Predicting stimulus-locked single unit spiking from cortical local field potentials

The rapidly increasing use of the local field potential (LFP) has motivated research to better understand its relation to the gold standard of neural activity, single unit (SU) spiking. We addressed this in an in vivo, awake, restrained mouse auditory cortical electrophysiology preparation by asking whether the LFP could actually be used to predict stimulus-evoked SU spiking. Implementing a Bayesian algorithm to predict the likelihood of spiking on a trial by trial basis from different representations of the despiked LFP signal, we were able to predict, with high quality and fine temporal resolution (2 ms), the time course of a SU’s excitatory or inhibitory firing rate response to natural species-specific vocalizations. Our best predictions were achieved by representing the LFP by its wide-band Hilbert phase signal, and approximating the statistical structure of this signal at different time points as independent. Our results show that each SU’s action potential has a unique relationship with the LFP that can be reliably used to predict the occurrence of spikes. This “signature” interaction can reflect both pre- and post-spike neural activity that is intrinsic to the local circuit rather than just dictated by the stimulus. Finally, the time course of this “signature” may be most faithful when the full bandwidth of the LFP, rather than specific narrow-band components, is used for representation.

[1]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[2]  Robert C. Liu,et al.  Auditory Cortical Detection and Discrimination Correlates with Communicative Significance , 2007, PLoS biology.

[3]  Arthur Gretton,et al.  Inferring spike trains from local field potentials. , 2008, Journal of neurophysiology.

[4]  Thomas M. Cover,et al.  Elements of Information Theory , 2005 .

[5]  Mu-ming Poo,et al.  Self-Control in Decision-Making Involves Modulation of the vmPFC Valuation System , 2012 .

[6]  Robert C. Liu,et al.  Inhibitory Plasticity in a Lateral Band Improves Cortical Detection of Natural Vocalizations , 2009, Neuron.

[7]  M. Weliky,et al.  Small modulation of ongoing cortical dynamics by sensory input during natural vision , 2004, Nature.

[8]  A. Grinvald,et al.  Spontaneously emerging cortical representations of visual attributes , 2003, Nature.

[9]  G. V. Simpson,et al.  Phase Locking of Single Neuron Activity to Theta Oscillations during Working Memory in Monkey Extrastriate Visual Cortex , 2003, Neuron.

[10]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[11]  G. Buzsáki,et al.  Gamma Oscillations in the Entorhinal Cortex of the Freely Behaving Rat , 1998, The Journal of Neuroscience.

[12]  Eran Stark,et al.  Comparison of direction and object selectivity of local field potentials and single units in macaque posterior parietal cortex during prehension. , 2007, Journal of neurophysiology.

[13]  N. Logothetis,et al.  Visual modulation of neurons in auditory cortex. , 2008, Cerebral cortex.

[14]  Christoph Kayser,et al.  Tuning to sound frequency in auditory field potentials. , 2007, Journal of neurophysiology.

[15]  A. Bruns Fourier-, Hilbert- and wavelet-based signal analysis: are they really different approaches? , 2004, Journal of Neuroscience Methods.

[16]  Ernst Niebur,et al.  Effect of Stimulus Intensity on the Spike–Local Field Potential Relationship in the Secondary Somatosensory Cortex , 2008, The Journal of Neuroscience.

[17]  N. C. Singh,et al.  Estimating spatio-temporal receptive fields of auditory and visual neurons from their responses to natural stimuli , 2001 .

[18]  J. Csicsvari,et al.  Intracellular features predicted by extracellular recordings in the hippocampus in vivo. , 2000, Journal of neurophysiology.

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

[20]  C. Schroeder,et al.  The Leading Sense: Supramodal Control of Neurophysiological Context by Attention , 2009, Neuron.

[21]  W. Newsome,et al.  Local Field Potential in Cortical Area MT: Stimulus Tuning and Behavioral Correlations , 2006, The Journal of Neuroscience.

[22]  Rajesh P. N. Rao,et al.  Nonlinear Phase–Phase Cross-Frequency Coupling Mediates Communication between Distant Sites in Human Neocortex , 2009, The Journal of Neuroscience.

[23]  J. Fell,et al.  Phase/amplitude reset and theta–gamma interaction in the human medial temporal lobe during a continuous word recognition memory task , 2005, Hippocampus.

[24]  N. Logothetis,et al.  Frequency-Band Coupling in Surface EEG Reflects Spiking Activity in Monkey Visual Cortex , 2009, Neuron.

[25]  Bijan Pesaran,et al.  Temporal structure in neuronal activity during working memory in macaque parietal cortex , 2000, Nature Neuroscience.

[26]  Stephen J. Anderson,et al.  Elsevier Editorial System(tm) for Brain Research Manuscript Draft Response Letter Reviewer Number 1 Attentional Changes in Pre-stimulus Oscillatory Activity within Early Visual Cortex Are Predictive of Human Visual Performance , 2007 .

[27]  O. Jensen,et al.  Cross-frequency coupling between neuronal oscillations , 2007, Trends in Cognitive Sciences.

[28]  Arthur Gretton,et al.  Low-Frequency Local Field Potentials and Spikes in Primary Visual Cortex Convey Independent Visual Information , 2008, The Journal of Neuroscience.

[29]  N. Logothetis The Underpinnings of the BOLD Functional Magnetic Resonance Imaging Signal , 2003, The Journal of Neuroscience.

[30]  R. Oostenveld,et al.  Theta and Gamma Oscillations Predict Encoding and Retrieval of Declarative Memory , 2006, The Journal of Neuroscience.

[31]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[32]  Jos J Eggermont,et al.  Comparison between local field potentials and unit cluster activity in primary auditory cortex and anterior auditory field in the cat , 2002, Hearing Research.

[33]  Arne D. Ekstrom,et al.  Brain Oscillations Control Timing of Single-Neuron Activity in Humans , 2007, The Journal of Neuroscience.

[34]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[35]  Robert C. Liu,et al.  Acoustic variability and distinguishability among mouse ultrasound vocalizations. , 2003, The Journal of the Acoustical Society of America.

[36]  Jeremy R. Manning,et al.  Broadband Shifts in Local Field Potential Power Spectra Are Correlated with Single-Neuron Spiking in Humans , 2009, The Journal of Neuroscience.

[37]  Boualem Boashash,et al.  Estimating and interpreting the instantaneous frequency of a signal. II. A/lgorithms and applications , 1992, Proc. IEEE.

[38]  E. Brown,et al.  Analysis of LFP phase predicts sensory response of barrel cortex. , 2006, Journal of neurophysiology.

[39]  Jürgen Kurths,et al.  Synchronization - A Universal Concept in Nonlinear Sciences , 2001, Cambridge Nonlinear Science Series.

[40]  Jürgen Kurths,et al.  Synchronization: Phase locking and frequency entrainment , 2001 .