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Synchronous inhibitory pathways create both efficiency and diversity in the retina

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 2022年第4期119卷 e2116589119页

作者： Manu, Mihai McIntosh, Lane T. Kastner, David B. Naecker, Benjamin N. Baccus, Stephen A. Stanford Univ Dept Neurobiol Stanford CA 94035 USA Stanford Univ Neurosci Program Sch Med Stanford CA 94035 USA Witten Herdecke Univ Cologne Merheim Med Ctr Dept Neurosurg Sch Med D-51109 Cologne Germany Univ Calif San Francisco Dept Psychiat San Francisco CA 94143 USA

Sensory receptive fields combine features that originate in different neural pathways. Retinal ganglion cell receptive fields compute intensity changes across space and time using a peripheral region known as the surround, a property that improves information transmission about natural scenes. The visual features that construct this fundamental property have not been quantitatively assigned to specific interneurons. Here, we describe a generalizable approach using simultaneous intracellular and multielectrode recording to directly measure and manipulate the sensory feature conveyed by a neural pathway to a downstream neuron. By directly controlling the gain of individual interneurons in the circuit, we show that rather than transmitting different temporal features, inhibitory horizontal cells and linear amacrine cells synchronously create the linear surround at different spatial scales and that these two components fully account for the surround. By analyzing a large population of ganglion cells, we observe substantial diversity in the relative contribution of amacrine and horizontal cell visual features while still allowing individual cells to increase information transmission under the statistics of natural scenes. Established theories of efficient coding have shown that optimal information transmission under natural scenes allows a diverse set of receptive fields. Our results give a mechanism for this theory, showing how distinct neural pathways synthesize a sensory computation and how this architecture both generates computational diversity and achieves the objective of high information transmission.

关键词： neural circuit computational model receptive field efficient coding perturbation

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Visual perception as retrospective Bayesian decoding from high- to low-level features

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 2017年第43期114卷 E9115-E9124页

作者： Ding, Stephanie Cueva, Christopher J. Tsodyks, Misha Qian, Ning Columbia Coll New York NY 10027 USA Columbia Univ Mortimer B Zuckerman Mind Brain Behav Inst New York NY 10027 USA Columbia Univ Dept Neurosci New York NY 10027 USA Weizmann Inst Sci Dept Neurobiol IL-76100 Rehovot Israel Columbia Univ Dept Physiol & Cellular Biophys New York NY 10032 USA

When a stimulus is presented, its encoding is known to progress from low- to high-level features. How these features are decoded to produce perception is less clear, and most models assume that decoding follows the same low-to high-level hierarchy of encoding. There are also theories arguing for global precedence, reversed hierarchy, or bidirectional processing, but they are descriptive without quantitative comparison with human perception. Moreover, observers often inspect different parts of a scene sequentially to form overall perception, suggesting that perceptual decoding requires working memory, yet few models consider how working-memory properties may affect decoding hierarchy. We probed decoding hierarchy by comparing absolute judgments of single orientations and relative/ordinal judgments between two sequentially presented orientations. We found that lower-level, absolute judgments failed to account for higher-level, relative/ordinal judgments. However, when ordinal judgment was used to retrospectively decode memory representations of absolute orientations, striking aspects of absolute judgments, including the correlation and forward/backward aftereffects between two reported orientations in a trial, were explained. We propose that the brain prioritizes decoding of higher-level features because they are more behaviorally relevant, and more invariant and categorical, and thus easier to specify and maintain in noisy working memory, and that more reliable higher-level decoding constrains less reliable lower-level decoding.

关键词： Bayesian prior interreport correlation bidirectional tilt aftereffect efficient coding adaptation theory

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Cochlea-scaled entropy, not consonants, vowels, or time, best predicts speech intelligibility

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 2010年第27期107卷 12387-12392页

作者： Stilp, Christian E. Kluender, Keith R. Univ Wisconsin Dept Psychol Madison WI 53706 USA

Speech sounds are traditionally divided into consonants and vowels. When only vowels or only consonants are replaced by noise, listeners are more accurate understanding sentences in which consonants are replaced but vowels remain. From such data, vowels have been suggested to be more important for understanding sentences;however, such conclusions are mitigated by the fact that replaced consonant segments were roughly one-third shorter than vowels. We report two experiments that demonstrate listener performance to be better predicted by simple psychoacoustic measures of cochlea-scaled spectral change across time. First, listeners identified sentences in which portions of consonants (C), vowels (V), CV transitions, or VC transitions were replaced by noise. Relative intelligibility was not well accounted for on the basis of Cs, Vs, or their transitions. In a second experiment, distinctions between Cs and Vs were abandoned. Instead, portions of sentences were replaced on the basis of cochlea-scaled spectral entropy (CSE). Sentence segments having relatively high, medium, or low entropy were replaced with noise. Intelligibility decreased linearly as the amount of replaced CSE increased. Duration of signal replaced and proportion of consonants/vowels replaced fail to account for listener data. CSE corresponds closely with the linguistic construct of sonority (or vowel-likeness) that is useful for describing phonological systematicity, especially syllable composition. Results challenge traditional distinctions between consonants and vowels. Speech intelligibility is better predicted by nonlinguistic sensory measures of uncertainty (potential information) than by orthodox physical acoustic measures or linguistic constructs.

关键词： auditory perception speech perception phonetics linguistics efficient coding

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Multiplicative mixing of object identity and image attributes in single inferior temporal neurons

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 2018年第14期115卷 E3276-E3285页

作者： Murty, N. Apurva Ratan Arun, S. P. Indian Inst Sci Ctr Neurosci Bangalore 560012 Karnataka India MIT McGovern Inst Brain Res 77 Massachusetts Ave Cambridge MA 02139 USA

Object recognition is challenging because the same object can produce vastly different images, mixing signals related to its identity with signals due to its image attributes, such as size, position, rotation, etc. Previous studies have shown that both signals are present in high-level visual areas, but precisely how they are combined has remained unclear. One possibility is that neurons might encode identity and attribute signals multiplicatively so that each can be efficiently decoded without interference from the other. Here, we show that, in high-level visual cortex, responses of single neurons can be explained better as a product rather than a sum of tuning for object identity and tuning for image attributes. This subtle effect in single neurons produced substantially better population decoding of object identity and image attributes in the neural population as a whole. This property was absent both in low-level vision models and in deep neural networks. It was also unique to invariances: when tested with two-part objects, neural responses were explained better as a sum than as a product of part tuning. Taken together, our results indicate that signals requiring separate decoding, such as object identity and image attributes, are combined multiplicatively in IT neurons, whereas signals that require integration (such as parts in an object) are combined additively.

关键词： object recognition invariance separability efficient coding computer vision

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Origin of information-limiting noise correlations

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 2015年第50期112卷 E6973-E6982页

作者： Kanitscheider, Ingmar Coen-Cagli, Ruben Pouget, Alexandre Univ Geneva Dept Basic Neurosci CH-1211 Geneva Switzerland Univ Texas Austin Ctr Learning & Memory Austin TX 78712 USA Univ Texas Austin Dept Neurosci Austin TX 78712 USA Univ Rochester Dept Brain & Cognit Sci Rochester NY 14627 USA UCL Gatsby Computat Neurosci Unit London W1T 4JG England

The ability to discriminate between similar sensory stimuli relies on the amount of information encoded in sensory neuronal populations. Such information can be substantially reduced by correlated trial-to-trial variability. Noise correlations have been measured across a wide range of areas in the brain, but their origin is still far from clear. Here we show analytically and with simulations that optimal computation on inputs with limited information creates patterns of noise correlations that account for a broad range of experimental observations while at same time causing information to saturate in large neural populations. With the example of a network of V1 neurons extracting orientation from a noisy image, we illustrate to our knowledge the first generative model of noise correlations that is consistent both with neurophysiology and with behavioral thresholds, without invoking suboptimal encoding or decoding or internal sources of variability such as stochastic network dynamics or cortical state fluctuations. We further show that when information is limited at the input, both suboptimal connectivity and internal fluctuations could similarly reduce the asymptotic information, but they have qualitatively different effects on correlations leading to specific experimental predictions. Our study indicates that noise at the sensory periphery could have a major effect on cortical representations in widely studied discrimination tasks. It also provides an analytical framework to understand the functional relevance of different sources of experimentally measured correlations.

关键词： noise correlations information theory neural computation efficient coding neuronal variability

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Divisive normalization is an efficient code for multivariate Pareto-distributed environments

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 2022年第40期119卷 e2120581119页

作者： Bucher, Stefan F. Brandenburger, Adam M. New York Univ Dept Econ New York NY 10012 USA Univ Tubingen Dept Comp Sci D-72076 Tubingen Germany Max Planck Inst Biol Cybernet Dept Computat Neurosci D-72076 Tubingen Germany New York Univ Stern Sch Business New York NY 10012 USA New York Univ Tandon Sch Engn Brooklyn NY 11201 USA New York Univ Shanghai Shanghai 200122 Peoples R China

Divisive normalization is a canonical computation in the brain, observed across neural systems, that is often considered to be an implementation of the efficient coding principle. We provide a theoretical result that makes the conditions under which divisive normalization is an efficient code analytically precise: We show that, in a low-noise regime, encoding an n-dimensional stimulus via divisive normalization is efficient if and only if its prevalence in the environment is described by a multivariate Pareto distribution. We generalize this multivariate analog of histogram equalization to allow for arbitrary metabolic costs of the representation, and show how different assumptions on costs are associated with different shapes of the distributions that divisive normal-ization efficiently encodes. Our result suggests that divisive normalization may have evolved to efficiently represent stimuli with Pareto distributions. We demonstrate that this efficiently encoded distribution is consistent with stylized features of naturalistic stimulus distributions such as their characteristic conditional variance dependence, and we provide empirical evidence suggesting that it may capture the statistics of filter responses to naturalistic images. Our theoretical finding also yields empirically testable predictions across sensory domains on how the divisive normalization parameters should be tuned to features of the input distribution.

关键词： divisive normalization efficient coding natural stimulus statistics histogram equalization Pareto distribution

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Somatosensory Cortex efficiently Processes Touch Located Beyond the Body

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CURRENT BIOLOGY 2019年第24期29卷 4276-+页

作者： Miller, Luke E. Fabio, Cecile Ravenda, Valeria Bahmad, Salam Koun, Eric Salemme, Romeo Luaute, Jacques Bolognini, Nadia Hayward, Vincent Farne, Alessandro Lyon Neurosci Res Ctr Integrat Multisensory Percept Act & Cognit Team CNRS U5292 INSERM U1028 16 Ave Doyen Lepine F-69676 Bron France Univ Lyon 1 43 Blvd 11 Novembre 1918 F-69100 Villeurbanne France Hosp Civils Lyon Neuroimmers 16 Ave Doyen Lepine F-69676 Bron France Sorbonne Univ ISIR 4 Pl Jussieu F-75005 Paris France Univ London Sch Adv Study Ctr Study Senses Senate HouseMalet St London WC1E 7HU England Univ Milano Bicocca Dept Psychol Bldg U61 Piazza Ateneo Nuovo I-20126 Milan Italy Univ Milano Bicocca Milan Ctr Neurosci NeuroMi Bldg U61 Piazza Ateneo Nuovo I-20126 Milan Italy IRCSS Ist Auxolog Italiano Lab Neuropsychol 28 Via G Mercalli I-20122 Milan Italy Univ Trento Ctr Mind Brain Sci 31 Corso Bettini I-38068 Rovereto Italy

The extent to which a tool is an extension of its user is a question that has fascinated writers and philosophers for centuries [1]. Despite two decades of research [2-7], it remains unknown how this could be instantiated at the neural level. To this aim, the present study combined behavior, electrophysiology and neuronal modeling to characterize how the human brain could treat a tool like an extended sensory "organ." As with the body, participants localize touches on a hand-held tool with near-perfect accuracy [7]. This behavior is owed to the ability of the somatosensory system to rapidly and efficiently use the tool as a tactile extension of the body. Using electroencephalography (EEG), we found that where a hand-held tool was touched was immediately coded in the neural dynamics of primary somatosensory and posterior parietal cortices of healthy participants. We found similar neural responses in a proprioceptively deafferented patient with spared touch perception, suggesting that location information is extracted from the rod's vibrational patterns. Simulations of mechanoreceptor responses [8] suggested that the speed at which these patterns are processed is highly efficient. A second EEG experiment showed that touches on the tool and arm surfaces were localized by similar stages of cortical processing. Multivariate decoding algorithms and cortical source reconstruction provided further evidence that early limb-based processes were repurposed to map touch on a tool. We propose that an elementary strategy the human brain uses to sense with tools is to recruit primary somatosensory dynamics otherwise devoted to the body.

关键词： touch sensorimotor efficient coding somatosensory cortex tool use embodiment extended sensing electroencephalography mechanoreceptors

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Contrast-dependent OFF-dominance in cat primary visual cortex facilitates discrimination of stimuli with natural contrast statistics

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EUROPEAN JOURNAL OF NEUROSCIENCE 2014年第12期39卷 2060-2070页

作者： Liu, Kefei Yao, Haishan Chinese Acad Sci Shanghai Inst Biol Sci Inst Neurosci Shanghai Peoples R China Chinese Acad Sci Shanghai Inst Biol Sci State Key Lab Neurosci Shanghai Peoples R China Univ Chinese Acad Sci Shanghai Peoples R China

Both theoretical and experimental studies suggest that response properties in the visual system are shaped by signals in the natural environment. Recent studies showed that, in the primary visual cortex (V1), neurons preferring light decrements (OFF stimuli) outnumber those preferring light increments (ON stimuli). However, it is not clear whether the OFF-dominance in V1 neurons is related to the contrast statistics in natural images. By analysing the distribution of negative and positive contrasts in natural images at several spatial scales, we showed that optimal coding of the natural contrast signals would lead to a contrast-dependent OFF-dominant response, with a stronger degree of OFF-dominance at a higher contrast. Using bright and dark stimuli at various contrast levels to measure the receptive fields of neurons in cat V1, we found an increasing degree of OFF-dominance of the neuronal population as the contrast was increased. By modeling receptive fields exhibiting OFF- and ON-dominance, we found that contrast-dependent OFF-dominance facilitated the discrimination of stimuli with natural contrast distribution. Thus, by matching contrast-dependent OFF-dominance to the statistics of contrast distribution in natural images, V1 neurons may better discriminate contrast information in natural scenes.

关键词： efficient coding log ON OFF ratio multi-filter linear-nonlinear model natural scenes

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Modeling Imprecision in Perception, Valuation, and Choice

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ANNUAL REVIEW OF ECONOMICS, VOL 12 2020年 12卷 579-601页

作者： Woodford, Michael Columbia Univ Dept Econ New York NY 10027 USA

Traditional decision theory assumes that people respond to the exact features of the options available to them, but observed behavior seemsmuch less precise. This review considers ways of introducing imprecision into models of economic decision making and stresses the usefulness of analogies with the way that imprecise perceptual judgments are modeled in psychophysics-the branch of experimental psychology concerned with the quantitative relationship between objective features of an observer's environment and elicited reports about their subjective appearance. It reviews key ideas from psychophysics, provides examples of the kinds of data that motivate them, and proposes lessons for economic modeling. Applications include stochastic choice, choice under risk, decoy effects in marketing, global game models of strategic interaction, and delayed adjustment of prices in response to monetary disturbances.

关键词： psychophysics efficient coding stochastic choice global games risk attitude context effect

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Acta Psychologica 2024年 248卷 104374页

作者： Ren, Xueying Libertus, Melissa E. Department of Psychology University of Pittsburgh Pittsburgh 15260 PA United States Learning Research and Development Center University of Pittsburgh Pittsburgh 15260 PA United States Center for the Neural Basis of Cognition Pittsburgh 15260 PA United States

Empirical evidence in support of a shared system for non-symbolic and symbolic number processing has been inconclusive. The current study aims to address this question in a novel way, specifically by testing whether the efficient coding principle based on co-occurrence of number symbols in natural language holds for both non-symbolic and symbolic number processing. The efficient coding principle postulates that perception is optimized when stimuli frequently co-occur in a natural environment. We hypothesized that both numerical ratios and co-occurrence frequencies of symbolic numbers would significantly influence participants' performance on a non-symbolic and symbolic number comparison task. To test this hypothesis, we employed latent semantic analysis on a TASA corpus to quantify number co-occurrence in natural language and calculate language similarity estimates. We engaged 73 native English speakers (mean age = 19.36, standard deviation = 1.83) with normal or corrected vision and no learning disorders in a number comparison task involving non-symbolic (dot arrays) and symbolic stimuli (Arabic numerals and English number words). Results showed that numerical ratios significantly predicted participants' performances across all number formats (ps < 0.001). Language similarity estimates derived from everyday language also predicted performance on the non-symbolic task and the symbolic task involving number words (ps < 0.007). Our results highlight the complex nature of numerical processing, pointing to the co-occurrence of number symbols in natural language as an auxiliary factor in understanding the shared characteristics between non-symbolic and symbolic number representations. Given that our study focused on a limited number range (5 to 16) and a specific task type, future studies should explore a wider range of tasks and numbers to further test the role of the efficient coding principle in number processing. © 2024 The Authors

关键词： efficient coding Non-symbolic number Numerical cognition Symbolic number Vector space model

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