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Reward expectation differentially modulates attentional behavior and activity in visual area V4

Nature Neuroscience volume 18, pages 1656–1663 (2015)Cite this article

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Abstract

Neural activity in visual area V4 is enhanced when attention is directed into neuronal receptive fields. However, the source of this enhancement is unclear, as most physiological studies have manipulated attention by changing the absolute reward associated with a particular location as well as its value relative to other locations. We trained monkeys to discriminate the orientation of two stimuli presented simultaneously in different hemifields while we independently varied the reward magnitude associated with correct discrimination at each location. Behavioral measures of attention were controlled by the relative value of each location. By contrast, neurons in V4 were consistently modulated by absolute reward value, exhibiting increased activity, increased gamma-band power and decreased trial-to-trial variability whenever receptive field locations were associated with large rewards. These data challenge the notion that the perceptual benefits of spatial attention rely on increased signal-to-noise in V4. Instead, these benefits likely derive from downstream selection mechanisms.

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Figure 1: Task and behavior.
Figure 2: Firing rate modulation in V4 reflects absolute value of RF stimuli.
Figure 3: Regression summary of independently changing reward at two spatial locations.
Figure 4: Correlations between neural effects.
Figure 5: Differences in population activity when changing average trial value are similar to those when changing relative value.
Figure 6: Relative RF value and average trial value similarly modulate power spectra, trial-to-trial reliability and orientation tuning
Figure 7: Normalization predicts interaction between reward and spatial scale.

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Acknowledgements

We thank S. Bouret, E. Bromberg-Martin, V. Ciaramitaro, K. Louie and F. Pestilli for helpful comments on an earlier version of the manuscript, S. Dashnaw for MRI support, G. Asfaw for veterinary support, and K. Marmon for technical support. This research was supported by grants to C.D.S. from the US National Institute of Mental Health (NIMH) (R01 MH082017) and by a core grant from the US National Eye Institute (NEI) (P30-EY19007) to Columbia University. B.L. received support from the NIMH (T32-MH015144) and the Helen Hay Whitney Foundation. J.K.B. received support from the NEI (T32-EY013933) and the Columbia University Medical Scientist Training Program.

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Author notes

  1. Brian Lau

    Present address: Present address: Brain and Spine Institute, Sorbonne Universités, UPMC University of Paris 06, UMR S 1127, CNRS UMR 7225, Paris, France.,

  2. Jalal K Baruni and Brian Lau: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Neuroscience, Columbia University, New York, New York, USA

    Jalal K Baruni, Brian Lau & C Daniel Salzman

  2. Kavli Institute for Brain Sciences, Columbia University, New York, New York, USA

    C Daniel Salzman

  3. Department of Psychiatry, Columbia University, New York, New York, USA

    C Daniel Salzman

  4. New York State Psychiatric Institute, New York, New York, USA

    C Daniel Salzman

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  1. Jalal K Baruni
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Contributions

B.L. designed the experiment. J.K.B. and B.L. collected the data and wrote the manuscript. J.K.B. analyzed the data with assistance from B.L. C.D.S. supervised and provided input about all aspects of the project and edited the manuscript.

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Integrated supplementary information

Supplementary Figure 1 Psychometric functions.

Proportion correct as a function of task difficulty, shown separately for Monkey 1 (a) and Monkey 2 (b). Labels on abscissa indicate orientation bin edges. Error bars indicate +/− 1 s.e.m.

Supplementary Figure 2 Behavioral effects were consistent across monkeys.

Behavioral data are presented as function of relative target value or average trial value, from all trials completed during recording sessions in Monkey 1 (a-d, 5,174 LS; 5,230 LL; 5,312 SL; and 5,226 SS trials) and Monkey 2 (e-h, 6,881 LS; 6,965 LL; 7,018 SL; and 6,953 SS trials). Error bars indicate +/− 1 s.e.m. Overlapping points are slightly offset for visualization. (a,b) Performance and reaction time track relative target value in M1. Percent correct was highest in LS (CMH, p<10−10 for all comparisons), and lowest in SL (CMH, p<10−10 for all comparisons). Reaction times were fastest in LS (WRS, p<10−10 for all comparisons), and slowest in SL (WRS, p<10−10 for all comparisons). Performance was slightly higher (CMH, p = .0402) and reaction times slightly faster (WRS, p<10−4) in LL compared to SS trials. (c,d) Pupil diameter and abort rate track average trial value in M1. Pupils were most dilated in LL (WRS, p<10−10 for all comparisons) and least dilated in SS (WRS, p<10−10 for all comparisons). Abort rate was highest in SS (CMH, p<10−10 for all comparisons) and lowest in LL (CMH, p<10−6 for all comparisons). (e,f) Performance and reaction time track relative target value in M2. Percent correct was highest in LS (CMH, p<10−3 for all comparisons), and lowest in SL (CMH, p<10−10 for all comparisons). Reaction times were fastest in LS (WRS, p<10−10 for all comparisons), and slowest in SL (WRS, p<10−10 for all comparisons). Performance was slightly higher (CMH, p=.0066) and reaction times faster (WRS, p<10−10) in LL compared to SS trials. (g,h) Pupil diameter and abort rate track average trial value in M2. Pupils were most dilated in LL (WRS, p<10−10 for all comparisons) and least dilated in SS (WRS, p<10−10 for all comparisons). Abort rate was highest in SS (CMH, p<10−5 for all comparisons), and did not significantly differ between the other three conditions (CMH, p>0.1 for all comparisons).

Supplementary Figure 3 Behavioral effects were consistent across locations.

Behavioral data are presented as function of relative target value, from all trials completed during recording sessions in Monkey 1 (a-d) and Monkey 2 (e-h). Behavioral data are shown separately for targets contralateral (a,b,e,f) and ipsilateral (c,d,g,h) to the recorded brain area. Error bars indicate +/− 1 s.e.m. Overlapping points are slightly offset for visualization. (a,c) Performance tracks relative target value at each location in M1. At each location, performance was highest in LS (CMH, p<10−4) and lowest in SL (CMH, p<10−10). (b,d) Reaction times track relative target value at each location in M1. At each location, reaction times were fastest in LS (WRS, p<10−10), and slowest in SL (WRS, p<10−10) (e) Performance tracks relative target value at the contralateral location in M2. Performance was highest in LS (CMH, p<10−3) and lowest in SL (CMH, p<10−10). (g) At the ipsilateral location, performance was highest in LS (79.24%), but not significantly higher than either LL (77.98%; CMH, p>0.05) or SS conditions (77.87%; CMH, p>0.05). Performance at the ipsilateral location was lowest in SL (64.05%, CMH, p<10−10). (f,h) Reaction times track relative target value at each location in M2. At each location, reaction times were fastest in LS (WRS, p<10−10) and slowest in SL (WRS, p<10−10).

Supplementary Figure 4 Neural and behavioral effects across the population were similar in each monkey

Joint and marginal distributions of regression coefficients for Monkey 1 (a-c, n = 46 behavioral sessions, n = 106 recorded units) and Monkey 2 (d-f, n = 33 behavioral sessions, n = 84 recorded units). Symbol style denotes significance for individual sessions/units. (a) Reaction times reflect relative target value in all M1 sessions. Associating the larger reward with the target location decreased reaction times (WSR, p<10−8), whereas large rewards at distracter locations increased reaction times (WSR, p<10−8). (b) Pupil diameter reflects average trial value in M1 sessions. Associating the large reward with either the target (WSR, p<10−7) or distracter (WSR, p<10−7) increased pupil diameters. (c) Neuronal modulation reflects RF value in M1. Large rewards at the RF location were associated with increased firing rates (mean = +3.55 spikes/s; WSR, p<10−8). Large rewards opposite the RF were not associated with a significant change in firing rate (mean = −0.301 spikes/s; WSR, p = 0.45). (d) Reaction times reflect relative target value in all M2 sessions. Associating the larger reward with the target location decreased reaction times (WSR, p<10−6), whereas large rewards at distracter locations increased reaction times (WSR, p<10−6). (e) Pupil diameter reflects average trial value in all M1 sessions. Associating the large reward with either the target (WSR, p<10−6) or distracter (WSR, p<10−6) increased pupil diameters. (f) Neuronal modulation reflects RF value in M1. Large rewards at the RF location were associated with increased firing rates (mean = +4.69 spikes/s; WSR, p<10−10). Large rewards opposite the RF were not associated with a significant change in firing rate (mean= +0.276 spikes/s; WSR, p = 0.32).

Supplementary Figure 5 Relative RF value and average trial value increase gamma band power in both monkeys.

Raw (a,b) and normalized (c,d) power spectra for each monkey. Power spectra from the reference epoch used for normalization are indicated by the dotted line (a,b). In Monkey 1 (a,c, n = 40 sites), increases in relative RF value and average trial value both increased power in the gamma band (40-80hz; WSR, p<10−3). In Monkey 2 (b,d, n = 29 sites), increases in relative RF value and average trial value both increased power in the gamma band (40-80hz; WSR, p<10−4).

Supplementary Figure 6 Pupil diameters diverge after reward cue presentation.

Z-scored pupil diameters are aligned on two events in the trial. On the left, pupil values are aligned to acquisition of fixation. On the right, pupil values are aligned to onset of discriminanda. In all traces, line thickness exceeds +/− 1 s.e.m. After reward cue presentation (shaded box at left) and through streaming Gabor stimulus (shaded box at right), pupil diameters reflect average trial value. (n = 48,103)

Supplementary Figure 7 Regression coefficients for expanded model.

Symbol style denotes significance for individual sessions/units (n = 190). (a) Large rewards at the RF location were associated with increased firing rates (mean β1 = +3.678 spikes/sec). (b) Large rewards opposite the RF were associated with small increases in firing rate (mean β2= +0.397 spikes/sec), inconsistent with relative value modulation (c) Increased reaction times were associated with small decreases in firing rate (mean β3 = −0.350 spikes/sec). (d) Increased pupil diameters were associated with small decreases in firing rate (mean β4= −0.350 spikes/sec).

Supplementary Figure 8 Procedure for constructing orientation-tuning functions.

(a) Spike density functions (SDF) for an example unit. Responses to individual 20ms Gabor presentations within the stimulus stream were sorted by orientation, aligned on presentation onset, and averaged to generate spike density functions. (b) To determine a unit-specific spike count window, we computed the effect size (η2) of Gabor orientation on firing rate in a sliding window (5 ms wide, 1 ms steps). Effect sizes, as well as correlation of SDFs across time, were used to define the window, denoted by the shaded line. (c,d) Spike counts were compiled into orientation tuning functions and fit with Gaussian functions. Error bars indicate +/− 1 s.e.m. Dashed lines indicate mean responses for each condition, averaged across orientation.

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Baruni, J., Lau, B. & Salzman, C. Reward expectation differentially modulates attentional behavior and activity in visual area V4. Nat Neurosci 18, 1656–1663 (2015). https://doi.org/10.1038/nn.4141

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