Dissociation of task engagement and arousal effects in auditory cortex and midbrain

Both generalized arousal and engagement in a specific task influence sensory neural processing. To isolate effects of these state variables in the auditory system, we recorded single-unit activity from primary auditory cortex (A1) and inferior colliculus (IC) of ferrets during a tone detection task, while monitoring arousal via changes in pupil size. We used a generalized linear model to assess the influence of task engagement and pupil size on sound-evoked activity. In both areas, these two variables affected independent neural populations. Pupil size effects were more prominent in IC, while pupil and task engagement effects were equally likely in A1. Task engagement was correlated with larger pupil; thus, some apparent effects of task engagement should in fact be attributed to fluctuations in pupil size. These results indicate a hierarchy of auditory processing, where generalized arousal enhances activity in midbrain, and effects specific to task engagement become more prominent in cortex.

[1]  F. Wilcoxon Individual Comparisons by Ranking Methods , 1945 .

[2]  D Kahneman,et al.  Pupil Diameter and Load on Memory , 1966, Science.

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

[4]  Josef M. Miller,et al.  Single cell activity in the auditory cortex of the unanesthetized, behaving monkey: Correlation with stimulus controlled behavior , 1975, Brain Research.

[5]  W. R. Webster,et al.  Inferior colliculus. I. Comparison of response properties of neurons in central, pericentral, and external nuclei of adult cat. , 1975, Journal of neurophysiology.

[6]  M. H. Goldstein,et al.  Evoked unit activity in auditory cortex of monkeys performing a selective attention task , 1976, Brain Research.

[7]  A. Ryan,et al.  Effects of behavioral performance on single-unit firing patterns in inferior colliculus of the rhesus monkey. , 1977, Journal of neurophysiology.

[8]  M. Posner,et al.  Attention and the detection of signals. , 1980, Journal of experimental psychology.

[9]  J. Beatty Task-evoked pupillary responses, processing load, and the structure of processing resources. , 1982, Psychological bulletin.

[10]  J. Beatty Task-evoked pupillary responses, processing load, and the structure of processing resources. , 1982 .

[11]  D. Moore,et al.  Some acoustic properties of neurones in the ferret inferior colliculus , 1983, Brain Research.

[12]  J. Kelly,et al.  Hearing in the ferret (Mustela putorius): Thresholds for pure tone detection , 1986, Hearing Research.

[13]  Robert Tibshirani,et al.  Bootstrap Methods for Standard Errors, Confidence Intervals, and Other Measures of Statistical Accuracy , 1986 .

[14]  Norman M. Weinberger,et al.  Classical conditioning induces CS-specific receptive field plasticity in the auditory cortex of the guinea pig , 1990, Brain Research.

[15]  S. Shamma,et al.  Organization of response areas in ferret primary auditory cortex. , 1993, Journal of neurophysiology.

[16]  Georg M. Klump,et al.  Methods in Comparative Psychoacoustics , 1995, BioMethods.

[17]  J. Bakin,et al.  Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[18]  M. Vater,et al.  A microiontophoretic study of acetylcholine effects in the inferior colliculus of horseshoe bats: implications for a modulatory role , 1996, Brain Research.

[19]  B R Rosen,et al.  Modulation of auditory and visual cortex by selective attention is modality-dependent. , 1996, Neuroreport.

[20]  G. Pepper,et al.  The Current State of Knowledge , 1998 .

[21]  H Stanislaw,et al.  Calculation of signal detection theory measures , 1999, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[22]  J. Fritz,et al.  Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex , 2003, Nature Neuroscience.

[23]  Jonathan Z. Simon,et al.  Robust Spectrotemporal Reverse Correlation for the Auditory System: Optimizing Stimulus Design , 2000, Journal of Computational Neuroscience.

[24]  H. Scheich,et al.  Nonauditory Events of a Behavioral Procedure Activate Auditory Cortex of Highly Trained Monkeys , 2005, The Journal of Neuroscience.

[25]  G. Pollak,et al.  Serotonin Shifts First-Spike Latencies of Inferior Colliculus Neurons , 2005, The Journal of Neuroscience.

[26]  J. Fritz,et al.  Differential Dynamic Plasticity of A1 Receptive Fields during Multiple Spectral Tasks , 2005, The Journal of Neuroscience.

[27]  J. Winer Decoding the auditory corticofugal systems , 2006, Hearing Research.

[28]  Nathaniel T. Greene,et al.  Effects of Reward and Behavioral Context on Neural Activity in the Primate Inferior Colliculus , 2022 .

[29]  S. David,et al.  Does attention play a role in dynamic receptive field adaptation to changing acoustic salience in A1? , 2007, Hearing Research.

[30]  Jonathan Z. Simon,et al.  Temporal Symmetry in Primary Auditory Cortex: Implications for Cortical Connectivity , 2006, Neural Computation.

[31]  Zador Anthony,et al.  Engaging in an auditory task suppresses responses in rat auditory cortex , 2008 .

[32]  Xiaoqin Wang,et al.  Neural substrates of vocalization feedback monitoring in primate auditory cortex , 2008, Nature.

[33]  J. Poulet,et al.  Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice , 2008, Nature.

[34]  B. Schofield,et al.  Sources of cholinergic input to the inferior colliculus , 2009, Neuroscience.

[35]  J. Maunsell,et al.  Attention improves performance primarily by reducing interneuronal correlations , 2009, Nature Neuroscience.

[36]  Dario L Ringach,et al.  Spontaneous and driven cortical activity: implications for computation , 2009, Current Opinion in Neurobiology.

[37]  Gonzalo H. Otazu,et al.  Engaging in an auditory task suppresses responses in auditory cortex , 2009, Nature Neuroscience.

[38]  Mounya Elhilali,et al.  Task Difficulty and Performance Induce Diverse Adaptive Patterns in Gain and Shape of Primary Auditory Cortical Receptive Fields , 2009, Neuron.

[39]  Michael J. Goard,et al.  Basal Forebrain Activation Enhances Cortical Coding of Natural Scenes , 2009, Nature Neuroscience.

[40]  Mark S. Gilzenrat,et al.  Pupil diameter tracks changes in control state predicted by the adaptive gain theory of locus coeruleus function , 2010, Cognitive, affective & behavioral neuroscience.

[41]  M. Stryker,et al.  Modulation of Visual Responses by Behavioral State in Mouse Visual Cortex , 2010, Neuron.

[42]  S. David,et al.  Adaptive, behaviorally-gated, persistent encoding of task-relevant auditory information in ferret frontal cortex , 2010, Nature Neuroscience.

[43]  Pingbo Yin,et al.  Do ferrets perceive relative pitch? , 2010, The Journal of the Acoustical Society of America.

[44]  John C. Middlebrooks,et al.  Auditory Cortex Spatial Sensitivity Sharpens During Task Performance , 2010, Nature Neuroscience.

[45]  A. Zador,et al.  Auditory cortex mediates the perceptual effects of acoustic temporal expectation , 2010, Nature Neuroscience.

[46]  Shihab A Shamma,et al.  Task reward structure shapes rapid receptive field plasticity in auditory cortex , 2012, Proceedings of the National Academy of Sciences.

[47]  Jeffrey S. Johnson,et al.  Active Engagement Improves Primary Auditory Cortical Neurons' Ability to Discriminate Temporal Modulation , 2012, The Journal of Neuroscience.

[48]  Laurel H. Carney,et al.  Semi-supervised spike sorting using pattern matching and a scaled Mahalanobis distance metric , 2012, Journal of Neuroscience Methods.

[49]  Jennifer M. Groh,et al.  Sounds and beyond: multisensory and other non-auditory signals in the inferior colliculus , 2012, Front. Neural Circuits.

[50]  Daniel P. Knudsen,et al.  Active recognition enhances the representation of behaviorally relevant information in single auditory forebrain neurons. , 2013, Journal of neurophysiology.

[51]  Joshua X. Gittelman,et al.  Dopamine Modulates Auditory Responses in the Inferior Colliculus in a Heterogeneous Manner , 2013, Journal of the Association for Research in Otolaryngology.

[52]  P. Golshani,et al.  Cellular mechanisms of brain-state-dependent gain modulation in visual cortex , 2013, Nature Neuroscience.

[53]  C. Schroeder,et al.  The Spectrotemporal Filter Mechanism of Auditory Selective Attention , 2013, Neuron.

[54]  Kerry M. M. Walker,et al.  Auditory Cortex Represents Both Pitch Judgments and the Corresponding Acoustic Cues , 2013, Current Biology.

[55]  Y. Cohen,et al.  The what, where and how of auditory-object perception , 2013, Nature Reviews Neuroscience.

[56]  S. A. Shamma,et al.  MANTA—an open-source, high density electrophysiology recording suite for MATLAB , 2013, Front. Neural Circuits.

[57]  R. Mooney,et al.  A synaptic and circuit basis for corollary discharge in the auditory cortex , 2014, Nature.

[58]  M. Stryker,et al.  A Cortical Circuit for Gain Control by Behavioral State , 2014, Cell.

[59]  Chris C. Rodgers,et al.  Neural Correlates of Task Switching in Prefrontal Cortex and Primary Auditory Cortex in a Novel Stimulus Selection Task for Rodents , 2014, Neuron.

[60]  J. Fritz,et al.  Rapid Spectrotemporal Plasticity in Primary Auditory Cortex during Behavior , 2014, The Journal of Neuroscience.

[61]  Li I. Zhang,et al.  Scaling down of balanced excitation and inhibition by active behavioral states in auditory cortex , 2014, Nature Neuroscience.

[62]  S. David,et al.  Emergent Selectivity for Task-Relevant Stimuli in Higher-Order Auditory Cortex , 2014, Neuron.

[63]  Stephen V. David,et al.  The Essential Complexity of Auditory Receptive Fields , 2015, PLoS Comput. Biol..

[64]  Stephen V David,et al.  Rapid Task-Related Plasticity of Spectrotemporal Receptive Fields in the Auditory Midbrain , 2015, The Journal of Neuroscience.

[65]  Mamiko Niwa,et al.  Task Engagement Selectively Modulates Neural Correlations in Primary Auditory Cortex , 2015, The Journal of Neuroscience.

[66]  Stephen V. David,et al.  Cortical Membrane Potential Signature of Optimal States for Sensory Signal Detection , 2015, Neuron.

[67]  Thomas Zhihao Luo,et al.  Neuronal Modulations in Visual Cortex Are Associated with Only One of Multiple Components of Attention , 2015, Neuron.

[68]  Martin Vinck,et al.  Arousal and Locomotion Make Distinct Contributions to Cortical Activity Patterns and Visual Encoding , 2014, Neuron.

[69]  Michael M. Halassa,et al.  Thalamic control of sensory selection in divided attention , 2015, Nature.

[70]  Sotiris C Masmanidis,et al.  Brain activity mapping at multiple scales with silicon microprobes containing 1,024 electrodes. , 2015, Journal of neurophysiology.

[71]  Matthew B. Winn,et al.  The Impact of Auditory Spectral Resolution on Listening Effort Revealed by Pupil Dilation , 2015, Ear and hearing.

[72]  C Daniel Salzman,et al.  Reward expectation differentially modulates attentional behavior and activity in visual area V4 , 2015, Nature Neuroscience.

[73]  J. Gold,et al.  Relationships between Pupil Diameter and Neuronal Activity in the Locus Coeruleus, Colliculi, and Cingulate Cortex , 2016, Neuron.

[74]  D. McCormick,et al.  Pupil fluctuations track rapid changes in adrenergic and cholinergic activity in cortex , 2016, Nature Communications.

[75]  Matteo Carandini,et al.  Kilosort: realtime spike-sorting for extracellular electrophysiology with hundreds of channels , 2016, bioRxiv.

[76]  Andrew S. Liu,et al.  Causal contribution of primate auditory cortex to auditory perceptual decision-making , 2015, Nature Neuroscience.

[77]  Grace W. Lindsay,et al.  Parallel processing by cortical inhibition enables context-dependent behavior , 2016, Nature Neuroscience.

[78]  Michele N. Insanally,et al.  Dynamics of auditory cortical activity during behavioural engagement and auditory perception , 2017, Nature Communications.

[79]  Stefano Panzeri,et al.  Distinct timescales of population coding across cortex , 2017, Nature.

[80]  Jakob Voigts,et al.  Open Ephys electroencephalography (Open Ephys  +  EEG): a modular, low-cost, open-source solution to human neural recording , 2017, Journal of neural engineering.

[81]  Shihab Shamma,et al.  Go/No-Go task engagement enhances population representation of target stimuli in primary auditory cortex , 2018, Nature Communications.

[82]  Stephen V David,et al.  Focal Suppression of Distractor Sounds by Selective Attention in Auditory Cortex , 2017, Cerebral cortex.

[83]  S. Bagdasarov,et al.  Pupil-linked arousal modulates behavior in rats performing a whisker deflection direction discrimination task. , 2018, Journal of neurophysiology.

[84]  Adriana A Zekveld,et al.  The Pupil Dilation Response to Auditory Stimuli: Current State of Knowledge , 2018, Trends in hearing.

[85]  J. Isaacson,et al.  Arousal regulates frequency tuning in primary auditory cortex , 2019, Proceedings of the National Academy of Sciences.

[86]  Giancarlo La Camera,et al.  Cortical computations via metastable activity , 2019, Current Opinion in Neurobiology.

[87]  Zachary P. Schwartz,et al.  -Pupil-associated states modulate excitability but not stimulus selectivity in primary auditory cortex. , 2019, Journal of neurophysiology.

[88]  Nicholas A. Steinmetz,et al.  Spontaneous behaviors drive multidimensional, brainwide activity , 2019, Science.

[89]  Zachary P. Schwartz,et al.  Pupil-associated states modulate excitability but not stimulus selectivity in primary auditory cortex , 2019, bioRxiv.

[90]  Philip A. Kragel,et al.  Deconstructing arousal into wakeful, autonomic and affective varieties , 2018, Neuroscience Letters.

[91]  Michael Brosch,et al.  Associations between sounds and actions in early auditory cortex of nonhuman primates , 2019, eLife.

[92]  Matthew T. Kaufman,et al.  Single-trial neural dynamics are dominated by richly varied movements , 2019, Nature Neuroscience.

[93]  F. Ohl,et al.  Representation of Auditory Task Components and of Their Relationships in Primate Auditory Cortex , 2020, Frontiers in Neuroscience.