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Attention-related changes in correlated neuronal activity arise from normalization mechanisms

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Abstract

Attention is believed to enhance perception by altering the activity-level correlations between pairs of neurons. How attention changes neuronal activity correlations is unknown. Using multielectrodes in monkey visual cortex, we measured spike-count correlations when single or multiple stimuli were presented and when stimuli were attended or unattended. When stimuli were unattended, adding a suppressive, nonpreferred stimulus beside a preferred stimulus increased spike-count correlations between pairs of similarly tuned neurons but decreased spike-count correlations between pairs of oppositely tuned neurons. A stochastic normalization model containing populations of oppositely tuned, mutually suppressive neurons explains these changes and also explains why attention decreased or increased correlations: as an indirect consequence of attention-related changes in the inputs to normalization mechanisms. Our findings link normalization mechanisms to correlated neuronal activity and attention, showing that normalization mechanisms shape response correlations and that these correlations change when attention biases normalization mechanisms.

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Figure 1: Multielectrode-array recordings of neuronal activity in area V4 during a visual attention task.
Figure 2: Normalization mechanisms determine spike-count correlations.
Figure 3: Visual attention engages normalization mechanisms to modulate spike-count correlations.
Figure 4: Attention modulation of spike-count correlations for neuron pairs with opposite selectivity is minor.
Figure 5: A stochastic normalization model accounts for the main trends in the observed correlations.
Figure 6: Normalization mechanisms affect spike-count correlations similarly for stimuli inside the cRF or in the surround.

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Acknowledgements

We thank D. Freedman for discussions. We thank J. Cone, S. Ghosh, G. Ibos and T. Luo for comments on an earlier version of the manuscript and S. Sleboda for technical assistance. B.-E.V. is supported by a postdoctoral research fellowship from the Flemish Fund for Scientific Research (FWO). This work was supported by NIH grant R01EY005911.

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Authors and Affiliations

  1. Department of Neurobiology, The University of Chicago, Chicago, Illinois, USA

    Bram-Ernst Verhoef & John H R Maunsell

  2. Laboratorium voor Neuro- en Psychofysiologie, KU Leuven, Leuven, Belgium

    Bram-Ernst Verhoef

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  1. Bram-Ernst Verhoef
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Contributions

B.-E.V. and J.H.R.M. designed the experiments, performed the surgeries and wrote the paper. B.-E.V. performed the experiments and analyzed the data.

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Correspondence to Bram-Ernst Verhoef.

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Integrated supplementary information

Supplementary Figure 1 Attention task and behavioral performance.

a,b, Stimuli could appear at two locations near the RFs of neurons, but the two locations differed between blocks of trials. One stimulus location (the middle location: location 1 in a, b) never varied, but in different blocks of trials the second stimulus location was shifted either clockwise (location 2 in a) or counterclockwise (location 3 in b). Stimulus locations 1, 2 and 3 were located near the RFs of the recorded neurons. c, A representative set of nine possible stimulus combinations, consisting of single Gabors of two different orientations and spatial locations and their combinations (i.e. Gabor pairs). d, For 91% of trials the target was presented at the cued location (location of the black circle; valid trials). On the remaining 9% of trials the target was presented at one of three uncued locations: adjacent to the cued location (location of the yellow circle; invalid near), or at one of two locations on the opposite side of the fixation point (location of the green circles; invalid far). Colored circles in (d) are shown for illustrative purposes and were never presented on the video display. e, Monkeys used the attention cue to improve their performance: valid vs. invalid near: monkey M1: p<0.0001, M2: p<0.0001; valid vs. invalid far: M1: p<0.0001, M2: p<0.0001; paired t-test on the average proportion correct across sessions; M1: N=52; M2: N=78). Error-bars represent ± 1 SEM.

Supplementary Figure 2 Normalization mechanisms determine spike-count correlations: similar results for preferred and nonpreferred stimuli.

All data in these plots were obtained while the monkeys' attention was directed far from the RF stimuli. Only data from neuron pairs with the same selectivity (selectivity > 0) are shown, because preferred and non-preferred are not defined for oppositely-tuned neurons (i.e., for oppositely-tuned neurons, one neuron's preferred stimulus is the other neuron's non-preferred stimulus and vice versa). a, Mean spike-count correlations, indicated by color, as a function of the selectivity and non-preferred suppression of neuron pairs, measured while a preferred stimulus was presented alone. b, Mean spike-count correlations measured while the preferred and non-preferred stimuli of neuron pairs were simultaneously presented. c, Difference in spike-count correlations between b and a. Main effect selectivity: P=0.04, main effect non-preferred suppression: P<0.0001, selectivity-suppression interaction: P<0.0001, N=1270826. d-f Same as a-c but for the non-preferred stimulus. Panel e is an exact replicate of panel b. Main effect selectivity: P<0.0001, main effect non-preferred suppression: P<0.0001, selectivity-suppression interaction: P<0.0001, N=1270826.

Supplementary Figure 3 Attention modulation of average neuronal responses.

All data in these plots were obtained with two stimuli, preferred and non-preferred, simultaneously presented inside the RF of units, but with attention directed to different stimulus locations. a, Mean response, indicated by color, as a function of the selectivity and non-preferred suppression, measured with attention directed far from RF stimuli. b, Mean response measured with attention directed to the preferred stimulus. c, Mean response measured with attention directed to the non-preferred stimulus. d, Difference between panel b and a. Attention to the preferred stimulus increases responses most for selective units that are strongly suppressed by their non-preferred stimulus. e, Difference between panel c and a. Attention to the non-preferred stimulus decreases responses most for selective units that are strongly suppressed by their non-preferred stimulus.

Supplementary Figure 4 Normalization mechanisms determine spike-count correlations for pairs of neurons in which one neuron is strongly suppressed and the other neuron weakly suppressed by the nonpreferred stimulus.

In the main results we focused on those neuron pairs in which both neurons are similarly suppressed by the non-preferred stimulus (see Fig. 2a): non-preferred suppression values smaller than 0.5 meant that both neurons of a pair were less suppressed by the non-preferred stimulus than by the preferred stimulus; non-preferred suppression values greater than 0.5 meant that both neurons of a pair were more suppressed by the non-preferred stimulus than by the preferred stimulus. Such neuron pairs represented the bulk (73%) of the dataset. However, in a smaller fraction (27%) of pairs one neuron received strong suppression from its non-preferred stimulus but the other neuron received weak suppression from its non-preferred stimulus (Supplementary Fig. 4a). For these neuron pairs there was always one neuron that was weakly suppressed by the non-preferred stimulus. In agreement with the findings from the main text, which shows that spike-count correlations are strongly modulated only when both neurons of a pair are substantially suppressed by the non-preferred stimulus, spike-count correlations were generally less modulated for these neuron pairs (Supplementary Fig. 4b, c). Nevertheless, even for these neuron pairs we observed significantly increased spike-count correlations following the addition of a second stimulus for neuron pairs with the same selectivity, whose responses were most strongly suppressed by their non-preferred stimulus (upper right quadrant in Supplementary Fig. 4b; main effect selectivity: P=0.0007, main effect suppression: P<0.0001, selectivity-suppression interaction: P<0.0001, linear regression, N=954772 correlations). Furthermore, pairs of neurons with opposite selectivity, whose responses are most strongly suppressed by each neuron's non-preferred stimulus, decreased their spike-count correlations (lower right quadrant in Supplementary Fig. 4b; main effect selectivity: P=0.7, main effect suppression: P<0.0001, selectivity-suppression interaction: P<0.0001, N=433808 correlations). In addition, these spike-count correlations were most strongly modulated by attention for neuron pairs with the same selectivity that were most selective and most suppressed by their non-preferred stimulus (upper right corner of Supplementary Fig. 4c; main effect selectivity: P<0.0001, main effect suppression: P<0.0001, selectivity-suppression interaction: P<0.0001). Note that for these neuron pairs the non-preferred suppression index ranges from zero to 0.71. This follows from the definition of the non-preferred suppression index (Online Methods), because the neuron that is most strongly suppressed by the non-preferred stimulus has a maximum non-preferred suppression value of one, while the other neuron of the pair that is only weakly suppressed by the non-preferred stimulus has a maximum non-preferred suppression value of 0.5 (non-preferred suppression < 0.5 indicate that the neuron is mostly suppressed by the preferred stimulus; 0.5 means equal suppression by the preferred and non-preferred stimulus). Combining these two values, i.e. one and 0.5, into the non-preferred suppression index for pairs of neurons (Online Methods), using the geometric mean, gives ~0.71.

Supplementary Figure 5 Neuron pairs covering the space spanned by the nonpreferred suppression and selectivity indices.

Each dot (N = 3804250 correlations) corresponds to a neuron pair for which spike-count correlations are shown in Figure 2b-d and Figure 3a-c. Pearson correlation between selectivity and non-preferred suppression = -0.07.

Supplementary Figure 6 Distribution of spike-count correlations in different stimulus and attention conditions.

In the box-and-whisker plots, the central horizontal line indicates the mean, the boundaries of the boxes indicated the 25th and 75th percentiles and the whiskers extend to 1.5 the interquartile range. As expected, spike-count correlations are variable. Because of this variability, we collected large amounts of data, aiming for precise estimates of the average spike-count correlations in each condition. a. Same conventions as in Figure 2e. b. Same conventions as in Figure 3d. c. Same conventions as in Figure 4b.

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Verhoef, BE., Maunsell, J. Attention-related changes in correlated neuronal activity arise from normalization mechanisms. Nat Neurosci 20, 969–977 (2017). https://doi.org/10.1038/nn.4572

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