Oscillatory waveform shape and temporal spike correlations differ across 1 bat frontal and auditory cortex

Neural oscillations are associated with diverse computations in the mammalian brain. The waveform shape of oscillatory activity measured in cortex relates to local physiology, and can be informative about aberrant or dynamically changing states. However, how waveform shape differs across distant yet functionally and anatomically related cortical regions is largely unknown. In this study, we capitalize on simultaneous recordings of local field potentials (LFPs) in the auditory and frontal cortices of awake Carollia perspicillata bats to examine, on a cycle-by-cycle basis, waveform shape differences across cortical regions. We find that waveform shape differs markedly in the fronto-auditory circuit even for rhythmic activity in comparable frequency ranges (i.e. in the delta and gamma bands) during spontaneous activity. In addition, we report consistent differences between areas in the variability of waveform shape across individual cycles. A conceptual model predicts higher spike-spike and spike-LFP correlations in regions with more asymmetric shape, a phenomenon that was observed in the data: spike-spike and spike-LFP correlations were higher in frontal cortex. The model suggests a relationship between waveform shape differences and differences in spike correlations across cortical areas. Altogether, these results indicate that oscillatory activity in frontal and auditory possess distinct dynamics related to the anatomical and functional diversity of the fronto-auditory circuit. Significance statement The brain activity of many animals displays intricate oscillations, which are usually characterized in terms of their frequency and amplitude. Here, we study oscillations from the bat frontal and auditory cortices on a cycle-by-cycle basis, additionally focusing on their characteristic waveform shape. The study reveals clear differences across regions in waveform shape and oscillatory regularity, even when the frequency of the oscillations is similar. A conceptual model predicts that more asymmetric waveforms result from stronger correlations between neural spikes and electrical field activity. Such predictions were supported by the data. The findings shed light onto the unique properties of different cortical areas, providing key insights into the distinctive physiology and functional diversity within the fronto-auditory circuit.

[1]  Jonas-Frederic Sauer,et al.  Behavioral State-Dependent Modulation of Prefrontal Cortex Activity by Respiration , 2023, The Journal of Neuroscience.

[2]  C. Schroeder,et al.  Detecting Spontaneous Neural Oscillation Events in Primate Auditory Cortex , 2022, eNeuro.

[3]  Julio C. Hechavarría,et al.  Echolocation-related reversal of information flow in a cortical vocalization network , 2022, Nature Communications.

[4]  P. Fries,et al.  Predictive coding of natural images by V1 firing rates and rhythmic synchronization , 2022, Neuron.

[5]  C. Herry,et al.  Breathing-driven prefrontal oscillations regulate maintenance of conditioned-fear evoked freezing independently of initiation , 2021, Nature Communications.

[6]  A. Sack,et al.  Top-down control of visual cortex by the frontal eye fields through oscillatory realignment , 2021, Nature Communications.

[7]  R. Saunders,et al.  Theta, but Not Gamma Oscillations in Area V4 Depend on Input from Primary Visual Cortex , 2020, Current Biology.

[8]  Richard Gao,et al.  Parameterizing neural power spectra into periodic and aperiodic components , 2020, Nature Neuroscience.

[9]  Bradley Voytek,et al.  Longitudinal changes in aperiodic and periodic activity in electrophysiological recordings in the first seven months of life , 2020, Developmental Cognitive Neuroscience.

[10]  Adriano B. L. Tort,et al.  Hippocampal-Prefrontal Interactions during Spatial Decision-Making , 2020, bioRxiv.

[11]  Boris Gourévitch,et al.  Oscillations in the auditory system and their possible role , 2020, Neuroscience & Biobehavioral Reviews.

[12]  Julio C. Hechavarría,et al.  Fronto-Temporal Coupling Dynamics During Spontaneous Activity and Auditory Processing in the Bat Carollia perspicillata , 2020, Frontiers in Systems Neuroscience.

[13]  Julio C. Hechavarría,et al.  Neural oscillations in the fronto-striatal network predict vocal output in bats , 2020, PLoS biology.

[14]  Yangyang Wang,et al.  Differential contributions of synaptic and intrinsic inhibitory currents to speech segmentation via flexible phase-locking in neural oscillators , 2020, bioRxiv.

[15]  Julio C. Hechavarría,et al.  Laminar specificity of oscillatory coherence in the auditory cortex , 2019, Brain Structure and Function.

[16]  Julio C. Hechavarría,et al.  Modified synaptic dynamics predict neural activity patterns in an auditory field within the frontal cortex , 2020, The European journal of neuroscience.

[17]  Nicole C. Swann,et al.  Characteristics of Waveform Shape in Parkinson’s Disease Detected with Scalp Electroencephalography , 2019, eNeuro.

[18]  David Poeppel,et al.  An oscillator model better predicts cortical entrainment to music , 2019, Proceedings of the National Academy of Sciences.

[19]  Hannah Monyer,et al.  Gamma oscillations in somatosensory cortex recruit prefrontal and descending serotonergic pathways in aversion and nociception , 2019, Nature Communications.

[20]  Sacha Jennifer van Albada,et al.  An architectonic type principle integrates macroscopic cortico-cortical connections with intrinsic cortical circuits of the primate brain , 2019, Network Neuroscience.

[21]  Julio C. Hechavarría,et al.  Neuronal coding of multiscale temporal features in communication sequences within the bat auditory cortex , 2018, Communications Biology.

[22]  Natalie Schaworonkow,et al.  Spatial neuronal synchronization and the waveform of oscillations: Implications for EEG and MEG , 2018, bioRxiv.

[23]  G. Mangun,et al.  Theta Oscillations Index Frontal Decision-Making and Mediate Reciprocal Frontal-Parietal Interactions in Willed Attention. , 2018, Cerebral cortex.

[24]  T. Klausberger,et al.  Spike-Timing of Orbitofrontal Neurons Is Synchronized With Breathing , 2018, Front. Cell. Neurosci..

[25]  Bradley Voytek,et al.  Cycle-by-cycle analysis of neural oscillations , 2018, bioRxiv.

[26]  Andreas Draguhn,et al.  Respiration-Entrained Brain Rhythms Are Global but Often Overlooked , 2018, Trends in Neurosciences.

[27]  David Poeppel,et al.  Concurrent temporal channels for auditory processing: Oscillatory neural entrainment reveals segregation of function at different scales , 2017, PLoS biology.

[28]  Bradley Voytek,et al.  Nonsinusoidal Beta Oscillations Reflect Cortical Pathophysiology in Parkinson's Disease , 2017, The Journal of Neuroscience.

[29]  S. Cole,et al.  Brain Oscillations and the Importance of Waveform Shape , 2017, Trends in Cognitive Sciences.

[30]  Julio C. Hechavarría,et al.  Vocal sequences suppress spiking in the bat auditory cortex while evoking concomitant steady-state local field potentials , 2016, Scientific Reports.

[31]  Wei-Cheng Chang,et al.  Organization of long-range inputs and outputs of frontal cortex for top-down control , 2016, Nature Neuroscience.

[32]  Yutaka Sakai,et al.  Similarity in Neuronal Firing Regimes across Mammalian Species , 2016, The Journal of Neuroscience.

[33]  Claus C. Hilgetag,et al.  Towards a “canonical” agranular cortical microcircuit , 2015, Front. Neuroanat..

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

[35]  C. Barnes,et al.  Reduced Gamma Frequency in the Medial Frontal Cortex of Aged Rats during Behavior and Rest: Implications for Age-Related Behavioral Slowing , 2012, The Journal of Neuroscience.

[36]  J. Obleser,et al.  Frequency modulation entrains slow neural oscillations and optimizes human listening behavior , 2012, Proceedings of the National Academy of Sciences.

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

[38]  L. Fadiga,et al.  Origins of 1/f2 scaling in the power spectrum of intracortical local field potential. , 2012, Journal of neurophysiology.

[39]  Maria V. Sanchez-Vives,et al.  Slow and fast rhythms generated in the cerebral cortex of the anesthetized mouse. , 2011, Journal of neurophysiology.

[40]  Bryan M. Hooks,et al.  Laminar Analysis of Excitatory Local Circuits in Vibrissal Motor and Sensory Cortical Areas , 2011, PLoS biology.

[41]  Jochen Braun,et al.  Attractors and noise: Twin drivers of decisions and multistability , 2010, NeuroImage.

[42]  Martin Vinck,et al.  The pairwise phase consistency: A bias-free measure of rhythmic neuronal synchronization , 2010, NeuroImage.

[43]  M. D’Esposito,et al.  Is the rostro-caudal axis of the frontal lobe hierarchical? , 2009, Nature Reviews Neuroscience.

[44]  Gordon M. G. Shepherd,et al.  Intracortical Cartography in an Agranular Area , 2009, Front. Neurosci..

[45]  Kikuro Fukushima,et al.  Relating Neuronal Firing Patterns to Functional Differentiation of Cerebral Cortex , 2009, PLoS Comput. Biol..

[46]  D. Poeppel,et al.  Phase Patterns of Neuronal Responses Reliably Discriminate Speech in Human Auditory Cortex , 2007, Neuron.

[47]  Joachim Gross,et al.  Gamma Oscillations in Human Primary Somatosensory Cortex Reflect Pain Perception , 2007, PLoS biology.

[48]  C. Schroeder,et al.  Neuronal Oscillations and Multisensory Interaction in Primary Auditory Cortex , 2007, Neuron.

[49]  Ankoor S. Shah,et al.  An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. , 2005, Journal of neurophysiology.

[50]  A. Medvedev,et al.  Local field potentials and spiking activity in the primary auditory cortex in response to social calls. , 2004, Journal of neurophysiology.

[51]  R. Douglas,et al.  Neuronal circuits of the neocortex. , 2004, Annual review of neuroscience.

[52]  Klaas E. Stephan,et al.  The anatomical basis of functional localization in the cortex , 2002, Nature Reviews Neuroscience.

[53]  R. Yuste,et al.  Cortical area and species differences in dendritic spine morphology , 2002, Journal of neurocytology.

[54]  J. Kanwal,et al.  Auditory responses from the frontal cortex in the mustached bat, Pteronotus parnellii , 2000, Neuroreport.

[55]  K. Esser,et al.  Auditory responses from the frontal cortex in the short‐tailed fruit bat Carollia perspicillata , 2000, Neuroreport.

[56]  K. Esser,et al.  Tonotopic organization and parcellation of auditory cortex in the FM‐bat Carollia perspicillata , 1999, The European journal of neuroscience.

[57]  V. Mountcastle The columnar organization of the neocortex. , 1997, Brain : a journal of neurology.

[58]  D. Pandya,et al.  Comparison of prefrontal architecture and connections. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[59]  A. Cowey,et al.  Patterns of inter- and intralaminar GABAergic connections distinguish striate (V1) and extrastriate (V2, V4) visual cortices and their functionally specialized subdivisions in the rhesus monkey , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  J. Kobler,et al.  Central acoustic tract in an echolocating bat: An extralemniscal auditory pathway to the thalamus , 1989, The Journal of comparative neurology.

[61]  J. Kobler,et al.  Auditory pathways to the frontal cortex of the mustache bat, Pteronotus parnellii. , 1987, Science.

[62]  R. Camarda,et al.  The frontal agranular cortex and the organization of purposeful movements , 1985, The Italian Journal of Neurological Sciences.

[63]  Jacob Cohen Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[64]  Robert T Knight,et al.  Cognitive neurophysiology of the prefrontal cortex. , 2019, Handbook of clinical neurology.

[65]  C. Schreiner,et al.  Columnar transformations in auditory cortex? A comparison to visual and somatosensory cortices. , 2003, Cerebral cortex.

[66]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .