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Visual space is compressed in prefrontal cortex before eye movements

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Abstract

We experience the visual world through a series of saccadic eye movements, each one shifting our gaze to bring objects of interest to the fovea for further processing. Although such movements lead to frequent and substantial displacements of the retinal image, these displacements go unnoticed. It is widely assumed that a primary mechanism underlying this apparent stability is an anticipatory shifting of visual receptive fields (RFs) from their presaccadic to their postsaccadic locations before movement onset1. Evidence of this predictive ‘remapping’ of RFs has been particularly apparent within brain structures involved in gaze control2,3,4. However, critically absent among that evidence are detailed measurements of visual RFs before movement onset. Here we show that during saccade preparation, rather than remap, RFs of neurons in a prefrontal gaze control area massively converge towards the saccadic target. We mapped the visual RFs of prefrontal neurons during stable fixation and immediately before the onset of eye movements, using multi-electrode recordings in monkeys. Following movements from an initial fixation point to a target, RFs remained stationary in retinocentric space. However, in the period immediately before movement onset, RFs shifted by as much as 18 degrees of visual angle, and converged towards the target location. This convergence resulted in a threefold increase in the proportion of RFs responding to stimuli near the target region. In addition, like in human observers5,6, the population of prefrontal neurons grossly mislocalized presaccadic stimuli as being closer to the target. Our results show that RF shifts do not predict the retinal displacements due to saccades, but instead reflect the overriding perception of target space during eye movements.

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Figure 1: Multi-electrode recordings and high-density mapping of FEF neuronal RFs.
Figure 2: Shifting of FEF neuronal RFs before saccade onset.
Figure 3: Fixation and presaccadic population RF densities of recorded FEF neurons.
Figure 4: Localization of probe stimuli by the population of recorded FEF neurons.

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Acknowledgements

This work was supported by National Institutes of Health grant EY014924 and the Howard Hughes Medical Institute (T.M.). We thank D.S. Aldrich for technical assistance.

Author information

Authors and Affiliations

Authors

Contributions

M.Z. and T.M. designed the study. M.Z., B.N. and K.Z.X. performed the experiments. M.Z. and N.A.S. analysed the data. M.Z., N.A.S. and T.M. wrote the manuscript.

Corresponding author

Correspondence to Marc Zirnsak.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Schematic illustration of expected RF shifts due to ‘predictive remapping’.

a, Three RFs (highlighted circles A1, B1 and C1) during stable fixation at FP1. b, The same RFs as in a are shown during stable fixation at FP2 (A2, B2 and C2). In retinocentric areas like the FEF, RFs are displaced across fixations by the direction and amplitude equal to the saccade vector. c, According to predictive remapping, RFs are shifted from their presaccadic locations (grey circles) to their postsaccadic locations (gold circles) before movement onset. That is, RF shifts anticipate the upcoming eye movement.

Extended Data Figure 2 Saccadic reaction time.

Plotted are the average deviations from the mean saccadic reaction time of a given recording session for the two monkeys as a function of probe location.

Extended Data Figure 3 Time dependency of RF shifts.

a, Distribution of changes in shift amplitude (ΔPRE) between ‘early’ and ‘late’ PRFs (n = 68). Solid line indicates the mean (1.56 dva) of the distribution. b, Distribution of changes in the distance of PRFs (late–early) to the saccade target. Solid line indicates the mean (−1.26 dva) of the distribution.

Extended Data Figure 4 Retinocentric properties of FEF RFs (I).

a, Distribution of RF1s and RF2s in retinocentric coordinates shown together with the average retinocentric difference between corresponding centres across fixations. Error bars indicate s.d. b, Distribution of RF1s and RF2s projected into the same quadrant shown together with the average retinocentric difference between corresponding centres. This was done to control for possible systematic effects that might cancel each other out across quadrants in a. Error bars indicate s.d.

Extended Data Figure 5 Retinocentric properties of FEF RFs (II) and their presaccadic changes.

a, Correlations between the distances of RF1s to FP1 (εRF1) and the distances of RF2s to FP2 (εRF2) (r = 0.95, t-test (t) = 39.59, degrees of freedom (df) = 177, P < 10−10)* and between the angles ϕRF1 and θRF2 (r = 0.96, t = 45.32, df = 177, P < 10−10) are shown. Lines denote best regression fits. b, Correlations between εRF1 and the distances of PRFs to FP2 (εPRF) (r = 0.51, t = 7.81, df = 177, P = 2.1 × 10−8) and between the angles ϕRF1 and θPRF are shown. If the predictive remapping hypothesis were true, the relationships shown in a and b should not differ. However, the correlation between εRF1 and εPRF (b, top) is significantly different from the correlation between εRF1 and εRF2 (a, top) (Steiger’s Z-test for dependent correlations, Z = 13.4, P < 10−10), as are the intercepts b0 (t = 5.23, df = 283, P = 3.3 × 10−7) and the slopes b1 (t = 12.87, df = 283, P < 10−10) of the respective regressions. Furthermore, instead of a positive correlation close to 1 (a, bottom) we find a significant negative circular correlation** between ϕRF1 and θPRF (b, bottom) (r = −0.53, P < 10−10). c, Correlations between εRF1 and the distances of PRFs to FP1 (εPRF) (r = 0.43, t = 6.4, df = 177, P = 1.1 × 10−9) and between the angles ϕRF1 and ϕPRF (r = 0.68, t = 12.4, df = 177, P < 10−10) are shown. If there were no presaccadic shifts of RFs the relationships shown in a and c should not differ. Again, however, we find the correlation between εRF1 and εPRF (c, top) to be significantly different from the correlation between εRF1 and εRF2 (a, top) (Z = 14.03, P < 10−10), as are the intercepts (t = 20.81, df = 286, P < 10−10) and the slopes (t = 14.4, df = 286, P < 10−10) of the regressions. The same is true for the correlation between ϕRF1 and θRF2 (a, bottom) and the correlation between ϕRF1 and ϕPRF (c, bottom) (Z = 13.02, P < 10−10), and for the intercepts (t = 17.69, df = 352, P < 10−10) and slopes (t = 20.74, df = 352, P < 10−10). *Note, the significance of all correlations in this figure, reported as Pearson’s r, was also assessed by computing Spearman’s rho and Kendall’s tau. All correlations were significant using these measures (P values not reported). **Note, circular statistics (correlation and regression)37 that are independent of a particular coordinate system had to be used in this case as the plotted angles fell outside the linear region. For the relationship between ϕRF1 and θRF2 and between ϕRF1 and ϕPRF ordinary statistics could be used. For comparisons, the respective circular correlations are 0.96 and 0.71.

Extended Data Figure 6 Examples of RFs in which single probe results would be consistent with the remapping hypothesis.

Two examples of RF maps in which the presaccadic RF converges towards the saccade target, rather than remap, yet it is clear that sampling of responses from only a single location would yield results consistent with remapping. In each example, the two fixation and one presaccadic RF response maps, and corresponding RF centres (black crosses, RF1, RF2 and PRF), are shown from top to bottom, respectively. As in previous figures, the blue filled circle indicates the location of fixation during probe presentation, although in the presaccadic RF plot the monkey is preparing a saccade to FP2 (target). In addition, in each plot, the gold arrow denotes the vector describing the RF shift expected with remapping if that shift is exactly equal to the saccade vector (as in most studies). In addition, indicated along with the PRF of each example is the location to which the RF1 centre is expected to shift with remapping if the location is based on the empirically mapped postsaccadic RF (RF2) (white square). As FEF RFs are retinocentric, both predictions are virtually the same, but shown for clarity. Note that in both examples, although the PRF clearly deviates from the remapping prediction overall, the predicted remapping location nonetheless yields a clear visual response. Thus, if only a single probe is used, the results would be consistent with the remapping hypothesis. The vector plots below show the comparison of the empirical remapping prediction based on RF2 with the measured PRF shifts. Conventions are as in Fig. 1.

Extended Data Figure 7 Centres of all measured FEF RFs.

Distribution of RF1s (dark grey), RF2s (light grey) and PRFs (gold) are shown in head-centred (screen) coordinates. For RF1s and PRFs the monkey fixated FP1. For RF2s the monkey fixated FP2.

Extended Data Figure 8 Example of single neuron isolation, corresponding RF measurements, and waveform stability.

a, Density plot of isolated (left panel) and all other waveforms (right panel) recorded from a single U-Probe channel. b, Inter spike interval (ISI) histogram of the isolated waveform. The number of ISI violations and the estimated false positive rate are based on a refractory period of 1.5 ms. b, Averaged (arithmetic mean) waveforms (solid lines) for the fixation (left) and presaccadic (middle) condition, and their differences (right). Grey and gold dashed lines indicate s.d. Black dashed lines enclose 95% confidence intervals. None of the depicted differences are statistically significant. d, Projection of fixation (grey) and presaccadic (gold) waveforms into principal component (PC) space. First two PC dimensions are shown. e, Distribution of Pseudo R2s (n = 40) resulting from logistic regression fits for each PC dimension in order to separate between fixation and presaccadic waveforms. Dnull designates the null deviance using the intercept in the regression exclusively. Dk designates the model deviance using a single PC dimension as predictor in addition. Perfect seperation would result in an R2 of 1. The mean of the depicted R2s is 0.01 (min = 2.9 × 10−6, max = 0.04). None of the R2s reached statistical significance (likelihood ratio chi-squared test). f, Performance of a linear support vector machine trained to discriminate between fixation and presaccadic waveforms using all 40 PC dimensions simultaneously. The estimated performance (gold line) of 59.4% correct classifications falls well within the 95% range (37.1, 62.9) (red lines) of the expected chance performance. g, Fixation and presaccadic RF maps are shown together with their respective RF centres (black crosses, RF1, RF2 and PRF). Same conventions as in Fig. 1. h, Histogram of the pseudo R2s as obtained by logistic regressions for 21 neurons with stable waveforms. The mean R2 is 0.01 (min = 0, max = 0.23). None of the individual R2s reached statistical significance. i, Support vector machine classification performance of fixation and presaccadic waveforms for the same set of neurons. The mean correct classification performance is 50.1% (s.d. = 7.3). All performance estimates (gold ellipses) fall well within the expected ranges of chance performance (grey lines).

Extended Data Figure 9 RF shifts of single neurons and comparison with RF shifts in the remaining population.

a, The presaccadic shift amplitude (ΔPRE) as a function of the distance of RF1 from the saccade target (FP2) (εRF1) for well-isolated single neurons with stable waveforms (left) and for the remaining set of RFs (right). Lines denote fits of a linear regression. b, The angular deviation of the presaccadic RF shift from the remapping prediction (ϕ′) as a function of θ for the two subpopulations of RFs. c, Comparison of the population of presaccadic RF shifts (gold vectors) with the remapping prediction (grey vectors) for the two subpopulations of RFs. Vector origins and end points are based on, respectively, RF1 and RF2 (grey) and RF1 and PRF (gold).

Extended Data Figure 10 Spike count correlations of recorded FEF neurons.

a, Decrease in mean spike count correlation (rSC) as a function of electrode distance. Solid line denotes the best fitting power function (axb; a = 0.12, P < 10−10; b = −0.45, P < 10−10). Data points are averages across neuronal pairs (n = 677) recorded at a fixed electrode distance, across all probe locations and across all three experimental conditions (fixation 1, fixation 2 and presaccadic). The number of neuronal pairs for each electrode distance, in order of increasing distance, was n = (128, 106, 92, 86, 68, 55, 44, 28, 24, 18, 14, 10, 4). Note that the fit was based on the non-averaged data. b, Top, mean rSC plotted as a function of baseline normalized firing rate during fixation (grey) and before saccade onset (gold). Positive values on the abscissa indicate combined responses above baseline. Error bars indicate s.e.m. Number of combined responses, in order of increasing baseline normalized response, was n = (8,805, 8,805, 8,806, 8,804, 8,806, 7,738, 7,737, 7,738, 7,737, 7,737, 7,738, 7,737, 7,738, 7,737, 7,737) for fixation, and n = (2,827, 1,742, 1,416, 1,185, 1,144, 1,026, 1,298, 1,655, 2,511, 3,876, 6,013, 7,342, 7,679, 9,013, 11,329) for the presaccadic condition. Middle, cumulative percentage of paired neuronal responses for which each individual response exceeds baseline during fixation (grey) and before saccade onset (gold). Bottom, difference in the mean rSC during fixation and before saccades. Error bars indicate Bonferroni-corrected (15 comparisons) 95% confidence intervals. Grey area indicates nonsignificant differences.

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Zirnsak, M., Steinmetz, N., Noudoost, B. et al. Visual space is compressed in prefrontal cortex before eye movements. Nature 507, 504–507 (2014). https://doi.org/10.1038/nature13149

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