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Title: Neural Coding of Natural Stimuli: Information at Sub-Millisecond Resolution

Journal Article · · PLoS Computational Biology (Online)
 [1];  [2];  [3];  [4]
  1. Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Center for Nonlinear Studies (CNLS). Computer, Computational and Statistical Sciences Division
  2. Princeton Univ., NJ (United States). The Hun School of Princeton
  3. Princeton Univ., NJ (United States). Joseph Henry Labs. of Physics; Princeton Univ., NJ (United States). Lewis-Sigler Inst. for Integrative Genomics
  4. Indiana Univ., Bloomington, IN (United States). Dept. of Physics
+ Show Author Affiliations

Sensory information about the outside world is encoded by neurons in sequences of discrete, identical pulses termed action potentials or spikes. There is persistent controversy about the extent to which the precise timing of these spikes is relevant to the function of the brain. We revisit this issue, using the motion-sensitive neurons of the fly visual system as a test case. Our experimental methods allow us to deliver more nearly natural visual stimuli, comparable to those which flies encounter in free, acrobatic flight. New mathematical methods allow us to draw more reliable conclusions about the information content of neural responses even when the set of possible responses is very large. We find that significant amounts of visual information are represented by details of the spike train at millisecond and sub-millisecond precision, even though the sensory input has a correlation time of ,55 ms; different patterns of spike timing represent distinct motion trajectories, and the absolute timing of spikes points to particular features of these trajectories with high precision. Finally, the efficiency of our entropy estimator makes it possible to uncover features of neural coding relevant for natural visual stimuli: first, the system’s information transmission rate varies with natural fluctuations in light intensity, resulting from varying cloud cover, such that marginal increases in information rate thus occur even when the individual photoreceptors are counting on the order of one million photons per second. Secondly, we see that the system exploits the relatively slow dynamics of the stimulus to remove coding redundancy and so generate a more efficient neural code.

Research Organization:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Science Foundation (NSF)
Grant/Contract Number:
AC52-06NA25396; PHY99-07949; ECS-0425850; IIS-0423039
OSTI ID:
1627185
Journal Information:
PLoS Computational Biology (Online), Vol. 4, Issue 3; ISSN 1553-7358
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

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Cited By (43)

A statistical framework for neuroimaging data analysis based on mutual information estimated via a gaussian copula: Gaussian Copula Mutual Information journal November 2016
Large and fast human pyramidal neurons associate with intelligence posted_content January 2018
Measurements of intrahost viral diversity require an unbiased diversity metric journal January 2019
What single neurons can tell us journal February 2019
Information Transduction Capacity of Noisy Biochemical Signaling Networks journal September 2011
Bayesian and Quasi-Bayesian Estimators for Mutual Information from Discrete Data journal May 2013
Mutual Information and Information Gating in Synfire Chains journal February 2018
Supervised Learning of Logical Operations in Layered Spiking Neural Networks with Spike Train Encoding journal May 2012
A view of Neural Networks as Dynamical Systems journal June 2010
Effects of a 60 Hz Magnetic Field Exposure Up to 3000 μT on Human Brain Activation as Measured by Functional Magnetic Resonance Imaging journal July 2015
Measurements of intrahost viral diversity require an unbiased diversity metric. text January 2019
Motor control by precisely timed spike patterns journal January 2017
Cellular and Network Mechanisms for Temporal Signal Propagation in a Cortical Network Model journal August 2019
Quantitative descriptions of generalized arousal, an elementary function of the vertebrate brain journal May 2011
The locus coeruleus and noradrenergic modulation of cognition journal February 2009
Motor control by precisely timed spike patterns. text January 2017
The Effect of Desflurane on Neuronal Communication at a Central Synapse journal April 2015
High Bandwidth Synaptic Communication and Frequency Tracking in Human Neocortex journal November 2014
A statistical framework for neuroimaging data analysis based on mutual information estimated via a Gaussian copula posted_content October 2016
Zipf’s Law and Criticality in Multivariate Data without Fine-Tuning journal August 2014
Motor control by precisely timed spike patterns posted_content May 2016
A view of Neural Networks as dynamical systems text January 2009
Zipf's law and criticality in multivariate data without fine-tuning text January 2013
Unsupervised Bayesian Ising Approximation for revealing the neural dictionary in songbirds posted_content January 2019
Information Processing in Living Systems journal March 2016
Millisecond-Scale Motor Encoding in a Cortical Vocal Area journal December 2014
Temporal Encoding in a Nervous System journal May 2011
Simple biochemical networks allow accurate sensing of multiple ligands with a single receptor journal April 2017
Point process analysis of noise in early invertebrate vision journal October 2017
Variability Measures of Positive Random Variables journal July 2011
Identifying Temporal Codes in Spontaneously Active Sensory Neurons journal November 2011
The Natural Variation of a Neural Code journal March 2012
A Spike-Timing Code for Discriminating Conspecific Vocalizations in the Thalamocortical System of Anesthetized and Awake Guinea Pigs journal January 2009
Sensory prediction on a whiskered robot: a tactile analogy to “optical flow” journal January 2012
On how correlations between excitatory and inhibitory synaptic inputs maximize the information rate of neuronal firing journal June 2014
Time resolution dependence of information measures for spiking neurons: scaling and universality journal August 2015
Transsynaptic modality codes in the brain: possible involvement of synchronized spike timing, microRNAs, exosomes and epigenetic processes journal January 2013
Coincidences and Estimation of Entropies of Random Variables with Large Cardinalities journal December 2011
Information theory and adaptation preprint January 2010
A Kernel-Based Calculation of Information on a Metric Space text January 2014
Modular Acquisition and Stimulation System for Timestamp-Driven Neuroscience Experiments text January 2015
Time Resolution Dependence of Information Measures for Spiking Neurons: Atoms, Scaling, and Universality preprint January 2015
Large and fast human pyramidal neurons associate with intelligence journal December 2018

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
97 MATHEMATICS AND COMPUTING
Entropy
action potentials
light
neurons
probability distribution
sensory perception
photons
coding mechanisms