Benefits of Pathway Splitting in Sensory Coding

In many sensory systems, the neural signal splits into multiple parallel pathways. For example, in the mammalian retina, ∼20 types of retinal ganglion cells transmit information about the visual scene to the brain. The purpose of this profuse and early pathway splitting remains unknown. We examine a common instance of splitting into ON and OFF neurons excited by increments and decrements of light intensity in the visual scene, respectively. We test the hypothesis that pathway splitting enables more efficient encoding of sensory stimuli. Specifically, we compare a model system with an ON and an OFF neuron to one with two ON neurons. Surprisingly, the optimal ON–OFF system transmits the same information as the optimal ON–ON system, if one constrains the maximal firing rate of the neurons. However, the ON–OFF system uses fewer spikes on average to transmit this information. This superiority of the ON–OFF system is also observed when the two systems are optimized while constraining their mean firing rate. The efficiency gain for the ON–OFF split is comparable with that derived from decorrelation, a well known processing strategy of early sensory systems. The gain can be orders of magnitude larger when the ecologically important stimuli are rare but large events of either polarity. The ON–OFF system also provides a better code for extracting information by a linear downstream decoder. The results suggest that the evolution of ON–OFF diversification in sensory systems may be driven by the benefits of lowering average metabolic cost, especially in a world in which the relevant stimuli are sparse.

• Publication year

  2014

• Venue

  Journal of Neuroscience

• Publication date

  2014-09-03

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1523/JNEUROSCI.1032-14.2014PMID 25186757PMCID PMC4152610
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Second Order Phase Transition Describes Maximally Informative Encoding in the Retina

  2014cited by this paper
• Neuronal nonlinearity explains greater visual spatial resolution for darks than lights

  2014cited by this paper
• Computing Complex Visual Features with Retinal Spike Times

  2013cited by this paper
• Interacting Linear and Nonlinear Characteristics Produce Population Coding Asymmetries between ON and OFF Cells in the Retina

  2013cited by this paper
• The neuronal organization of the retina.

  2012influential reference
• Possible Principles Underlying the Transformations of Sensory Messages

  2012cited by this paper
• Decorrelation and efficient coding by retinal ganglion cells

  2012influential reference
• Seeing things in motion: models, circuits, and mechanisms.

  2011cited by this paper
• System identification of Drosophila olfactory sensory neurons

  2011cited by this paper
• Cone photoreceptor contributions to noise and correlations in the retinal output

  2011cited by this paper
• Could information theory provide an ecological theory of sensory processing?

  2011cited by this paper
• Response rescaling in bacterial chemotaxis

  2011cited by this paper
• The coding of temperature in the Drosophila brain.

  2011cited by this paper
• Nonoverlapping sets of synapses drive on responses and off responses in auditory cortex.

  2010cited by this paper
• Biophysical mechanisms underlying olfactory receptor neuron dynamics

  2010cited by this paper
• Symmetry Breakdown in the ON and OFF Pathways of the Retina at Night: Functional Implications

  2010cited by this paper
• Retina is structured to process an excess of darkness in natural scenes

  2010influential reference
• Eye smarter than scientists believed: neural computations in circuits of the retina.

  2010cited by this paper
• ON and OFF pathways in Drosophila motion vision

  2010cited by this paper
• “Black” Responses Dominate Macaque Primary Visual Cortex V1

  2009cited by this paper
• Neural encoding of rapidly fluctuating odors.

  2009cited by this paper
• Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans

  2008cited by this paper
• Neural population coding is optimized by discrete tuning curves.

  2008cited by this paper
• On and off domains of geniculate afferents in cat primary visual cortex

  2008cited by this paper
• Rapid Neural Coding in the Retina with Relative Spike Latencies

  2008cited by this paper
• Visual perception and the statistical properties of natural scenes.

  2008cited by this paper
• Spatio-temporal correlations and visual signalling in a complete neuronal population

  2008cited by this paper
• A Neural Computation for Visual Acuity in the Presence of Eye Movements

  2007cited by this paper
• The ON-OFF dichotomy in visual processing: from receptors to perception.

  2007cited by this paper
• Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans

  2007cited by this paper
• A theory of maximizing sensory information

  2004cited by this paper
• Neural Engineering: Computation, Representation, and Dynamics in Neurobiological Systems

  2004cited by this paper
• Precision of spike trains in primate retinal ganglion cells.

  2004influential reference
• Parallel processing in the mammalian retina

  2004influential reference
• Optimal neural rate coding leads to bimodal firing rate distributions

  2003cited by this paper
• Modulation spectra of natural sounds and ethological theories of auditory processing.

  2003cited by this paper
• Functional Asymmetries in ON and OFF Ganglion Cells of Primate Retina

  2002influential reference
• Face identification using one spike per neuron: resistance to image degradations

  2001cited by this paper
• Adaptation to Temporal Contrast in Primate and Salamander Retina

  2001cited by this paper
• Calculating the contrasts that retinal ganglion cells and LGN neurones encounter in natural scenes.

  2000cited by this paper
• Visual coding and the phase structure of natural scenes.

  1999cited by this paper
• The "independent components" of natural scenes are edge filters.

  1997cited by this paper
• Processing of natural time series of intensities by the visual system of the blowfly.

  1997cited by this paper
• Adaptation of retinal processing to image contrast and spatial scale

  1997cited by this paper
• The structure and precision of retinal spike trains.

  1997cited by this paper
• STATISTICS OF NATURAL TIME-VARYING IMAGES

  1995influential reference
• Theory in motion.

  1995cited by this paper
• What Is the Goal of Sensory Coding?

  1994cited by this paper
• Membrane properties underlying the firing of neurons in the avian cochlear nucleus

  1994cited by this paper
• The statistics of natural images

  1994cited by this paper
• Statistics of Natural Images: Scaling in the Woods

  1993cited by this paper
• Simple models for reading neuronal population codes.

  1993cited by this paper
• What Does the Retina Know about Natural Scenes?

  1992cited by this paper
• The ON and OFF channels of the visual system.

  1992cited by this paper
• Theoretical predictions of spatiotemporal receptive fields of fly LMCs, and experimental validation

  1992cited by this paper
• Towards a Theory of Early Visual Processing

  1990cited by this paper
• Capacity of a pulse amplitude modulated direct detection photon channel

  1990cited by this paper
• Sensitivity of macaque retinal ganglion cells to chromatic and luminance flicker.

  1989cited by this paper
• Visual Behavior in Salamanders

  1987cited by this paper
• Temporal comparisons in bacterial chemotaxis.

  1986cited by this paper
• Functions of the ON and OFF channels of the visual system

  1986cited by this paper
• Impulse responses in bacterial chemotaxis.

  1982cited by this paper
• Morphology and topography of on- and off-alpha cells in the cat retina

  1981cited by this paper
• Morphology and mosaic of on- and off-beta cells in the cat retina and some functional considerations

  1981cited by this paper
• Light Antennas in phototactic algae.

  1980cited by this paper
• Intracellular rotation and the phototropic response of Phycomyces.

  1977cited by this paper
• Psychophysical studies of monkey vision. 3. Spatial luminance contrast sensitivity tests of macaque and human observers.

  1974cited by this paper
• The information capacity of nerve cells using a frequency code.

  1967cited by this paper
• Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit

  1964cited by this paper
• Some informational aspects of visual perception.

  1954cited by this paper
• Discharge patterns and functional organization of mammalian retina.

  1953cited by this paper

• Convex Efficient Coding

  2026cites this paper
• On analogies in vertebrate and insect visual systems

  2025cites this paper
• Effect of stimulus onset and offset asynchrony on audiovisual temporal recalibration.

  2025cites this paper
• Asymmetric activation of retinal ON and OFF pathways by AOSLO raster-scanned visual stimuli

  2025cites this paper
• Convergence of efficient and predictive coding in multimodal sensory processing

  2025cites this paper
• Retinal processing of natural scenes: challenges ahead.

  2025cites this paper
• Origins and objectives of computational diversity in sensory populations.

  2025cites this paper
• Neurons as Detectors of Coherent Sets in Sensory Dynamics

  2025cites this paper
• An opponent striatal circuit for distributional reinforcement learning

  2025influential citation
• Evolution of rod bipolar cells and rod vision

  2025cites this paper
• Molecular mechanism establishing the OFF pathway in vision

  2025cites this paper
• A Network of Biologically Inspired Rectified Spectral Units (ReSUs) Learns Hierarchical Features Without Error Backpropagation

  2025cites this paper
• Adaptation to visual sparsity enhances responses to isolated stimuli.

  2024cites this paper
• Asymmetric Activation of Retinal ON and OFF Pathways by AOSLO Raster-Scanned Visual Stimuli

  2024cites this paper
• Connectome-constrained networks predict neural activity across the fly visual system

  2024cites this paper
• Nanotechnology for vision restoration

  2024cites this paper
• Visual Field Asymmetries in Responses to ON and OFF Pathway Biasing Stimuli

  2024cites this paper
• EAPTON: Event-based Antinoise Powerlines Tracking with ON/OFF Enhancement

  2024cites this paper
• Cell firing between ON alpha retinal ganglion cells and coupled amacrine cells in the mouse retina.

  2024cites this paper
• Slow and steady: auditory features for discriminating animal vocalizations

  2024cites this paper
• Divergent short-term plasticity creates parallel pathways for computation and behavior in an olfactory circuit

  2024cites this paper
• Adaptation to visual sparsity enhances responses to infrequent stimuli

  2024cites this paper
• Distributed feature representations of natural stimuli across parallel retinal pathways

  2024cites this paper
• A general model unifying the adaptive, transient and sustained properties of ON and OFF auditory neural responses

  2024cites this paper
• An opponent striatal circuit for distributional reinforcement learning

  2024cites this paper
• Jointly efficient encoding and decoding in neural populations

  2024cites this paper
• Spatiotemporal visual statistics of aquatic environments in the natural habitats of zebrafish

  2023cites this paper
• Connectome-constrained deep mechanistic networks predict neural responses across the fly visual system at single-neuron resolution

  2023cites this paper
• Birds multiplex spectral and temporal visual information via retinal On- and Off-channels

  2023cites this paper
• Disynaptic inhibition shapes tuning of OFF-motion detectors in Drosophila.

  2023cites this paper
• Applications of information geometry to spiking neural network activity.

  2023cites this paper
• Interpreting the retinal neural code for natural scenes: From computations to neurons

  2023cites this paper
• Population coding strategies in human tactile afferents

  2022cites this paper
• Birds multiplex spectral and temporal visual information via retinal On- and Off-channels

  2022cites this paper
• Coarse-to-fine processing drives the efficient coding of natural scenes in mouse visual cortex

  2022cites this paper
• Efficient processing of natural scenes in visual cortex

  2022cites this paper
• Birds multiplex spectral and 1 temporal visual information via 2 retinal On- and Off-channels

  2022cites this paper
• Efficient population coding of sensory stimuli

  2022cites this paper
• Efficient Temporal Coding in the Early Visual System: Existing Evidence and Future Directions

  2022cites this paper
• Reconstruction of visual images from mouse retinal ganglion cell spiking activity using convolutional neural networks

  2022cites this paper
• Natural environment statistics in the upper and lower visual field are reflected in mouse retinal specializations.

  2021cites this paper
• Non-preferred contrast responses in the Drosophila motion pathways reveal a receptive field structure that explains a common visual illusion

  2021cites this paper
• Natural image statistics for mouse vision

  2021cites this paper
• Synergistic population coding of natural communication stimuli by hindbrain electrosensory neurons

  2021cites this paper
• Retinal OFF ganglion cells allow detection of quantal shadows at starlight

  2021cites this paper
• Neuroscience: Convergence of biological and artificial networks

  2021cites this paper
• Scene statistics and noise determine the relative arrangement of receptive field mosaics

  2021cites this paper
• The optimal spatial arrangement of ON and OFF receptive fields

  2021cites this paper
• Impact of Photoreceptor Loss on Retinal Circuitry.

  2021cites this paper
• Temporal vision: measures, mechanisms and meaning

  2021cites this paper
• Predicting individual neuron responses with anatomically constrained task optimization.

  2021cites this paper
• Inter-mosaic coordination of retinal receptive fields

  2021cites this paper
• Electric Stimulation Elicits Heterogeneous Responses in ON but Not OFF Retinal Ganglion Cells to Transmit Rich Neural Information

  2021cites this paper
• Circuit mechanisms for colour vision in zebrafish.

  2021cites this paper
• Stimulus Contrast Affects Spatial Integration in the Lateral Geniculate Nucleus of Macaque Monkeys

  2021cites this paper
• Inferring the function performed by a recurrent neural network

  2021cites this paper
• Quadratic Mutual Information estimation of mouse dLGN receptive fields reveals asymmetry between ON and OFF visual pathways

  2020cites this paper
• Age-related changes in sound onset and offset intensity coding in auditory cortical fields A1 and CL of rhesus macaques.

  2020cites this paper
• Defocused Images Change Multineuronal Firing Patterns in the Mouse Retina

  2020cites this paper
• Clustering of Neural Activity: A Design Principle for Population Codes

  2020cites this paper
• Circuits for Feature Selectivity in the Inner Retina

  2020cites this paper
• Efficient Coding by Midget and Parasol Ganglion Cells in the Human Retina.

  2020cites this paper
• Efficient population coding depends on stimulus convergence and source of noise

  2020influential citation
• Neuronal On- and Off-type heterogeneities improve population coding of envelope signals in the presence of stimulus-induced noise

  2020cites this paper
• Mechanism for analogous illusory motion perception in flies and humans

  2020cites this paper
• Individual bitter-sensing neurons in Drosophila exhibit both ON and OFF responses that influence synaptic plasticity

  2020cites this paper
• Mice Preferentially Use Increases in Cerebral Cortex Spiking to Detect Changes in Visual Stimuli

  2020influential citation
• Mouse retinal specializations reflect knowledge of natural environment statistics

  2020cites this paper
• Developmental and evolutionary constraints on olfactory circuit selection

  2020cites this paper
• How inhibitory neurons increase information transmission under threshold modulation

  2020cites this paper
• Quantifying encoding redundancy induced by rate correlations in Poisson neurons.

  2019cites this paper
• Differential sensitivity of the On and Off visual responses to retinal ischemia.

  2019cites this paper
• Nonlinear transfer and temporal gain control in ON bipolar cells

  2019cites this paper
• Understanding the retinal basis of vision across species

  2019cites this paper
• Perceptual detection depends on spike count integration

  2019cites this paper
• Multiple Timescale Online Learning Rules for Information Maximization with Energetic Constraints

  2019cites this paper
• Activity Correlations between Direction-Selective Retinal Ganglion Cells Synergistically Enhance Motion Decoding from Complex Visual Scenes

  2019cites this paper
• Mice preferentially use increases in cerebral cortex spike rates to detect changes in visual stimuli

  2019influential citation
• Nonlinear convergence boosts information coding in circuits with parallel outputs

  2019influential citation
• ON selectivity in the Drosophila visual system is a multisynaptic process involving both glutamatergic and GABAergic inhibition

  2019cites this paper
• Paradoxical Rules of Spike Train Decoding Revealed at the Sensitivity Limit of Vision.

  2019cites this paper
• Synaptic Information Transmission in a Two-State Model of Short-Term Facilitation

  2019cites this paper
• Defocused Image Changes Signaling of Ganglion Cells in the Mouse Retina

  2019cites this paper
• Functional Diversity in the Retina Improves the Population Code

  2019cites this paper
• Efficient and adaptive sensory codes

  2019cites this paper
• Statistical analysis and optimality of neural systems

  2019cites this paper
• Linking neural responses to behavior with information-preserving population vectors.

  2019cites this paper
• Training and inferring neural network function with multi-agent reinforcement learning

  2019influential citation
• The Neuronal Basis of an Illusory Motion Percept Is Explained by Decorrelation of Parallel Motion Pathways.

  2018cites this paper
• The emergence of multiple retinal cell types through efficient coding of natural movies

  2018cites this paper
• Characterization of Retinal Functionality at Different Eccentricities in a Diurnal Rodent

  2018cites this paper
• Stimulus- and goal-oriented frameworks for understanding natural vision

  2018cites this paper
• Pregnancy-Associated Plasma Protein-aa Regulates Photoreceptor Synaptic Development to Mediate Visually Guided Behavior

  2018cites this paper
• Optimal information transmission by overlapping retinal cell mosaics

  2018cites this paper
• Pathway-Specific Asymmetries between ON and OFF Visual Signals

  2018cites this paper
• When Sound Stops: Offset Responses in the Auditory System.

  2018cites this paper
• Bayesian Efficient Coding

  2017cites this paper
• Functional diversity among sensory neurons from efficient coding principles

  2017cites this paper
• Top-down control of sensory focus in bursty pyramidal cell populations

  2017cites this paper
• Synchronous inhibitory pathways create both efficiency and diversity in the retina

  2017cites this paper