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Variance as a Signature of Neural Computations during Decision Making
Open accessAbstract
Traditionally, insights into neural computation have been furnished by averaged firing rates from many stimulus repetitions or trials. We pursue an analysis of neural response variance to unveil neural computations that cannot be discerned from measures of average firing rate. We analyzed single-neuron recordings from the lateral intraparietal area (LIP), during a perceptual decision-making task. Spike count variance was divided into two components using the law of total variance for doubly stochastic processes: (1) variance of counts that would be produced by a stochastic point process with a given rate, and loosely (2) the variance of the rates that would produce those counts (i.e., "conditional expectation"). The variance and correlation of the conditional expectation exposed several neural mechanisms: mixtures of firing rate states preceding the decision, accumulation of stochastic "evidence" during decision formation, and a stereotyped response at decision end. These analyses help to differentiate among several alternative decision-making models.
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“When VarCE is calculated from residuals (5, 51) (Materials and Methods), it is similar (Fig. 4G, black) showing linear increase between decision onset (Fig. 4G, up arrow) and decision termination (Fig. 4G, down arrow) times.”
From Neural correlates of perceptual decision-making in the primary somatosensory cortex (2026) · cites this paper as [51]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Analysis of spike count noise during this period showed characteristic linear increase in internally driven spike rate variability (VarCE) and decrease of its correlations (CorCE) consistent with the gradual accumulation models of decision-making (51).”
From Neural correlates of perceptual decision-making in the primary somatosensory cortex (2026) · cites this paper as [51]
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In the citing paper
“indicating accumulation of stochastic trial-by-trial diffusion noise (5, 51).”
From Neural correlates of perceptual decision-making in the primary somatosensory cortex (2026) · cites this paper as [51]
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“An important diagnostic signature of perceptual decision-making is the gradual accumulation of noise (5, 51) expected for most accumulation-to-bound decision models.”
From Neural correlates of perceptual decision-making in the primary somatosensory cortex (2026) · cites this paper as [51]
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“Total variance of this doubly stochastics process becomes a sum of two separate components (51) (Materials and Methods): PPV, proportional to mean spike rates, and variance of conditional expectation (VarCE), reflecting variance of rates.”
From Neural correlates of perceptual decision-making in the primary somatosensory cortex (2026) · cites this paper as [51]
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“It has been argued (51) that if the variance of spike rates during evidence accumulation is defined by a diffusion process, then expectation of spike counts in consecutive time bins (CorCE) should covary.”
From Neural correlates of perceptual decision-making in the primary somatosensory cortex (2026) · cites this paper as [51]
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“The calculated (Materials and Methods) CorCE matrix (Fig. 4J) indeed exhibits characteristic increase of correlation as a function of time and, for given time (e.g., along the top row), shows sequential decay as often observed (5, 51) during decision-making.”
From Neural correlates of perceptual decision-making in the primary somatosensory cortex (2026) · cites this paper as [51]
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“Overall, VarCE exhibits a linear increase during epoch 4, a characteristic signature of diffusion process consistent with an accumulation-to-bound model (5, 51).”
From Neural correlates of perceptual decision-making in the primary somatosensory cortex (2026) · cites this paper as [51]
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Citations
Cites
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“Lastly, we consider a recurrent neural network that is exemplary of a class of dynamical ‘‘attractor’’ models of decision making (e.g., Albantakis and Deco, 2009; Bogacz et al., 2006; Machens et al., 2005; Usher and McClelland, 2001; Wang, 2002).”
Self-citationNeural Control of Voluntary Movement Initiation
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“For example, the rise of mean firing rates to a threshold value could imply preparation for a saccadic eye movement (Hanes and Schall, 1996).”
BackgroundStimulus onset quenches neural variability: A widespread cortical phenomenon
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“An extension to the cross correlation of firing rates (or spike cross-correlogram) is another potentially useful extension, especially when the rate is changing in time and from trial to trial (Aertsen et al., 1989; Vaadia et al., 1995).”
BackgroundPsychology and neurobiology of simple decisions
Smith, P. L., & Ratcliff, R. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.01.006 · Cited by 1,051 · cited 2×
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“These values approximate the average firing rate of a population of weakly correlated MT neurons to 0% coherent motion in a 10 ms sample (Britten et al., 1996).”
BackgroundSelf-citationErratum: Cognitive neuroscience: new kids on the block?
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“All models were parameterized to approximate the firing rates of LIP neurons in Churchland et al. (2008).”
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“…near independence from conditions affecting the mean firing rate, such as motion strength, contrast, and attentional state (Britten et al., 1993; Geisler et al., 2001; McAdams and Maunsell, 1999; Tolhurst et al., 1983), imply that f is unlikely to vary systematically as a function of firing rate.”
BackgroundNeural computation of log likelihood in control of saccadic eye movements
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“The monkeys’ choices and RTs on this and similar tasks suggest that the decision is based on the accumulation of noisy samples of evidence (Bogacz et al., 2006; Gold and Shadlen, 2007; Ratcliff and Rouder, 1998).”
BackgroundInfluentialDynamics of neuronal interactions in monkey cortex in relation to behavioural events
Vaadia, E., Haalman, I., Abeles, M., Bergman, H., Prut, Y., Slovin, H., & Aertsen, A. (1995) · Nature · doi:10.1038/373515a0 · Cited by 802 · cited 1×
“An extension to the cross correlation of firing rates (or spike cross-correlogram) is another potentially useful extension, especially when the rate is changing in time and from trial to trial (Aertsen et al., 1989; Vaadia et al., 1995).”
BackgroundSENSE AND THE SINGLE NEURON: Probing the Physiology of Perception
Parker, A. J., & Newsome, W. T. (1998) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.21.1.227 · Cited by 801 · cited 2×
“Together, the mean and variance of neural responses furnish rich insight into the limits of perception, motor control and decision making (Faisal et al., 2008; Glimcher, 2005; Parker and Newsome, 1998; Shadlen and Newsome, 1998).”
BackgroundDecision-making with multiple alternatives
Churchland, A. K., Kiani, R., & Shadlen, M. N. (2008) · Nature Neuroscience · doi:10.1038/nn.2123 · Cited by 671
Self-citationProbabilistic population codes for Bayesian decision making
Beck, J. M., Ma, W. J., Kiani, R., Hanks, T., Churchland, A. K., Roitman, J., Shadlen, M. N., Latham, P. E., & Pouget, A. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.021 · Cited by 645 · cited 5×
“Some features of the PPC are very similar to the DDM: firing rates of LIP neurons are produced by a mixture of deterministic and stochastic components, and independent samples of evidence from noisy, direction selective neurons are effectively summed at each time step.”
MethodInfluentialSelf-citationResponses of neurons in macaque MT to stochastic motion signals
Britten, K. H., Shadlen, M. N., Newsome, W. T., & Movshon, J. A. (1993) · Visual Neuroscience · doi:10.1017/s0952523800010269 · Cited by 594 · cited 3×
“…mean spike count and its near independence from conditions affecting the mean firing rate, such as motion strength, contrast, and attentional state (Britten et al., 1993; Geisler et al., 2001; McAdams and Maunsell, 1999; Tolhurst et al., 1983), imply that f is unlikely to vary systematically as a…”
BackgroundSelf-citationDecisions in Changing Conditions: The Urgency-Gating Model
Cisek, P., Puskas, G. A., & El-Murr, S. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1844-09.2009 · Cited by 541 · cited 3×
“All motion strengths are included (7008 trials). representation of noisy momentary evidence, without appreciable integration (Cisek et al., 2009), possibly related to agradual shift of attention to a choice target (Gottlieb and Balan, 2010).”
BackgroundHuk, A. C., & Shadlen, M. N. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.4684-04.2005 · Cited by 538 · cited 2×
“By perturbing the background of random dot motion displays, Huk and Shadlen (2005) demonstrated that LIP neurons represent the integral of motion evidence in the display, but thesemeasurements did not demonstrate that spike trains from individual trials represent realizations of random walk or…”
BackgroundSelf-citationFlexible control of mutual inhibition: a neural model of two-interval discrimination
Machens, C. K., Romo, R., & Brody, C. D. (2005) · Science · doi:10.1126/science.1104171 · Cited by 535 · cited 1×
“Lastly, we consider a recurrent neural network that is exemplary of a class of dynamical ‘‘attractor’’ models of decision making (e.g., Albantakis and Deco, 2009; Bogacz et al., 2006; Machens et al., 2005; Usher and McClelland, 2001; Wang, 2002).”
MethodNeural Variability in Premotor Cortex Provides a Signature of Motor Preparation
Churchland, M. M., Yu, B. M., Ryu, S. I., Santhanam, G., & Shenoy, K. V. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3762-05.2006 · Cited by 491 · cited 2×
“For example, in dorsal premotor cortex, neural variability decreases gradually until the monkey’s movement, sometimes over a period as long as 400 ms (Churchland et al., 2006).”
BackgroundModulation of Neuronal Activity in Superior Colliculus by Changes in Target Probability
Basso, M. A., & Wurtz, R. H. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-18-07519.1998 · Cited by 474 · cited 2×
“The lower average rate is probably not explained by amechanism that invokes less excitation or greater suppression on all trials, owing perhaps to greater uncertainty (Basso and Wurtz, 1998), or normalization (Tolhurst and Heeger, 1997), or surround inhibition (Balan et al., 2008).”
BackgroundRetinal Noise and Absolute Threshold
Barlow, H. B. (1956) · Journal of the Optical Society of America · doi:10.1364/josa.46.000634 · Cited by 433 · cited 2×
“during Decision Making”
BackgroundVere-Jones, D. (2011) · International Encyclopedia of Statistical Science · doi:10.1007/978-3-642-04898-2_447 · Cited by 433 · cited 1×
“A constant VarCE is still evident when the firing rate is perturbed by additive noise, as in a doubly stochastic Poisson process (Figure 2D and magenta lines in Figure 2F), also known as a Cox process (Cox and Isham, 1980).”
MethodRefractoriness and Neural Precision
Berry, M. J., & Meister, M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-06-02200.1998 · Cited by 402
Keat, J., Reinagel, P., Reid, R. C., & Meister, M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00322-1 · Cited by 328 · cited 1×
“A Poisson process with refractoriness ensures f < 1 (Berry and Meister, 1998; Keat et al., 2001).”
MethodEffects of Attention on the Reliability of Individual Neurons in Monkey Visual Cortex
McAdams, C. J., & Maunsell, J. H. R. (1999) · Neuron · doi:10.1016/s0896-6273(01)80034-9 · Cited by 286 · cited 1×
“…near independence from conditions affecting the mean firing rate, such as motion strength, contrast, and attentional state (Britten et al., 1993; Geisler et al., 2001; McAdams and Maunsell, 1999; Tolhurst et al., 1983), imply that f is unlikely to vary systematically as a function of firing rate.”
BackgroundTouch and Go: Decision-Making Mechanisms in Somatosensation
Romo, R., & Salinas, E. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.107 · Cited by 262 · cited 2×
“For example, responses of neurons in primary somatosensory cortex lay the foundation for understanding vibrotactile sensation because mean firing rates are significantly higher for more intense tactile stimuli (Romo and Salinas, 2001).”
BackgroundBeyond Poisson: Increased Spike-Time Regularity across Primate Parietal Cortex
Maimon, G., & Assad, J. A. (2009) · Neuron · doi:10.1016/j.neuron.2009.03.021 · Cited by 230 · cited 1×
“These are conditions in which we would expect the VarCE to be minimal, and the same holds for LIP neurons when rates are relatively stationary, as in the delay period preceding a saccade to one target or during the late predecision period (cf. Maimon and Assad, 2009).”
BackgroundAccuracy, Information, and Response Time in a Saccadic Decision Task
Reddi, B. A. J., Asrress, K. N., & Carpenter, R. H. S. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00689.2002 · Cited by 217 · cited 2×
“This model would also explain decisions using competing mechanisms (Reddi et al., 2003), although we did not implement this.”
BackgroundFractal character of the neural spike train in the visual system of the cat
Teich, M. C., Heneghan, C., Lowen, S. B., Ozaki, T., & Kaplan, E. (1997) · Journal of the Optical Society of America A · doi:10.1364/josaa.14.000529 · Cited by 208 · cited 1×
“Other violations of the renewallike assumption are characterized in Teich et al. (1997), although we suspect some are simply manifestations of VarCE and less exotic than these authors propose.”
BackgroundMeasurement of variability dynamics in cortical spike trains
Nawrot, M. P., Boucsein, C., Molina, V., Riehle, A., Aertsen, A., & Rotter, S. (2007) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2007.10.013 · Cited by 206 · cited 1×
“Other violations of the renewallike assumption are characterized in Teich et al. (1997), although we suspect some are simply manifestations of VarCE and less exotic than these authors propose.”
BackgroundIndeterminacy in brain and behavior
Glimcher, P. W. (2005) · Annual Review of Psychology · doi:10.1146/annurev.psych.55.090902.141429 · Cited by 206 · cited 2×
“Together, the mean and variance of neural responses furnish rich insight into the limits of perception, motor control and decision making (Faisal et al., 2008; Glimcher, 2005; Parker and Newsome, 1998; Shadlen and Newsome, 1998).”
BackgroundWong, K.-F. (2007) · Frontiers in Computational Neuroscience · doi:10.3389/neuro.10.006.2007 · Cited by 204 · cited 3×
“Here, we used a simplified firing-rate version of such a model (Wong et al., 2007).”
BackgroundMethodInfluentialSimilarity Effect and Optimal Control of Multiple-Choice Decision Making
Furman, M., & Wang, X. (2008) · Neuron · doi:10.1016/j.neuron.2008.12.003 · Cited by 147
Self-citationMotion direction signals in the primary visual cortex of cat and monkey
Geisler, W. S., Albrecht, D. G., Crane, A. M., & STERN, L. (2001) · Visual Neuroscience · doi:10.1017/s0952523801184014 · Cited by 133 · cited 2×
“…near independence from conditions affecting the mean firing rate, such as motion strength, contrast, and attentional state (Britten et al., 1993; Geisler et al., 2001; McAdams and Maunsell, 1999; Tolhurst et al., 1983), imply that f is unlikely to vary systematically as a function of firing…”
BackgroundAttention as a decision in information space
Gottlieb, J. P., & Balan, P. F. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.03.001 · Cited by 125 · cited 3×
“All motion strengths are included (7008 trials). representation of noisy momentary evidence, without appreciable integration (Cisek et al., 2009), possibly related to agradual shift of attention to a choice target (Gottlieb and Balan, 2010).”
BackgroundGeisler, W. S., & Albrecht, D. G. (1995) · Vision Research · doi:10.1016/0042-6989(95)00029-y · Cited by 105 · cited 1×
“There is an approximately linear relationship between the mean and variance of the spike counts for neurons in several cortical areas for repetitions of identical stimuli (Britten et al., 1993; Churchland et al., 2006; Geisler and Albrecht, 1995;McAdams andMaunsell, 1999).”
BackgroundTolhurst, D. J., & Heeger, D. J. (1997) · Visual Neuroscience · doi:10.1017/s0952523800011433 · Cited by 99 · cited 2×
“The lower average rate is probably not explained by amechanism that invokes less excitation or greater suppression on all trials, owing perhaps to greater uncertainty (Basso and Wurtz, 1998), or normalization (Tolhurst and Heeger, 1997), or surround inhibition (Balan et al., 2008).”
BackgroundNeuronal correlates of the set-size effect in monkey lateral intraparietal area
Balan, P. F., Oristaglio, J., Schneider, D. M., & Gottlieb, J. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060158 · Cited by 83 · cited 1×
“The lower average rate is probably not explained by amechanism that invokes less excitation or greater suppression on all trials, owing perhaps to greater uncertainty (Basso and Wurtz, 1998), or normalization (Tolhurst and Heeger, 1997), or surround inhibition (Balan et al., 2008).”
BackgroundThe encoding of alternatives in multiple-choice decision making
Albantakis, L., & Deco, G. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901621106 · Cited by 66
Power-Law Neuronal Fluctuations in a Recurrent Network Model of Parametric Working Memory
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Self-citationNoise and the Visual Threshold
Bulmer, M. G., & Howarth, C. (1957) · Nature · doi:10.1038/1801403a0 · Cited by 17 · cited 1×
“It follows that the variability of firing rate across repetitions might bear on the fidelity of these neural signals (Barlow, 1956; Bulmer et al., 1957; Tolhurst et al., 1983).”
BackgroundThe encoding of alternatives in multiple-choice decision-making
Albantakis, L., & Deco, G. (2009) · BMC Neuroscience · doi:10.1186/1471-2202-10-s1-p166 · Cited by 12 · cited 1×
“Lastly, we consider a recurrent neural network that is exemplary of a class of dynamical ‘‘attractor’’ models of decision making (e.g., Albantakis and Deco, 2009; Bogacz et al., 2006; Machens et al., 2005; Usher and McClelland, 2001; Wang, 2002).”
Method
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Sorted by citations
Diffusion decision model: Current issues and history
Ratcliff, R., Smith, P. L., Brown, S. D., & McKoon, G. (2016) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2016.01.007 · Cited by 1,630
“Many studies have assumed that the decision system accumulates the noisy output of a motion discrimination system, in which the noise arises from variability in the stimulus sequence (following [88,99]).”
BackgroundNeuronal Reward and Decision Signals: From Theories to Data
Schultz, W. (2015) · Physiological Reviews · doi:10.1152/physrev.00023.2014 · Cited by 1,126
“The statistical variance of neuronal activity in LIP increases gradually and declines earlier for one option compared with the other option immediately before the action (96).”
BackgroundA hierarchy of intrinsic timescales across primate cortex
Murray, J. D., Bernacchia, A., Freedman, D. J., Romo, R., Wallis, J. D., Cai, X., Padoa-Schioppa, C., Pasternak, T., Seo, H., Lee, D., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3862 · Cited by 990
Self-citationChanging concepts of working memory
Ma, W. J., Husain, M., & Bays, P. M. (2014) · Nature Neuroscience · doi:10.1038/nn.3655 · Cited by 1,208
Decision Making as a Window on Cognition
Shadlen, M. N., & Kiani, R. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.047 · Cited by 694
Self-citation
Metadata
- Authors
- Churchland, A. K., Kiani, R., Chaudhuri, R., Wang, X.-J., Pouget, A., & Shadlen, M. N.
- Affiliations
- University of Washington (US)
- Howard Hughes Medical Institute (US)
- Yale University (US)
- University of Rochester (US)
- Corresponding author
- Churchland, Anne. K.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2011-02
- Volume
- 69
- Issue
- 4
- Pages
- 818-831
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3066020
- OpenAlex
- W2105007656
- Cited by
- 350
- References
- 56
- Citations by year
- 2026: 7 · 2025: 19 · 2024: 27 · 2023: 15 · 2022: 20 · 2021: 25 · 2020: 21 · 2019: 20 · 2018: 20 · 2017: 22 · 2016: 30 · 2015: 35 · 2014: 28 · 2013: 20 · 2012: 33
- FWCI
- 14.30
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- James S. McDonnell Foundation (P30 EY001319)
- National Institutes of Health (RR001 66, EY001319)
- U.S. Public Health Service (BCS0346785)
- Multidisciplinary University Research Initiative (N00014-07-1-0937)
- National Institute of Mental Health (MH 062349, R01MH062349)
- National Institute on Drug Abuse (DA022780, R01DA022780)
- National Eye Institute (EY011378, EY019072, R00EY019072, K99EY019072, R01EY011378, P30EY001319)
- National Center for Research Resources (RR00166, P51RR000166)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- perceptual decision making, lateral intraparietal area, law of total variance, doubly stochastic processes, conditional expectation, single-unit recording, decision models
- MeSH terms
- Action Potentials, Animals, Haplorhini, Computer Simulation, Decision Making, Models, Neurological, Motion Perception, Neurons, Numerical Analysis, Computer-Assisted, Photic Stimulation, Reaction Time, Statistics as Topic, Stochastic Processes, Time Factors
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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