temporal property are represented in auditory cortical fields and an association area (dorsal field) of the pups' mothers. We stimulated either with a call model releasing maternal behaviour at a high rate (call recognition) or with two models of low behavioural significance (perception without recognition). Brain activation was quantified using c‐Fos immunocytochemistry, counting Fos‐positive cells in electrophysiologically mapped auditory cortical fields and the dorsal field. A frequency‐specific labelling in two primary auditory fields is related to call perception but not to the discrimination of the biological significance of the call models used. Labelling related to call recognition is present in the second auditory field (AII). A left hemisphere advantage of labelling in the dorsoposterior field seems to reflect an integration of call recognition with maternal responsiveness. The dorsal field is activated only in the left hemisphere. The spatial extent of Fos‐positive cells within the auditory cortex and its fields is larger in the left than in the right hemisphere. Our data show that a left hemisphere advantage in processing of a species‐specific vocalization up to recognition is present in mice. The differential representation of vocalizations of high vs. low biological significance, as seen only in higher‐order and not in primary fields of the auditory cortex, is discussed in the context of perceptual strategies.

[1]  D. Moody,et al.  Neural lateralization of species-specific vocalizations by Japanese macaques (Macaca fuscata). , 1978, Science.

[2]  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.

[3]  J. Kaas,et al.  Subdivisions of auditory cortex and processing streams in primates. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[4]  N. Geschwind,et al.  Right-left asymmetrics in the brain. , 1978, Science.

[5]  A. Schleicher,et al.  Excitatory and inhibitory neurons express c-Fos in barrel-related columns after exploration of a novel environment , 2002, Neuroscience.

[6]  Richard S. J. Frackowiak,et al.  The anatomy of phonological and semantic processing in normal subjects. , 1992, Brain : a journal of neurology.

[7]  L. Kaczmarek,et al.  Sensory regulation of immediate–early gene expression in mammalian visual cortex: implications for functional mapping and neural plasticity , 1997, Brain Research Reviews.

[8]  R. Ilmoniemi,et al.  Processing of novel sounds and frequency changes in the human auditory cortex: magnetoencephalographic recordings. , 1998, Psychophysiology.

[9]  B. T. Woods,et al.  Is the left hemisphere specialized for language at birth? , 1983, Trends in Neurosciences.

[10]  Stephen McAdams,et al.  Dichotic perception and laterality in neonates , 1989, Brain and Language.

[11]  William C. Stebbins,et al.  Perception of Conspecific Vocalizations by Japanese Macaques , 1979 .

[12]  A. J. Moffat,et al.  II. Single unit responses to tones, noise and tone-noise combinations as a function of sound intensity , 1985 .

[13]  M W Brown,et al.  Fos imaging reveals differential neuronal activation of areas of rat temporal cortex by novel and familiar sounds , 2001, The European journal of neuroscience.

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

[15]  Henning Scheich,et al.  Functional Organization of Auditory Cortex in the Mongolian Gerbil (Meriones unguiculatus). I. Electrophysiological Mapping of Frequency Representation and Distinction of Fields , 1993, The European journal of neuroscience.

[16]  M. Greenberg,et al.  The regulation and function of c-fos and other immediate early genes in the nervous system , 1990, Neuron.

[17]  W. Tischmeyer,et al.  Activation of immediate early genes and memory formation , 1999, Cellular and Molecular Life Sciences CMLS.

[18]  G. Ehret Left hemisphere advantage in the mouse brain for recognizing ultrasonic communication calls , 1987, Nature.

[19]  L. Kaczmarek Molecular biology of vertebrate learning: Is c‐fos a new beginning? , 1993, Journal of neuroscience research.

[20]  O Bertrand,et al.  Analysis of speech sounds is left-hemisphere predominant at 100-150ms after sound onset. , 1999, Neuroreport.

[21]  Alan C. Evans,et al.  Left‐hemisphere specialization for the processing of acoustic transients , 1997, Neuroreport.

[22]  H Scheich,et al.  Comparison of Frequency‐specific c‐Fos Expression and Fluoro‐2‐deoxyglucose Uptake in Auditory Cortex of Gerbils (Meriones unguiculatus) , 1995, The European journal of neuroscience.

[23]  A. David,et al.  The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance , 1999, Brain Research Reviews.

[24]  G. Ehret,et al.  The auditory cortex of the house mouse: left-right differences, tonotopic organization and quantitative analysis of frequency representation , 1997, Journal of Comparative Physiology A.

[25]  Inferior colliculus of the house mouse , 1985 .

[26]  E. Friauf Tonotopic Order in the Adult and Developing Auditory System of the Rat as Shown by c‐fos Immunocytochemistry , 1992, The European journal of neuroscience.

[27]  G. Ehret,et al.  Frequency response areas of neurons in the mouse inferior colliculus. I. Threshold and tuning characteristics , 2001, Experimental Brain Research.

[28]  G. Ehret,et al.  Low-frequency sound communication by mouse pups (Mus musculus): wriggling calls release maternal behaviour , 1986, Animal Behaviour.

[29]  E. T. Possing,et al.  Human temporal lobe activation by speech and nonspeech sounds. , 2000, Cerebral cortex.

[30]  Alan C. Evans,et al.  Lateralization of phonetic and pitch discrimination in speech processing. , 1992, Science.

[31]  William C. Stebbins,et al.  Neural lateralization of vocalizations by Japanese macaques: communicative significance is more important than acoustic structure. , 1984, Behavioral neuroscience.

[32]  R. Reale,et al.  Tonotopic organization in auditory cortex of the cat , 1980, The Journal of comparative neurology.

[33]  J. T. Erichsen,et al.  Fos Imaging Reveals Differential Patterns of Hippocampal and Parahippocampal Subfield Activation in Rats in Response to Different Spatial Memory Tests , 2000, The Journal of Neuroscience.

[34]  J A Wada,et al.  Cerebral hemispheric asymmetry in humans. Cortical speech zones in 100 adults and 100 infant brains. , 1975, Archives of neurology.

[35]  A. Chaudhuri,et al.  Neural activity mapping with inducible transcription factors. , 1997, Neuroreport.

[36]  H. Scheich,et al.  Mapping of stimulus features and meaning in gerbil auditory cortex with 2-deoxyglucose and c-Fos antibodies , 1995, Behavioural Brain Research.

[37]  B. Slotnick Stereotaxic surgical techniques for the mouse. , 1972, Physiology & behavior.

[38]  I. Fichtel,et al.  Perception and recognition discriminated in the mouse auditory cortex by c-Fos labeling. , 1999, Neuroreport.

[39]  C S Watson,et al.  Auditory psychophysics and perception. , 1996, Annual review of psychology.

[40]  G. Ehret,et al.  Categorical perception of mouse-pup ultrasounds in the temporal domain , 1992, Animal Behaviour.

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

[42]  G. Rebec,et al.  A simple device for the reliable production of varnish-insulated, high-impedance tungsten microelectrodes , 1989, Journal of Neuroscience Methods.

[43]  T. Curran,et al.  Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. , 1991, Annual review of neuroscience.

[44]  T. Hashikawa,et al.  Temporal Integration and Duration Tuning in the Dorsal Zone of Cat Auditory Cortex , 1997, The Journal of Neuroscience.

[45]  O D Creutzfeldt,et al.  Functional subdivisions in the auditory cortex of the guinea pig , 1989, The Journal of comparative neurology.

[46]  Israel Nelken,et al.  Feature Detection by the Auditory Cortex , 2002 .

[47]  Günter Ehret,et al.  Mice and humans perceive multiharmonic communication sounds in the same way , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[48]  C. Carr,et al.  Comparative Psychology of Audition , 2003 .

[49]  P. Marler,et al.  Neural lateralization of vocalizations by Japanese macaques: communicative significance is more important than acoustic structure. , 1984, Behavioral Neuroscience.

[50]  P F Liddle,et al.  The role of the left prefrontal cortex in verbal processing: semantic processing or willed action? , 1994, Neuroreport.

[51]  T. Curran,et al.  Expression of c-fos protein in brain: metabolic mapping at the cellular level. , 1988, Science.

[52]  Günter Ehret,et al.  Schallsignale Der Hausmaus (Mus Musculus) , 1974 .

[53]  Alan R. Palmer,et al.  Identification and localisation of auditory areas in guinea pig cortex , 2000, Experimental Brain Research.

[54]  V. Caviness Architectonic map of neocortex of the normal mouse , 1975, The Journal of comparative neurology.

[55]  Christoph E. Schreiner,et al.  Spatial Distribution of Responses to Simple and Complex Sounds in the Primary Auditory Cortex , 1998, Audiology and Neurotology.

[56]  M. Mishkin,et al.  Functional Mapping of the Primate Auditory System , 2003, Science.

[57]  D. Moody,et al.  Perception of conspecific vocalizations by Japanese macaques. Evidence for selective attention and neural lateralization. , 1979, Brain, behavior and evolution.

[58]  N. Suga,et al.  Specificity of combination-sensitive neurons for processing of complex biosonar signals in auditory cortex of the mustached bat. , 1983, Journal of neurophysiology.

[59]  Stephen M. Rao,et al.  Human Brain Language Areas Identified by Functional Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

[60]  G. Ehret,et al.  The auditory cortex of the mouse: Connections of the ultrasonic field , 1992, The Journal of comparative neurology.

[61]  Günter Ehret,et al.  Time-critical integration of formants for perception of communication calls in mice , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[63]  A. Braun,et al.  Asymmetry of chimpanzee planum temporale: humanlike pattern of Wernicke's brain language area homolog. , 1998, Science.

[64]  D. Molfese,et al.  Hemisphere and Stimulus Differences as Reflected in the Cortical Responses of Newborn Infants to Speech Stimuli. , 1979 .

[65]  Daniel S. Barth,et al.  Polysensory evoked potentials in rat parietotemporal cortex: combined auditory and somatosensory responses , 1994, Brain Research.

[66]  G. Ehret,et al.  Neuronal activity and tonotopy in the auditory system visualized by c-fos gene expression , 1991, Brain Research.