Spatial organization of the mouse auditory cortex to sound dynamics revealed using automated image segmentation

Sound stimuli are characterized by their rich spectral and temporal dynamic properties. Individual neurons in auditory cortex (ACX) encode both spectral and temporal aspects of sounds e.g. sound onset and/or offset. While the different fields of the ACX show gradients of frequency selectivity the large-scale organization of sound dynamics is unknown. We used widefield imaging of GCaMP6s in awake mouse ACX combined with a novel unsupervised image segmentation technique to investigate the spatiotemporal representation of sound onset and offset. Using this technique, we identified known auditory fields but also detected novel ACX areas. Furthermore, we found that ACX areas differed in their responses to tone onset and offset. Multiple areas were preferentially activated by tone offset, and on-response areas were more spatially localized than off-response areas. We also found tonotopy in off-responses. Together our results demonstrate a different spatial distribution of neurons across ACX for processing sound onsets versus offsets.

[1]  Jufang He,et al.  ON and OFF Pathways Segregated at the Auditory Thalamus of the Guinea Pig , 2001, The Journal of Neuroscience.

[2]  H. Read,et al.  Multiparametric auditory receptive field organization across five cortical fields in the albino rat. , 2007, Journal of neurophysiology.

[3]  Brenda C. Shields,et al.  Thy1-GCaMP6 Transgenic Mice for Neuronal Population Imaging In Vivo , 2014, PloS one.

[4]  Kuniyuki Takahashi,et al.  Delineation of a frequency-organized region isolated from the mouse primary auditory cortex , 2015, Journal of neurophysiology.

[5]  Ling Qin,et al.  Comparison between offset and onset responses of primary auditory cortex ON-OFF neurons in awake cats. , 2007, Journal of neurophysiology.

[6]  Richard J. Salvi,et al.  Genetic background effects on age-related hearing loss associated with Cdh23 variants in mice , 2012, Hearing Research.

[7]  B. Godde,et al.  A Map of Periodicity Orthogonal to Frequency Representation in the Cat Auditory Cortex , 2009, Frontiers in integrative neuroscience.

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

[9]  C. Schreiner,et al.  Periodicity coding in the inferior colliculus of the cat. II. Topographical organization. , 1988, Journal of neurophysiology.

[10]  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.

[11]  Shihab A. Shamma,et al.  Dichotomy of functional organization in the mouse auditory cortex , 2010, Nature Neuroscience.

[12]  Daniel E. Winkowski,et al.  Laminar Transformation of Frequency Organization in Auditory Cortex , 2013, The Journal of Neuroscience.

[13]  H. Redies,et al.  Functional organization of the auditory thalamus in the guinea pig , 2004, Experimental Brain Research.

[14]  C. Schreiner,et al.  Representation of amplitude modulation in the auditory cortex of the cat. I. The anterior auditory field (AAF) , 1986, Hearing Research.

[15]  J. Winer,et al.  Auditory thalamocortical projections in the cat: Laminar and areal patterns of input , 2000, The Journal of comparative neurology.

[16]  Israel Nelken,et al.  Local versus global scales of organization in auditory cortex , 2014, Trends in Neurosciences.

[17]  B. Haeffele,et al.  Multiscale Optical Ca2+ Imaging of Tonal Organization in Mouse Auditory Cortex , 2014, Neuron.

[18]  S. Sherman,et al.  Evidence for nonreciprocal organization of the mouse auditory thalamocortical‐corticothalamic projection systems , 2008, The Journal of comparative neurology.

[19]  Pascal Vincent,et al.  Representation Learning: A Review and New Perspectives , 2012, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[20]  Mark W. Schmidt,et al.  Optimizing Costly Functions with Simple Constraints: A Limited-Memory Projected Quasi-Newton Algorithm , 2009, AISTATS.

[21]  Mitchell Steinschneider,et al.  Temporally dynamic frequency tuning of population responses in monkey primary auditory cortex , 2009, Hearing Research.

[22]  Matthew R Whiteway,et al.  Revealing unobserved factors underlying cortical activity using a rectified latent variable model applied to neural population recordings , 2016, bioRxiv.

[23]  T. Hromádka,et al.  Sparse Representation of Sounds in the Unanesthetized Auditory Cortex , 2008, PLoS biology.

[24]  T W Picton,et al.  ON and OFF components in the auditory evoked potential , 1978, Perception & psychophysics.

[25]  G. Langner,et al.  Temporal and spatial coding of periodicity information in the inferior colliculus of awake chinchilla (Chinchilla laniger) , 2002, Hearing Research.

[26]  M M Merzenich,et al.  Representation of cochlea within primary auditory cortex in the cat. , 1975, Journal of neurophysiology.

[27]  D. Irvine,et al.  Sensitivity of neurons in cat primary auditory cortex to tones and frequency-modulated stimuli. I: Effects of variation of stimulus parameters , 1992, Hearing Research.

[28]  M. Wehr,et al.  Nonoverlapping Sets of Synapses Drive On Responses and Off Responses in Auditory Cortex , 2010, Neuron.

[29]  T. Imig,et al.  Organization of the thalamocortical auditory system in the cat. , 1983, Annual review of neuroscience.

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

[31]  S. Sherman,et al.  Synaptic properties of thalamic and intracortical inputs to layer 4 of the first- and higher-order cortical areas in the auditory and somatosensory systems. , 2008, Journal of neurophysiology.

[32]  Kuniyuki Takahashi,et al.  Auditory cortical field coding long-lasting tonal offsets in mice , 2016, Scientific Reports.

[33]  G. Recanzone Response profiles of auditory cortical neurons to tones and noise in behaving macaque monkeys , 2000, Hearing Research.

[34]  T. Hackett,et al.  Linking Topography to Tonotopy in the Mouse Auditory Thalamocortical Circuit , 2011, The Journal of Neuroscience.

[35]  Günter Ehret,et al.  Mapping responses to frequency sweeps and tones in the inferior colliculus of house mice , 2003, The European journal of neuroscience.

[36]  Susan Brown,et al.  THE GUINEA PIG , 2003 .

[37]  Benjamin D. Haeffele,et al.  Multiscale mapping of frequency sweep rate in mouse auditory cortex , 2017, Hearing Research.

[38]  Simone Kurt,et al.  Quantitative analysis of neuronal response properties in primary and higher-order auditory cortical fields of awake house mice (Mus musculus) , 2014, The European journal of neuroscience.

[39]  Robert D. Frisina,et al.  F1 (CBA×C57) mice show superior hearing in old age relative to their parental strains: Hybrid vigor or a new animal model for “Golden Ears”? , 2011, Neurobiology of Aging.

[40]  Anna R. Chambers,et al.  Robustness of Cortical Topography across Fields, Laminae, Anesthetic States, and Neurophysiological Signal Types , 2012, The Journal of Neuroscience.

[41]  W. R. Webster,et al.  Medial geniculate body of the cat: organization and responses to tonal stimuli of neurons in ventral division. , 1972, Journal of neurophysiology.

[42]  Jeffery A Winer,et al.  Connections of cat auditory cortex: I. Thalamocortical system , 2008, The Journal of comparative neurology.

[43]  Gerald Langner,et al.  Ontogenic development of periodicity coding in the inferior colliculus of the mongolian gerbil , 1995 .

[44]  Matthias H Hennig,et al.  The Sound of Silence: Ionic Mechanisms Encoding Sound Termination , 2011, Neuron.

[45]  I. Nelken,et al.  Functional organization and population dynamics in the mouse primary auditory cortex , 2010, Nature Neuroscience.

[46]  Kenneth R. Henry,et al.  Tuning of the auditory brainstem OFF responses is complementary to tuning of the auditory brainstem ON response , 1985, Hearing Research.

[47]  Ian Nauhaus,et al.  Automated identification of mouse visual areas with intrinsic signal imaging , 2016, Nature Protocols.