Neural correlates of reliability-based cue weighting during multisensory integration

Journal name:
Nature Neuroscience
Volume:
15,
Pages:
146–154
Year published:
DOI:
doi:10.1038/nn.2983
Received
Accepted
Published online
Corrected online

Abstract

Integration of multiple sensory cues is essential for precise and accurate perception and behavioral performance, yet the reliability of sensory signals can vary across modalities and viewing conditions. Human observers typically employ the optimal strategy of weighting each cue in proportion to its reliability, but the neural basis of this computation remains poorly understood. We trained monkeys to perform a heading discrimination task from visual and vestibular cues, varying cue reliability randomly. The monkeys appropriately placed greater weight on the more reliable cue, and population decoding of neural responses in the dorsal medial superior temporal area closely predicted behavioral cue weighting, including modest deviations from optimality. We found that the mathematical combination of visual and vestibular inputs by single neurons is generally consistent with recent theories of optimal probabilistic computation in neural circuits. These results provide direct evidence for a neural mechanism mediating a simple and widespread form of statistical inference.

At a glance

Figures

  1. Cue-conflict configuration and example behavioral session.
    Figure 1: Cue-conflict configuration and example behavioral session.

    (a) Monkeys were presented with visual (optic flow) and/or vestibular (inertial motion) heading stimuli in the horizontal plane. The heading (θ) was varied in fine steps around straight ahead, and the task was to indicate rightward or leftward heading with a saccade after each trial. On a subset of visual-vestibular (combined) trials, the headings specified by each cue were separated by a conflict angle (Δ) of ±4°, where positive Δ indicates visual to the right of vestibular, and vice versa for negative Δ. Schematic shows two possible combinations of θ and Δ. (b) Psychometric functions for an example session showing the proportion of rightward choices as a function of heading for the single-cue conditions. Psychophysical thresholds were taken as the s.d. (σ) of the best-fitting cumulative Gaussian function (smooth curves) for each modality. Single-cue thresholds were used to predict (via equation (2)), the weights that an optimal observer should assign to each cue during combined trials. (c) Psychometric functions for the combined modality at low (16%) coherence, plotted separately for each value of Δ. The shifts of the PSEs during cue-conflict were used to compute observed vestibular weights (equation (4)). (d) Data are presented as in c, but for the high (60%) coherence combined trials.

  2. Average behavioral performance.
    Figure 2: Average behavioral performance.

    (a,b) Optimal (equation (2), open symbols and dashed line) and observed (equation (4), filled symbols and solid line) vestibular weights as a function of visual motion coherence (cue reliability), shown separately for the two monkeys (a, monkey Y, N = 40 sessions; b, monkey W, N = 26). (c,d) Optimal (equation (3)) and observed (estimated from the psychometric fits) psychophysical thresholds, normalized separately by each monkey's vestibular threshold. Error bars represent 95% confidence intervals computed with a bootstrap procedure.

  3. Example MSTd neuron showing a correlate of trial-by-trial cue reweighting.
    Figure 3: Example MSTd neuron showing a correlate of trial-by-trial cue reweighting.

    (ac) Mean firing rate (spikes per s) ± s.e.m. is plotted as a function of heading for the single-cue trials (a), and combined trials at low (b) and high (c) coherence. The shift in combined tuning curves with cue conflict, in opposite directions for the two levels of reliability, forms the basis for the reweighting effects in the population decoding analysis depicted in Figures 4 and 6 (see Supplementary Figs. 1 and 2 for single-cell neurometric analyses).

  4. Likelihood-based decoding approach used to simulate behavioral performance based on MSTd activity.
    Figure 4: Likelihood-based decoding approach used to simulate behavioral performance based on MSTd activity.

    (a,b) Example likelihood functions (P(r|θ)) for the single-cue modalities. Four individual trials of the same heading (θ = 1.2°, green arrow) are superimposed for each condition. Likelihoods were computed from equation (14) using simulated population responses (r) comprised of random draws of single-neuron activity. (c) Simulated psychometric functions for a decoded population that included all 108 MSTd neurons in our sample. (d,e) Combined modality likelihood functions for θ = 1.2° (green arrow and dashed line) and Δ = +4°, for low (cyan) and high (blue) coherence. Black and red inverted triangles indicate the headings specified by vestibular and visual cues, respectively, in this stimulus configuration. (f) Psychometric functions for the simulated combined modality, showing the shift in the PSE resulting from the change in coherence (that is, reweighting).

  5. Visual-vestibular congruency and average MSTd tuning curves.
    Figure 5: Visual-vestibular congruency and average MSTd tuning curves.

    (a) Histogram of congruency index (CI) values for monkey Y (top), monkey W (middle) and both animals together (bottom). Positive congruency index values indicate consistent tuning slope across visual (60% coh) and vestibular single-cue conditions, whereas negative values indicate opposite tuning slopes. Filled bars indicate congruency index values whose constituent correlation coefficients were both statistically significant11; however, here we defined congruent and opposite cells by an arbitrary criterion of congruency index > 0.4 and congruency index < −0.4, respectively. (b,c) Population average of MSTd tuning curves for the five stimulus conditions, vestibular (black), low-coherence visual (magenta, dashed), high-coherence visual (red), low-coherence combined (cyan, dashed) and high-coherence combined (blue), separated into congruent (b) and opposite (c) classes. Prior to averaging, some neurons' tuning preferences were mirrored such that all cells preferred rightward heading in the high-coherence visual modality.

  6. Population decoding results and comparison with monkey behavior.
    Figure 6: Population decoding results and comparison with monkey behavior.

    (af) Weights (left column, data are presented as in Fig. 2a,b; from equation (2) and (4)) and thresholds (right column, data presented as in Fig. 2c,d; from equation (3) and psychometric fits to real or simulated choice data) quantifying the performance of an optimal observer reading out MSTd population activity. Thresholds were normalized by the value of the vestibular threshold. The population of neurons included in the decoder was varied to examine the readout of all cells (a,b), opposite cells only (c,d; note the different ordinate scale in d) or congruent cells only (e,f). (g,h) Monkey behavioral performance (pooled across the two animals) is summarized. Error bars indicate 95% confidence intervals.

  7. Goodness-of-fit of linear weighted sum model and distribution of vestibular and visual neural weights.
    Figure 7: Goodness-of-fit of linear weighted sum model and distribution of vestibular and visual neural weights.

    Combined responses during the discrimination task (N = 108) were modeled as a weighted sum of visual and vestibular responses, separately for each coherence level (equation (5)). (a,b) Histograms of a goodness-of-fit metric (R2), taken as the square of the correlation coefficient between the modeled response and the real response. The statistical significance of this correlation was used to code the R2 histograms. (c,d) Histograms of vestibular (c) and visual (d) neural weights, separated by coherence (gray bars = 16%, black bars = 60%). Color-matched arrowheads indicate medians of the distributions. Only neurons with significant R2 values for both coherences were included (N = 83).

  8. Comparison of optimal and actual (fitted) neural weights.
    Figure 8: Comparison of optimal and actual (fitted) neural weights.

    (a) Actual weight ratios (Aves/Avis) for each cell were derived from the best-fitting linear model (equation (5), as in Fig. 7), and optimal weight ratios (ρopt) for the corresponding cells were computed according to equation (7). Symbol color indicates coherence (16%, blue; 60%, red) and shape indicates monkey identity. Note that the derivation of equation (7) assumes congruent tuning (see Supplementary Analysis), and ρopt is therefore constrained to be positive (because the sign of the tuning slopes will be equal). Thus, only congruent cells with positive weight ratios were included in this comparison (N = 36 for low coherence, 37 for high coherence). (b,d) Decoder performance (data are presented as in Figure 6, using equation (2)–(4) and fits to simulated choice data) based on congruent neurons, after replacing combined modality responses with weighted sums of single-cue responses, using the optimal weights from equation (7) (abscissa in a). (c,e) Data are presented as in b and c, using the actual (fitted) weights (ordinate in a) to generate the artificial combined responses.

Change history

Corrected online 03 April 2013
In the version of this article initially published, there were typographical errors in the numerators of equations (12) and (13). The terms μcomb in equation (12) and PSEvis in equation (13) were preceded by plus signs; the correct equations contain minus signs in those locations. The errors have been corrected in the HTML and PDF versions of the article.

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Author information

  1. These authors contributed equally to this work.

    • Gregory C DeAngelis &
    • Dora E Angelaki

Affiliations

  1. Department of Anatomy and Neurobiology, Washington University School of Medicine, Saint Louis, Missouri, USA.

    • Christopher R Fetsch,
    • Gregory C DeAngelis &
    • Dora E Angelaki
  2. Department of Brain and Cognitive Sciences, University of Rochester, Rochester, New York, USA.

    • Alexandre Pouget &
    • Gregory C DeAngelis
  3. Department of Basic Neuroscience, University of Geneva, Geneva, Switzerland.

    • Alexandre Pouget
  4. Department of Neuroscience, Baylor College of Medicine, Houston, Texas, USA.

    • Dora E Angelaki

Contributions

C.R.F., G.C.D. and D.E.A. conceived the study and designed the analyses. C.R.F. performed the experiments and analyzed the data. A.P. derived equations 6–8 and consulted on all theoretical aspects of the work. All of the authors wrote the paper.

Competing financial interests

The authors declare no competing financial interests.

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Supplementary information

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  1. Supplementary Text and Figures (2 MB)

    Supplementary Figures 1–6 and Supplementary Analysis

Additional data