Discovering Precise Temporal Patterns in Large-Scale Neural Recordings through Robust and Interpretable Time Warping

Alex H Williams; Ben Poole; Niru Maheswaranathan; Ashesh K Dhawale; Tucker Fisher; Christopher D Wilson; David H Brann; Eric M Trautmann; Stephen Ryu; Roman Shusterman; Dmitry Rinberg; Bence P Ölveczky; Krishna V Shenoy; Surya Ganguli

doi:10.1016/j.neuron.2019.10.020

Discovering Precise Temporal Patterns in Large-Scale Neural Recordings through Robust and Interpretable Time Warping

Neuron. 2020 Jan 22;105(2):246-259.e8. doi: 10.1016/j.neuron.2019.10.020. Epub 2019 Nov 27.

Authors

Affiliations

¹ Neuroscience Program, Stanford University, Stanford, CA 94305, USA. Electronic address: ahwillia@stanford.edu.
² Google Brain, Google Inc., Mountain View, CA 94043, USA.
³ Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA; Center for Brain Science, Harvard University, Cambridge, MA 02138, USA.
⁴ Neuroscience Program, Stanford University, Stanford, CA 94305, USA.
⁵ Neuroscience Institute, New York University School of Medicine, New York, NY 10016, USA.
⁶ Neuroscience Program, Stanford University, Stanford, CA 94305, USA; Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA.
⁷ Electrical Engineering Department, Stanford University, Stanford, CA 94305, USA; Department of Neurosurgery, Palo Alto Medical Foundation, Palo Alto, CA 94301, USA.
⁸ Institute of Neuroscience, University of Oregon, Eugene, OR 97403, USA.
⁹ Neuroscience Institute, New York University School of Medicine, New York, NY 10016, USA; Center for Neural Science, New York University, New York, NY 10016, USA.
¹⁰ Neurobiology Department, Stanford University, Stanford, CA 94305, USA; Electrical Engineering Department, Stanford University, Stanford, CA 94305, USA; Bioengineering Department, Stanford University, Stanford, CA 94305, USA; Bio-X Program, Stanford University, Stanford, CA 94305, USA; Wu Tsai Stanford Neurosciences Institute, Stanford University, Stanford, CA 94305, USA; Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA.
¹¹ Applied Physics Department, Stanford University, Stanford, CA 94305, USA; Neurobiology Department, Stanford University, Stanford, CA 94305, USA; Electrical Engineering Department, Stanford University, Stanford, CA 94305, USA; Bio-X Program, Stanford University, Stanford, CA 94305, USA; Wu Tsai Stanford Neurosciences Institute, Stanford University, Stanford, CA 94305, USA; Google Brain, Google Inc., Mountain View, CA 94043, USA. Electronic address: sganguli@stanford.edu.

Abstract

Though the temporal precision of neural computation has been studied intensively, a data-driven determination of this precision remains a fundamental challenge. Reproducible spike patterns may be obscured on single trials by uncontrolled temporal variability in behavior and cognition and may not be time locked to measurable signatures in behavior or local field potentials (LFP). To overcome these challenges, we describe a general-purpose time warping framework that reveals precise spike-time patterns in an unsupervised manner, even when these patterns are decoupled from behavior or are temporally stretched across single trials. We demonstrate this method across diverse systems: cued reaching in nonhuman primates, motor sequence production in rats, and olfaction in mice. This approach flexibly uncovers diverse dynamical firing patterns, including pulsatile responses to behavioral events, LFP-aligned oscillatory spiking, and even unanticipated patterns, such as 7 Hz oscillations in rat motor cortex that are not time locked to measured behaviors or LFP.

Keywords: Exploratory Data Analysis; Neural Oscillations; Population Dynamics; Spike Train Analysis; Statistics; Time Warping; Unsupervised Learning.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Action Potentials / physiology*
Amyloid beta-Protein Precursor / genetics
Animals
Gene Knock-In Techniques
Macaca mulatta
Male
Mice
Mice, Transgenic
Microinjections
Motor Cortex / physiology
Neurons / physiology*
Pattern Recognition, Automated / methods*
Peptide Fragments / genetics
Primary Cell Culture
Proteins / genetics
Rats
Time Factors

Substances

Amyloid beta-Protein Precursor
Peptide Fragments
Proteins
amyloid beta-protein precursor 695 (681-695)
familial Alzheimer's disease protein 1

Abstract

Publication types

MeSH terms

Substances

Grants and funding