Differential Coding of Conspecific Vocalizations in the Ventral Auditory Cortical Stream

The mammalian auditory cortex integrates spectral and temporal acoustic features to support the perception of complex sounds, including conspecific vocalizations. Here we investigate coding of vocal stimuli in different subfields in macaque auditory cortex. We simultaneously measured auditory evoked potentials over a large swath of primary and higher order auditory cortex along the supratemporal plane in three animals chronically using high-density microelectrocorticographic arrays. To evaluate the capacity of neural activity to discriminate individual stimuli in these high-dimensional datasets, we applied a regularized multivariate classifier to evoked potentials to conspecific vocalizations. We found a gradual decrease in the level of overall classification performance along the caudal to rostral axis. Furthermore, the performance in the caudal sectors was similar across individual stimuli, whereas the performance in the rostral sectors significantly differed for different stimuli. Moreover, the information about vocalizations in the caudal sectors was similar to the information about synthetic stimuli that contained only the spectral or temporal features of the original vocalizations. In the rostral sectors, however, the classification for vocalizations was significantly better than that for the synthetic stimuli, suggesting that conjoined spectral and temporal features were necessary to explain differential coding of vocalizations in the rostral areas. We also found that this coding in the rostral sector was carried primarily in the theta frequency band of the response. These findings illustrate a progression in neural coding of conspecific vocalizations along the ventral auditory pathway.

[1]  S. Garrod,et al.  Brain-to-brain coupling: a mechanism for creating and sharing a social world , 2012, Trends in Cognitive Sciences.

[2]  Yale E Cohen,et al.  Acoustic features of rhesus vocalizations and their representation in the ventrolateral prefrontal cortex. , 2007, Journal of neurophysiology.

[3]  D. Rendall,et al.  Vocal recognition of individuals and kin in free-ranging rhesus monkeys , 1996, Animal Behaviour.

[4]  T. Womelsdorf,et al.  Attentional Stimulus Selection through Selective Synchronization between Monkey Visual Areas , 2012, Neuron.

[5]  D B Moody,et al.  Categorical perception of conspecific communication sounds by Japanese macaques, Macaca fuscata. , 1989, The Journal of the Acoustical Society of America.

[6]  Asif A Ghazanfar,et al.  The auditory behaviour of primates: a neuroethological perspective , 2001, Current Opinion in Neurobiology.

[7]  N. Logothetis,et al.  Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. , 2003, Cerebral cortex.

[8]  Christoph Kayser,et al.  Voice Cells in the Primate Temporal Lobe , 2011, Current Biology.

[9]  P. Marler,et al.  Food-associated calls in rhesus macaques (Macaca mulatta): I. Socioecological factors , 1993 .

[10]  N. Logothetis,et al.  A voice region in the monkey brain , 2008, Nature Neuroscience.

[11]  Stefano Panzeri,et al.  Analysis of Slow (Theta) Oscillations as a Potential Temporal Reference Frame for Information Coding in Sensory Cortices , 2012, PLoS Comput. Biol..

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

[13]  Ning Liu,et al.  Dynamic and Static Facial Expressions Decoded from Motion-Sensitive Areas in the Macaque Monkey , 2012, The Journal of Neuroscience.

[14]  Peter Brown,et al.  Effects of dopamine depletion on information flow between the subthalamic nucleus and external globus pallidus. , 2011, Journal of neurophysiology.

[15]  J. Bullier,et al.  Cortical mapping of gamma oscillations in areas V1 and V4 of the macaque monkey , 2001, Visual Neuroscience.

[16]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[17]  Masa-aki Sato,et al.  Visual Image Reconstruction from Human Brain Activity using a Combination of Multiscale Local Image Decoders , 2008, Neuron.

[18]  M. Berger,et al.  High gamma activity in response to deviant auditory stimuli recorded directly from human cortex. , 2005, Journal of neurophysiology.

[19]  Roy D. Patterson,et al.  Vocal-Tract Resonances as Indexical Cues in Rhesus Monkeys , 2007, Current Biology.

[20]  C. Goutis,et al.  Estimation in linear models using gradient descent with early stopping , 1994 .

[21]  Dwight J. Kravitz,et al.  The ventral visual pathway: an expanded neural framework for the processing of object quality , 2013, Trends in Cognitive Sciences.

[22]  Nicolas Brunel,et al.  Sensory neural codes using multiplexed temporal scales , 2010, Trends in Neurosciences.

[23]  Brian H Scott,et al.  Transformation of temporal processing across auditory cortex of awake macaques. , 2011, Journal of neurophysiology.

[24]  M J Owren,et al.  The role of vocal tract filtering in identity cueing in rhesus monkey (Macaca mulatta) vocalizations. , 1998, The Journal of the Acoustical Society of America.

[25]  Brian N. Pasley,et al.  Reconstructing Speech from Human Auditory Cortex , 2012, PLoS biology.

[26]  Barry J. Richmond,et al.  Decoding cortical neuronal signals: Network models, information estimation and spatial tuning , 1994, Journal of Computational Neuroscience.

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

[28]  N. C. Singh,et al.  Modulation spectra of natural sounds and ethological theories of auditory processing. , 2003, The Journal of the Acoustical Society of America.

[29]  Christoph Kayser,et al.  Monkeys are perceptually tuned to facial expressions that exhibit a theta-like speech rhythm , 2013, Proceedings of the National Academy of Sciences.

[30]  M. Mishkin,et al.  Species-specific calls evoke asymmetric activity in the monkey's temporal poles , 2004, Nature.

[31]  M. Mishkin,et al.  Spontaneous High-Gamma Band Activity Reflects Functional Organization of Auditory Cortex in the Awake Macaque , 2012, Neuron.

[32]  C. Petkov,et al.  Birds, primates, and spoken language origins: behavioral phenotypes and neurobiological substrates , 2012, Front. Evol. Neurosci..

[33]  B. Averbeck,et al.  The primate cortical auditory system and neural representation of conspecific vocalizations. , 2009, Annual review of neuroscience.

[34]  M M Merzenich,et al.  Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. , 1995, Journal of neurophysiology.

[35]  D. Bendor,et al.  The neuronal representation of pitch in primate auditory cortex , 2005, Nature.

[36]  I. Gauthier,et al.  Expertise for cars and birds recruits brain areas involved in face recognition , 2000, Nature Neuroscience.

[37]  M. Tarr,et al.  Activation of the middle fusiform 'face area' increases with expertise in recognizing novel objects , 1999, Nature Neuroscience.

[38]  Takafumi Suzuki,et al.  Simultaneous recording of ECoG and intracortical neuronal activity using a flexible multichannel electrode-mesh in visual cortex , 2011, NeuroImage.

[39]  P. Kuhl,et al.  Birdsong and human speech: common themes and mechanisms. , 1999, Annual review of neuroscience.

[40]  Bruno B Averbeck,et al.  Probabilistic Encoding of Vocalizations in Macaque Ventral Lateral Prefrontal Cortex , 2006, The Journal of Neuroscience.

[41]  Daniel Bendor,et al.  Differential neural coding of acoustic flutter within primate auditory cortex , 2007, Nature Neuroscience.

[42]  Lori L. Holt,et al.  Expertise with Artificial Nonspeech Sounds Recruits Speech-Sensitive Cortical Regions , 2009, The Journal of Neuroscience.

[43]  Josh H. McDermott,et al.  Cortical Pitch Regions in Humans Respond Primarily to Resolved Harmonics and Are Located in Specific Tonotopic Regions of Anterior Auditory Cortex , 2013, The Journal of Neuroscience.

[44]  Bruno B Averbeck,et al.  Principal and independent components of macaque vocalizations: constructing stimuli to probe high-level sensory processing. , 2004, Journal of neurophysiology.

[45]  Bradley Greger,et al.  Decoding spoken words using local field potentials recorded from the cortical surface , 2010, Journal of neural engineering.

[46]  T. Hackett Information flow in the auditory cortical network , 2011, Hearing Research.

[47]  A. King,et al.  Unraveling the principles of auditory cortical processing: can we learn from the visual system? , 2009, Nature Neuroscience.

[48]  Daniel Bendor,et al.  Neural coding of periodicity in marmoset auditory cortex. , 2010, Journal of neurophysiology.

[49]  J. Gallant,et al.  Identifying natural images from human brain activity , 2008, Nature.

[50]  Ryan J. Prenger,et al.  Bayesian Reconstruction of Natural Images from Human Brain Activity , 2009, Neuron.

[51]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[52]  Yukiko Kikuchi,et al.  Hierarchical Auditory Processing Directed Rostrally along the Monkey's Supratemporal Plane , 2010, The Journal of Neuroscience.

[53]  D. Bendor,et al.  Neural response properties of primary, rostral, and rostrotemporal core fields in the auditory cortex of marmoset monkeys. , 2008, Journal of neurophysiology.