Decision-related signals in the presence of nonzero signal stimuli, internal bias, and feedback

Understanding the nature of decision-related signals in sensory neurons promises to give insights into their role in perceptual decision-making. Those signals, traditionally quantified as choice probabilities (CP), are well-understood in a feedforward framework assuming zero-signal trials with no choice bias. Here, we extend this understanding by analytically solving models of choice-related signals that account for informative stimuli, choice bias, and importantly, feedback signals reflecting either internal states, such as attention or belief, or the outcome of the decision process. First, we relate CPs to Choice Triggered Averages (CTAs), which quantify choice-related average changes in neural responses, and show that both have general expressions valid for activity-choice covariations of both feedforward or feedback origin. These expressions allow a meaningful calculation of CPs across all trials, including non-zero signal trials. Second, we derive how CPs and CTAs depend on feedforward and feedback weights and on noise correlations under several plausible model architectures. Third, we examine different types of feedback signals, related to predictive coding, probabilistic inference, and attention, and we predict how CPs and CTAs depend in each case on the stimulus signal level and on the neural tuning properties. Finally, we show that measuring both CPs and CTAs offers complementary information about the origin of choice-related signals, especially when studying temporal changes of activity-choice covariations across the trial time. Overall, our work provides new analytical tools to better understand the link between sensory representations and perceptual decisions.

[1]  Pieter R Roelfsema,et al.  Belief states as a framework to explain extra-retinal influences in visual cortex , 2015, Current Opinion in Neurobiology.

[2]  A. Borst Seeing smells: imaging olfactory learning in bees , 1999, Nature Neuroscience.

[3]  Katherine E. Conen,et al.  Neuronal variability in orbitofrontal cortex during economic decisions. , 2015, Journal of neurophysiology.

[4]  W. Newsome,et al.  Estimates of the Contribution of Single Neurons to Perception Depend on Timescale and Noise Correlation , 2009, The Journal of Neuroscience.

[5]  Bruce G Cumming,et al.  Decision-related activity in sensory neurons: correlations among neurons and with behavior. , 2012, Annual review of neuroscience.

[6]  Wolfgang Maass,et al.  Neural Dynamics as Sampling: A Model for Stochastic Computation in Recurrent Networks of Spiking Neurons , 2011, PLoS Comput. Biol..

[7]  G. DeAngelis,et al.  How Can Single Sensory Neurons Predict Behavior? , 2015, Neuron.

[8]  D. Owen Tables for Computing Bivariate Normal Probabilities , 1956 .

[9]  R. Romo,et al.  Neural codes for perceptual discrimination in primary somatosensory cortex , 2005, Nature Neuroscience.

[10]  Bruce Cumming,et al.  Correlations between the activity of sensory neurons and behavior: how much do they tell us about a neuron's causality? , 2010, Current Opinion in Neurobiology.

[11]  Eero P. Simoncelli,et al.  Partitioning neuronal variability , 2014, Nature Neuroscience.

[12]  J. Maunsell,et al.  Effects of Stimulus Direction on the Correlation between Behavior and Single Units in Area MT during a Motion Detection Task , 2011, The Journal of Neuroscience.

[13]  P. Berkes,et al.  Statistically Optimal Perception and Learning: from Behavior to Neural Representations , 2022 .

[14]  J. Gold,et al.  Neural computations that underlie decisions about sensory stimuli , 2001, Trends in Cognitive Sciences.

[15]  M. Shadlen,et al.  Representation of Confidence Associated with a Decision by Neurons in the Parietal Cortex , 2009, Science.

[16]  Eero P. Simoncelli,et al.  Attention stabilizes the shared gain of V4 populations , 2015, eLife.

[17]  Bingni W. Brunton,et al.  Rats and Humans Can Optimally Accumulate Evidence for Decision-Making , 2013, Science.

[18]  Timothy D. Hanks,et al.  Bounded Integration in Parietal Cortex Underlies Decisions Even When Viewing Duration Is Dictated by the Environment , 2008, The Journal of Neuroscience.

[19]  John H R Maunsell,et al.  Potential confounds in estimating trial-to-trial correlations between neuronal response and behavior using choice probabilities. , 2012, Journal of neurophysiology.

[20]  A. Azzalini A class of distributions which includes the normal ones , 1985 .

[21]  J. Macke,et al.  Quantifying the effect of intertrial dependence on perceptual decisions. , 2014, Journal of vision.

[22]  Thomas J. Anastasio,et al.  Using Bayes' Rule to Model Multisensory Enhancement in the Superior Colliculus , 2000, Neural Computation.

[23]  Bruce G Cumming,et al.  Feedforward and Feedback Sources of Choice Probability in Neural Population Responses This Review Comes from a Themed Issue on Neurobiology of Cognitive Behavior Evidence for Feed-forward Models and Optimal Linear Readout? , 2022 .

[24]  W. Newsome,et al.  Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  Ralf M. Haefner,et al.  A Modality-Specific Feedforward Component of Choice-Related Activity in MT , 2015, Neuron.

[26]  B. Cumming,et al.  Decision-related activity in sensory neurons reflects more than a neuron’s causal effect , 2009, Nature.

[27]  Timothée Masquelier,et al.  Neural variability, or lack thereof , 2013, Front. Comput. Neurosci..

[28]  Alexander S. Ecker,et al.  On the Structure of Neuronal Population Activity under Fluctuations in Attentional State , 2015, The Journal of Neuroscience.

[29]  John H. R. Maunsell,et al.  Feature-based attention in visual cortex , 2006, Trends in Neurosciences.

[30]  Jonathan W. Pillow,et al.  Dissociated functional significance of decision-related activity in the primate dorsal stream , 2016, Nature.

[31]  Alexander S. Ecker,et al.  State Dependence of Noise Correlations in Macaque Primary Visual Cortex , 2014, Neuron.

[32]  Peter Dayan,et al.  Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems , 2001 .

[33]  Hang-Hyun Jo,et al.  Tail-scope: Using friends to estimate heavy tails of degree distributions in large-scale complex networks , 2014, Scientific Reports.

[34]  Hideyuki Suzuki,et al.  Population Code Dynamics in Categorical Perception , 2016, Scientific Reports.

[35]  C. Padoa-Schioppa Neuronal Origins of Choice Variability in Economic Decisions , 2013, Neuron.

[36]  J. Gold,et al.  The neural basis of decision making. , 2007, Annual review of neuroscience.

[37]  Wei Ji Ma,et al.  Bayesian inference with probabilistic population codes , 2006, Nature Neuroscience.

[38]  A note on choice and detect probabilities in the presence of choice bias , 2015, 1501.03173.

[39]  M. Bethge,et al.  Inferring decoding strategies from choice probabilities in the presence of correlated variability , 2013, Nature Neuroscience.

[40]  József Fiser,et al.  Perceptual Decision-Making as Probabilistic Inference by Neural Sampling , 2014, Neuron.

[41]  A. Parker,et al.  Sense and the single neuron: probing the physiology of perception. , 1998, Annual review of neuroscience.

[42]  Karen R Dobkins,et al.  The face inversion effect in infants is driven by high, and not low, spatial frequencies. , 2014, Journal of vision.

[43]  J. Maunsell,et al.  Attention improves performance primarily by reducing interneuronal correlations , 2009, Nature Neuroscience.

[44]  Bagrat Amirikian,et al.  Directional tuning profiles of motor cortical cells , 2000, Neuroscience Research.

[45]  Tai Sing Lee,et al.  Hierarchical Bayesian inference in the visual cortex. , 2003, Journal of the Optical Society of America. A, Optics, image science, and vision.

[46]  Jude F. Mitchell,et al.  Spatial Attention Decorrelates Intrinsic Activity Fluctuations in Macaque Area V4 , 2009, Neuron.

[47]  K. H. Britten,et al.  A relationship between behavioral choice and the visual responses of neurons in macaque MT , 1996, Visual Neuroscience.

[48]  N. Parga,et al.  An Optimal Decision Population Code that Accounts for Correlated Variability Unambiguously Predicts a Subject’s Choice , 2013, Neuron.

[49]  Anthony J. Movshon,et al.  Optimal representation of sensory information by neural populations , 2006, Nature Neuroscience.

[50]  J. Movshon,et al.  A computational analysis of the relationship between neuronal and behavioral responses to visual motion , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.