Prefrontal Activity Predicts Monkeys' Decisions During an Auditory Category Task

The neural correlates that relate auditory categorization to aspects of goal-directed behavior, such as decision-making, are not well understood. Since the prefrontal cortex (PFC) plays an important role in executive function and the categorization of auditory objects, we hypothesized that neural activity in the PFC should predict an animal's behavioral reports (decisions) during a category task. To test this hypothesis, we tested PFC activity that was recorded while monkeys categorized human spoken words (Russ et al., 2008b). We found that activity in the ventrolateral PFC, on average, correlated best with the monkeys' choices than with the auditory stimuli. This finding demonstrates a direct link between PFC activity and behavioral choices during a non-spatial auditory task.

[1]  Risto N t nen Attention and brain function , 1992 .

[2]  Yale E Cohen,et al.  Selectivity for the Spatial and Nonspatial Attributes of Auditory Stimuli in the Ventrolateral Prefrontal Cortex , 2004, The Journal of Neuroscience.

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

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

[5]  Marc D. Hauser,et al.  The Neurophysiology of Functionally Meaningful Categories: Macaque Ventrolateral Prefrontal Cortex Plays a Critical Role in Spontaneous Categorization of Species-Specific Vocalizations , 2005, Journal of Cognitive Neuroscience.

[6]  P. D. Eimas,et al.  Speech Perception in Infants , 1971, Science.

[7]  Stuart Rosen,et al.  A positron emission tomography study of the neural basis of informational and energetic masking effects in speech perception. , 2004, The Journal of the Acoustical Society of America.

[8]  P K Kuhl,et al.  Enhanced discriminability at the phonetic boundaries for the voicing feature in macaques , 1982, Perception & psychophysics.

[9]  Tsuhan Chen,et al.  Audio Feature Extraction and Analysis for Scene Segmentation and Classification , 1998, J. VLSI Signal Process..

[10]  C. Schroeder,et al.  Physiologic Correlates of the Voice Onset Time Boundary in Primary Auditory Cortex (A1) of the Awake Monkey: Temporal Response Patterns , 1995, Brain and Language.

[11]  R J Wise,et al.  Separate neural subsystems within 'Wernicke's area'. , 2001, Brain : a journal of neurology.

[12]  W. T. Illingworth,et al.  Practical guide to neural nets , 1991 .

[13]  Yoshua Bengio,et al.  Gradient-based learning applied to document recognition , 1998, Proc. IEEE.

[14]  J D Miller,et al.  Speech perception by the chinchilla: identification function for synthetic VOT stimuli. , 1978, The Journal of the Acoustical Society of America.

[15]  Micah M. Murray,et al.  Rapid Brain Discrimination of Sounds of Objects , 2006, The Journal of Neuroscience.

[16]  M Steinschneider,et al.  Consonance and dissonance of musical chords: neural correlates in auditory cortex of monkeys and humans. , 2001, Journal of neurophysiology.

[17]  Elyse S Sussman,et al.  Integration and segregation in auditory scene analysis. , 2005, The Journal of the Acoustical Society of America.

[18]  Anders Krogh,et al.  Introduction to the theory of neural computation , 1994, The advanced book program.

[19]  Federico Turkheimer,et al.  Speech production after stroke: The role of the right pars opercularis , 2003, Annals of neurology.

[20]  Kevin Murphy,et al.  Speech production: Wernicke, Broca and beyond. , 2002, Brain : a journal of neurology.

[21]  Y. Gutfreund,et al.  Stimulus-Specific Adaptations in the Gaze Control System of the Barn Owl , 2008, The Journal of Neuroscience.

[22]  J. Rauschecker Cortical processing of complex sounds , 1998, Current Opinion in Neurobiology.

[23]  Alexander Grunewald,et al.  Neural Correlates of Structure-from-Motion Perception in Macaque V1 and MT , 2002, The Journal of Neuroscience.

[24]  M. Turk,et al.  Eigenfaces for Recognition , 1991, Journal of Cognitive Neuroscience.

[25]  N. Logothetis,et al.  Category-Specific Responses to Faces and Objects in Primate Auditory Cortex , 2007, Frontiers in systems neuroscience.

[26]  R. Diehl,et al.  Speech Perception , 2004, Annual review of psychology.

[27]  P. Goldman-Rakic,et al.  Auditory belt and parabelt projections to the prefrontal cortex in the Rhesus monkey , 1999, The Journal of comparative neurology.

[28]  David J. Freedman,et al.  The prefrontal cortex: categories, concepts and cognition. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[29]  J. Rauschecker,et al.  Perceptual Organization of Tone Sequences in the Auditory Cortex of Awake Macaques , 2005, Neuron.

[30]  Rich Caruana,et al.  Overfitting in Neural Nets: Backpropagation, Conjugate Gradient, and Early Stopping , 2000, NIPS.

[31]  R. Zatorre,et al.  Sensitivity to Auditory Object Features in Human Temporal Neocortex , 2004, The Journal of Neuroscience.

[32]  D. G. Albrecht,et al.  Visual cortex neurons in monkeys and cats: Detection, discrimination, and identification , 1997, Visual Neuroscience.

[33]  M Steinschneider,et al.  Complex tone processing in primary auditory cortex of the awake monkey. I. Neural ensemble correlates of roughness. , 2000, The Journal of the Acoustical Society of America.

[34]  Sophie K Scott,et al.  Auditory processing — speech, space and auditory objects , 2005, Current Opinion in Neurobiology.

[35]  S. Sternberg,et al.  Separate modifiability, mental modules, and the use of pure and composite measures to reveal them. , 2001, Acta psychologica.

[36]  W. Freeman,et al.  Change in pattern of ongoing cortical activity with auditory category learning , 2001, Nature.

[37]  J. Gold,et al.  The neural basis of decision making. , 2007, Annual review of neuroscience.

[38]  Frank Rosenblatt,et al.  PRINCIPLES OF NEURODYNAMICS. PERCEPTRONS AND THE THEORY OF BRAIN MECHANISMS , 1963 .

[39]  J. D. Miller,et al.  Speech perception by the chinchilla: voiced-voiceless distinction in alveolar plosive consonants , 1975, Science.

[40]  Heekuck Oh,et al.  Neural Networks for Pattern Recognition , 1993, Adv. Comput..

[41]  C. Darwin Auditory grouping , 1997, Trends in Cognitive Sciences.

[42]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  Xiaoqin Wang,et al.  Sustained firing in auditory cortex evoked by preferred stimuli , 2005, Nature.

[44]  A. Braun,et al.  Auditory lexical decision, categorical perception, and FM direction discrimination differentially engage left and right auditory cortex , 2004, Neuropsychologia.

[45]  H. Scheich,et al.  Dual Time Scales for Categorical Decision Making in Auditory Cortex , 2006, Current Biology.

[46]  I. Nelken,et al.  Processing of low-probability sounds by cortical neurons , 2003, Nature Neuroscience.

[47]  R. Andersen,et al.  Intention-related activity in the posterior parietal cortex: a review , 2000, Vision Research.

[48]  L. B. Lmeida Backpropagation in perceptrons with feedback , 1988 .

[49]  L. B. Almeida,et al.  BACKPROPAGATION IN PERCEPTRONS WITH FEEDBACK , 2022 .

[50]  M Steinschneider,et al.  Complex tone processing in primary auditory cortex of the awake monkey. II. Pitch versus critical band representation. , 2000, The Journal of the Acoustical Society of America.

[51]  Nello Cristianini,et al.  An Introduction to Support Vector Machines and Other Kernel-based Learning Methods , 2000 .

[52]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[53]  Sophie K. Scott,et al.  The functional neuroanatomy of prelexical processing in speech perception , 2004, Cognition.

[54]  Y. Cohen,et al.  Neural and behavioral correlates of auditory categorization , 2007, Hearing Research.

[55]  Bernard Widrow,et al.  30 years of adaptive neural networks: perceptron, Madaline, and backpropagation , 1990, Proc. IEEE.

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

[57]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

[58]  R. Shepard,et al.  Toward a universal law of generalization for psychological science. , 1987, Science.

[59]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

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

[61]  K. Spence The differential response in animals to stimuli varying within a single dimension. , 1937 .

[62]  Yale E Cohen,et al.  Spontaneous processing of abstract categorical information in the ventrolateral prefrontal cortex , 2006, Biology Letters.

[63]  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.

[64]  P. Kuhl,et al.  Enhanced discriminability at the phonetic boundaries for the place feature in macaques. , 1983, The Journal of the Acoustical Society of America.

[65]  Karl J. Friston,et al.  Brain Mechanisms for Detecting Perceptual, Semantic, and Emotional Deviance , 2000, NeuroImage.

[66]  David J. Freedman,et al.  Visual categorization and the primate prefrontal cortex: neurophysiology and behavior. , 2002, Journal of neurophysiology.

[67]  Alon Fishbach,et al.  Primary auditory cortex of cats: feature detection or something else? , 2003, Biological Cybernetics.

[68]  S. Scott,et al.  Identification of a pathway for intelligible speech in the left temporal lobe. , 2000, Brain : a journal of neurology.

[69]  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.

[70]  Anil K. Jain,et al.  Feature Selection: Evaluation, Application, and Small Sample Performance , 1997, IEEE Trans. Pattern Anal. Mach. Intell..

[71]  Hideki Kawahara,et al.  Restructuring speech representations using a pitch-adaptive time-frequency smoothing and an instantaneous-frequency-based F0 extraction: Possible role of a repetitive structure in sounds , 1999, Speech Commun..

[72]  Satrajit S. Ghosh,et al.  Representation of sound categories in auditory cortical maps. , 2004, Journal of speech, language, and hearing research : JSLHR.

[73]  Pineda,et al.  Generalization of back-propagation to recurrent neural networks. , 1987, Physical review letters.

[74]  Stephanie Clarke,et al.  Automatic and intrinsic auditory "what" and "where" processing in humans revealed by electrical neuroimaging. , 2006, Cerebral cortex.

[75]  Roberto Battiti,et al.  Using mutual information for selecting features in supervised neural net learning , 1994, IEEE Trans. Neural Networks.

[76]  Xiaoqin Wang,et al.  Differential representation of species-specific primate vocalizations in the auditory cortices of marmoset and cat. , 2001, Journal of neurophysiology.

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

[78]  Brian E. Russ,et al.  Prefrontal Neurons Predict Choices during an Auditory Same-Different Task , 2008, Current Biology.

[79]  George Cybenko,et al.  Approximation by superpositions of a sigmoidal function , 1989, Math. Control. Signals Syst..

[80]  David J. Freedman,et al.  A Comparison of Primate Prefrontal and Inferior Temporal Cortices during Visual Categorization , 2003, The Journal of Neuroscience.

[81]  G. DeAngelis,et al.  A functional link between area MSTd and heading perception based on vestibular signals , 2007, Nature Neuroscience.

[82]  Anil K. Jain,et al.  Feature extraction methods for character recognition-A survey , 1996, Pattern Recognit..

[83]  M. Hauser,et al.  Functional referents and acoustic similarity: field playback experiments with rhesus monkeys , 1998, Animal Behaviour.

[84]  M. Kilgard,et al.  Cortical activity patterns predict speech discrimination ability , 2008, Nature Neuroscience.

[85]  Joanne L. Miller,et al.  Speech Perception , 1990, Springer Handbook of Auditory Research.

[86]  Bruno B Averbeck,et al.  Neural representation of vocalizations in the primate ventrolateral prefrontal cortex. , 2005, Journal of neurophysiology.

[87]  Asif A. Ghazanfar,et al.  Integration of Bimodal Looming Signals through Neuronal Coherence in the Temporal Lobe , 2008, Current Biology.

[88]  Yale E Cohen,et al.  Coding of auditory-stimulus identity in the auditory non-spatial processing stream. , 2008, Journal of neurophysiology.

[89]  T. Griffiths,et al.  What is an auditory object? , 2004, Nature Reviews Neuroscience.