Representations of specific acoustic patterns in the auditory cortex and hippocampus

Previous behavioural studies have shown that repeated presentation of a randomly chosen acoustic pattern leads to the unsupervised learning of some of its specific acoustic features. The objective of our study was to determine the neural substrate for the representation of freshly learnt acoustic patterns. Subjects first performed a behavioural task that resulted in the incidental learning of three different noise-like acoustic patterns. During subsequent high-resolution functional magnetic resonance imaging scanning, subjects were then exposed again to these three learnt patterns and to others that had not been learned. Multi-voxel pattern analysis was used to test if the learnt acoustic patterns could be ‘decoded’ from the patterns of activity in the auditory cortex and medial temporal lobe. We found that activity in planum temporale and the hippocampus reliably distinguished between the learnt acoustic patterns. Our results demonstrate that these structures are involved in the neural representation of specific acoustic patterns after they have been learnt.

[1]  Timothy D. Griffiths,et al.  A unified framework for the organization of the primate auditory cortex , 2013, Front. Syst. Neurosci..

[2]  Brian C J Moore,et al.  Navigating the Auditory Scene: An Expert Role for the Hippocampus , 2012, The Journal of Neuroscience.

[3]  Katharina von Kriegstein,et al.  Encoding of Spectral Correlation over Time in Auditory Cortex , 2008, The Journal of Neuroscience.

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

[5]  Richard W. Hamming,et al.  Error detecting and error correcting codes , 1950 .

[6]  Trevor R. Agus,et al.  Perceptual learning of acoustic noise by individuals with dyslexia. , 2014, Journal of speech, language, and hearing research : JSLHR.

[7]  Alan C. Evans,et al.  Quantifying variability in the planum temporale: a probability map. , 1999, Cerebral cortex.

[8]  Robert T. Knight,et al.  Superior Temporal SulcusIt's My Area: Or Is It? , 2008, Journal of Cognitive Neuroscience.

[9]  E. DeYoe,et al.  Distinct Cortical Pathways for Processing Tool versus Animal Sounds , 2005, The Journal of Neuroscience.

[10]  K Zilles,et al.  Cerebral asymmetry: MR planimetry of the human planum temporale. , 1989, Journal of computer assisted tomography.

[11]  Nikolaus Weiskopf,et al.  Detecting Representations of Recent and Remote Autobiographical Memories in vmPFC and Hippocampus , 2012, The Journal of Neuroscience.

[12]  M. Sharda,et al.  Auditory perception of natural sound categories – An fMRI study , 2012, Neuroscience.

[13]  Karl J. Friston,et al.  Segregating the functions of human hippocampus. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Trevor R. Agus,et al.  The detection of repetitions in noise before and after perceptual learning. , 2013, The Journal of the Acoustical Society of America.

[15]  D. Hassabis,et al.  Decoding Individual Episodic Memory Traces in the Human Hippocampus , 2010, Current Biology.

[16]  Robert J. Zatorre,et al.  A role for the right superior temporal sulcus in categorical perception of musical chords , 2011, Neuropsychologia.

[17]  Chih-Jen Lin,et al.  LIBSVM: A library for support vector machines , 2011, TIST.

[18]  Alan C. Evans,et al.  Interhemispheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. , 1996, Cerebral cortex.

[19]  Yoram Singer,et al.  Reducing Multiclass to Binary: A Unifying Approach for Margin Classifiers , 2000, J. Mach. Learn. Res..

[20]  Josh H McDermott,et al.  Recovering sound sources from embedded repetition , 2011, Proceedings of the National Academy of Sciences.

[21]  E. Musser,et al.  The neural correlates of maternal sensitivity: An fMRI study , 2012, Developmental Cognitive Neuroscience.

[22]  N. Weinberger Auditory associative memory and representational plasticity in the primary auditory cortex , 2007, Hearing Research.

[23]  Eleanor A. Maguire,et al.  Decoding information in the human hippocampus: A user's guide , 2012, Neuropsychologia.

[24]  N. Weinberger Specific long-term memory traces in primary auditory cortex , 2004, Nature Reviews Neuroscience.

[25]  Thomas G. Dietterich,et al.  Solving Multiclass Learning Problems via Error-Correcting Output Codes , 1994, J. Artif. Intell. Res..

[26]  H. Duvernoy,et al.  The Human Hippocampus: Functional Anatomy, Vascularization and Serial Sections with MRI , 1997 .

[27]  Daniel Pressnitzer,et al.  Rapid Formation of Robust Auditory Memories: Insights from Noise , 2010, Neuron.

[28]  Isabelle Guyon,et al.  An Introduction to Variable and Feature Selection , 2003, J. Mach. Learn. Res..

[29]  D. Hassabis,et al.  Decoding Neuronal Ensembles in the Human Hippocampus , 2009, Current Biology.

[30]  A. R. Jennings,et al.  Analysis of the spectral envelope of sounds by the human brain , 2005, NeuroImage.

[31]  S. Köhler,et al.  Why is the meaning of a sentence better remembered than its form? An fMRI study on the role of novelty‐encoding processes , 2008, Hippocampus.

[32]  Karl J. Friston,et al.  Hierarchical Processing of Auditory Objects in Humans , 2007, PLoS Comput. Biol..

[33]  Rhodri Cusack,et al.  Cortical Mechanisms for the Segregation and Representation of Acoustic Textures , 2010, The Journal of Neuroscience.

[34]  D. Poeppel,et al.  Neural Response Phase Tracks How Listeners Learn New Acoustic Representations , 2013, Current Biology.

[35]  David A. Medler,et al.  Cerebral Cortex doi:10.1093/cercor/bhi040 Cerebral Cortex Advance Access published February 9, 2005 , 2022 .

[36]  H. Soininen,et al.  MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. , 1998, AJNR. American journal of neuroradiology.

[37]  D. Amaral,et al.  Evidence for a direct projection from the superior temporal gyrus to the entorhinal cortex in the monkey , 1983, Brain Research.

[38]  Jeffrey R Binder,et al.  Human brain regions involved in recognizing environmental sounds. , 2004, Cerebral cortex.

[39]  H. Steinmetz,et al.  Structure, Function and Cerebral Asymmetry: In Vivo Morphometry of the Planum Temporale , 1996, Neuroscience & Biobehavioral Reviews.

[40]  Roy D. Patterson,et al.  Neural Representation of Auditory Size in the Human Voice and in Sounds from Other Resonant Sources , 2007, Current Biology.

[41]  T. Teyler,et al.  Induction of LTP in the human auditory cortex by sensory stimulation , 2005, The European journal of neuroscience.

[42]  Jean-Francois Mangin,et al.  Sulcal pattern and morphology of the superior temporal sulcus , 2004, NeuroImage.

[43]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Guido Gerig,et al.  User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability , 2006, NeuroImage.

[45]  S. Rosen,et al.  British Society of Audiology Short Papers Meeting on Experimental Studies of Hearing and Deafness , 2002, British journal of audiology.

[46]  Robert J Zatorre,et al.  Representations of Invariant Musical Categories Are Decodable by Pattern Analysis of Locally Distributed BOLD Responses in Superior Temporal and Intraparietal Sulci. , 2015, Cerebral cortex.

[47]  Pierre Fonlupt,et al.  Listening to a walking human activates the temporal biological motion area , 2005, NeuroImage.