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Articles, Systems/Circuits

Spatial and Temporal Eye–Hand Coordination Relies on the Parietal Reach Region

Eun Jung Hwang, Markus Hauschild, Melanie Wilke and Richard A. Andersen
Journal of Neuroscience 17 September 2014, 34 (38) 12884-12892; DOI: https://doi.org/10.1523/JNEUROSCI.3719-13.2014
Eun Jung Hwang
1Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California 91125,
2Division of Biological Sciences, University of California, San Diego, California 92093,
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Markus Hauschild
1Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California 91125,
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Melanie Wilke
1Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California 91125,
3Department of Cognitive Neurology, University of Göttingen, Göttingen, 37075, Germany, and
4German Primate Center, Leibniz Institute for Primate Research, Göttingen, 37077, Germany
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Richard A. Andersen
1Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California 91125,
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  • Figure 1.
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    Figure 1.

    Natural eye–hand coordination in the eye–hand task. a, The temporal sequence of events in the eye–hand task. Eyes were unconstrained. b, The inactivation site shown on the horizontal brain MRI slice. The bright spot indicates where MR visible gadolinium was injected in the same way as muscimol. c, The hand and eye positions of seven example trials in the eye–hand task are aligned to the go cue. Each pair of a solid and a dashed line in the same color represents the hand and eye positions of the same single trial. The arrows mark the positions of the central hand-fixation and the reach target. d, Reach and saccade endpoints for six target locations in the eye–hand task from an example pair of a control and an inactivation session. The saccades occurred under free-gaze condition in the absence of experimental requirements.

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    Figure 2.

    PRR inactivation shortens the amplitude of coordinated saccades and reaches but not of saccades executed alone. a, Reach and saccade amplitudes in three task conditions for each of six target locations. For each target, the mean amplitude and its 95% confidence interval are plotted for control versus inactivation reaches in the eye–hand task, control versus inactivation saccades in the eye–hand task, control versus inactivation reaches in the hand-only task, and control versus inactivation saccades in the saccade-only task, from left to right. The horizontal dashed line in each plot marks the target amplitude. b, Within-session means of reach and saccade amplitudes in the eye–hand task for the contralateral target, in control versus inactivation sessions. Each pair of a control and an inactivation session is connected with a solid line if their means are significantly different (p < 0.05), and with a dashed line otherwise.

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    Figure 3.

    PRR inactivation weakens the temporal correlation between spatially coordinated reaches and saccades. a, Saccade reaction times versus reach reaction times (RTs) for the contralateral target in the eye–hand task for all control versus inactivation trials. Each dot represents a single trial, and the lines are the linear regression. b, The mean and its 95% confidence interval of the correlation coefficient between saccade and reach RTs of all control versus inactivation trials for each of the six target locations. c, Within-session RT correlation coefficients for the contralateral target, in control versus inactivation sessions. Each pair of a control and an inactivation session is connected with a solid line if their coefficients are significantly different (p < 0.05), and with a dashed line otherwise.

Tables

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    Table 1.

    The average number of trials per target location, task condition, and session

    MonkeySession no.No. of trials per target
    Eye–handHand-onlyEye-only
    ControlInactivationControlInactivationControlInactivation
    Y122 (21)11 (10)2211
    220 (20)19 (17)1419
    321 (20)22 (18)2022
    413 (12)25 (21)1425
    525 (25)25 (25)25292627
    625 (24)25 (23)28332625
    726 (24)13 (12)40132615
    G18 (7)19 (17)921919
    215 (12)18 (6)14181314
    319 (15)11 (8)189179
    415 (12)19 (17)13181317
    518 (17)19 (17)17201818
    6*258 (234)266 (240)33533457
    • Each session is a pair of control and inactivation that were typically separated by 1 d. The numbers in parenthesis indicate the number of trials in which both eye and hand positions at the onset of go cue were within 1 cm from the hand-fixation target. The italicized sessions and tasks are data previously presented in Hwang et al. (2012).

    • ↵*Tasks were performed with only two targets (contralateral and ipsilateral). In the other sessions, tasks were performed with six targets.

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    Table 2.

    Summary statistics of inactivation effects on movement amplitude, reaction time, and movement duration (from top to bottom)

    Changes in mean (mean, SEM, p)Changes in variance (mean, SEM, p)Changes in CC (mean, SEM, p)
    Reach_EHSaccade_EHReach_HOSaccade_EOReach_EHSaccade_EHReach_HOSaccade_EO
    Movement amplitude
        Monkey Y: I−0.26 0.092 0.000−0.21 0.083 0.001−0.63 0.080 0.000−0.07 0.075 1.000−0.04 0.070 1.000−0.06 0.088 1.000−0.02 0.048 1.0000.21 0.090 0.001−0.24 0.109 0.012
        IU−0.38 0.090 0.000−0.01 0.147 1.000−1.01 0.052 0.0000.24 0.179 0.370−0.02 0.077 1.000−0.58 0.321 0.092−0.05 0.044 1.000−0.95 0.907 1.000−0.07 0.112 1.000
        CU−0.57 0.065 0.0000.11 0.149 1.000−1.46 0.081 0.000−0.08 0.125 1.000−0.32 0.082 0.0000.34 0.361 1.000−0.27 0.059 0.0050.85 0.452 0.002−0.17 0.126 0.294
        C−0.59 0.068 0.000−0.38 0.123 0.000−1.68 0.079 0.000−0.06 0.148 1.0000.13 0.072 0.0920.20 0.258 1.0000.05 0.082 1.000−1.38 0.886 0.1800.27 0.135 0.066
        CD−1.07 0.086 0.000−0.13 0.099 0.335−1.60 0.104 0.0001.11 1.237 1.0000.13 0.080 0.8510.07 0.109 1.000−0.05 0.134 1.000−0.07 0.157 1.000−0.04 0.184 1.000
        ID−0.44 0.093 0.000−0.08 0.085 0.986−0.49 0.104 0.000−0.02 0.074 1.0000.05 0.089 1.0000.00 0.098 1.000−0.22 0.095 0.0770.02 0.071 1.000−0.02 0.113 1.000
        Monkey G: I−0.12 0.082 0.232−0.08 0.091 1.000−1.57 0.190 0.0000.05 0.091 1.000−0.14 0.074 0.0400.19 0.520 1.000−0.45 0.184 0.137−0.01 0.084 1.000−0.01 0.078 1.000
        IU−0.64 0.143 0.0000.12 0.158 1.000−1.78 0.152 0.0000.43 0.155 0.0010.26 0.150 0.2020.09 0.210 1.000−0.19 0.208 1.000−0.29 0.258 1.0000.31 0.252 0.528
        CU−0.22 0.146 0.237−0.23 0.235 1.000−0.52 0.107 0.000−0.16 0.179 1.0000.18 0.146 0.5451.31 0.876 0.156−0.15 0.127 0.565−0.15 0.271 1.000−0.04 0.235 1.000
        C−0.69 0.076 0.000−0.44 0.104 0.000−0.71 0.165 0.000−0.08 0.296 1.000−0.21 0.081 0.007−1.87 1.446 0.007−0.63 0.254 0.0330.33 0.143 0.0160.17 0.078 0.048
        CD−0.31 0.135 0.0050.05 0.184 1.000−1.03 0.152 0.000−0.15 0.147 0.8560.18 0.170 1.0000.53 0.347 0.199−0.15 0.162 1.0000.16 0.165 1.0000.00 0.221 1.000
        ID−0.11 0.124 1.0000.20 0.129 0.214−0.85 0.139 0.0000.03 0.153 1.000−0.28 0.154 0.0530.02 0.128 1.000−0.27 0.188 0.6570.29 0.184 0.139−0.22 0.194 0.564
    Reaction time
        Monkey Y: I2.74 4.133 1.0003.75 3.899 1.00024.24 9.128 0.001−0.22 4.355 1.000−0.84 0.505 0.0950.94 0.602 0.094−1.51 1.263 0.6620.39 0.665 1.0000.02 0.123 1.000
        IU−3.24 4.147 1.0003.49 4.850 1.00030.30 8.487 0.000−15.06 6.049 0.004−0.40 0.313 0.4681.55 0.780 0.013−1.31 0.933 0.411−1.38 1.188 0.912−0.20 0.108 0.048
        CU0.50 3.488 1.000−8.18 4.399 0.05817.90 6.932 0.0027.27 5.073 0.247−0.36 0.198 0.073−1.21 0.615 0.051−0.75 0.554 0.5791.38 0.982 0.2580.16 0.133 0.516
        C16.02 6.204 0.00016.54 7.925 0.0199.08 6.646 0.394−16.39 5.598 0.0002.71 2.211 0.7500.83 1.213 1.000−0.83 0.981 1.000−1.73 1.247 0.336−0.26 0.109 0.018
        CD12.86 5.146 0.000−18.04 11.528 0.15628.45 6.440 0.000−4.78 5.248 1.0001.53 1.749 1.0000.94 1.022 1.000−0.66 0.860 1.000−1.11 0.815 0.462−0.08 0.200 1.000
        ID2.57 6.443 1.000−22.35 7.071 0.000−1.21 13.776 1.000−7.81 4.163 0.046−4.90 4.432 1.000−1.12 0.644 0.128−1.87 3.732 1.0000.46 0.738 1.0000.09 0.176 1.000
        Monkey G: I−9.07 4.859 0.058−24.72 3.846 0.000−32.0 12.59 0.001−9.13 5.878 0.165−1.36 0.665 0.025−0.33 0.579 1.000−4.98 4.614 0.6830.20 0.728 1.0000.04 0.115 1.000
        IU27.81 17.450 0.1610.54 5.916 1.0002.33 12.68 1.0005.71 8.678 1.0007.75 7.653 1.000−0.30 0.468 1.000−6.62 3.936 0.0081.48 1.324 0.7500.04 0.136 1.000
        CU−6.17 13.919 1.000−8.56 9.404 1.00016.74 13.045 0.451−19.03 6.861 0.001−2.77 2.074 0.423−0.17 0.731 1.0004.02 3.389 0.488−0.22 0.475 1.000−0.28 0.202 0.684
        C−24.4 25.504 0.000−15.83 3.673 0.000−10.53 11.50 1.000−9.82 4.969 0.0271.68 1.745 1.000−0.91 0.381 0.0015.14 4.254 0.654−0.67 0.249 0.000−0.15 0.072 0.036
        CD32.61 19.249 0.11030.90 8.990 0.0009.54 11.743 1.000−1.59 7.450 1.00014.52 6.887 0.0051.36 0.675 0.0561.17 1.538 1.000−0.32 0.729 1.0000.12 0.189 1.000
        ID14.19 24.094 1.000−5.38 7.306 1.0001.23 12.414 1.000−10.82 8.154 0.3562.49 6.224 1.0000.19 0.596 1.0000.46 2.634 1.0000.89 1.087 1.0000.10 0.175 1.000
    Movement duration
        Monkey Y: I−16.7 4.43 0.0000.4 0.55 1.000−15.7 4.38 0.0000.4 0.53 1.000−0.03 0.449 1.0000.00 0.004 1.000−0.07 0.326 1.0000.00 0.005 1.0000.09 0.140 1.000
        IU−22.5 5.45 0.0000.1 0.59 1.000−28.7 4.34 0.0000.8 0.64 0.622−1.10 0.854 0.6680.00 0.005 1.000−0.46 0.304 0.805−0.01 0.007 0.0510.03 0.095 1.000
        CU−28.9 5.64 0.0000.3 0.87 1.000−22.8 4.82 0.0000.0 0.96 1.000−3.45 1.196 0.000−0.01 0.009 0.501−0.17 0.472 1.000−0.01 0.010 1.0000.08 0.113 1.000
        C−24.4 5.17 0.0001.0 0.81 0.4181.1 10.41 1.000−0.2 0.99 1.000−1.39 0.706 0.0430.01 0.009 0.3115.31 5.551 1.0000.03 0.039 1.000−0.03 0.163 1.000
        CD−16.0 3.79 0.0002.2 1.25 0.06044.0 22.44 0.014−1.5 1.16 0.404−0.25 0.171 0.5060.07 0.064 0.19638.77 13.922 0.0000.01 0.013 0.835−0.07 0.206 1.000
        ID−14.0 4.80 0.0000.8 0.60 0.504−10.5 4.74 0.0162.1 1.08 0.039−2.03 1.290 0.0160.00 0.006 1.000−0.52 0.362 0.5500.01 0.012 0.557−0.13 0.139 1.000
        Monkey G: I−34.4 5.96 0.000−3.6 1.58 0.006−38.71 1.32 0.000−1.6 0.88 0.076−5.13 4.665 1.0000.14 0.217 1.000−3.57 3.723 1.000−0.03 0.021 0.4280.06 0.054 1.000
        IU−8.0 7.55 0.829−0.8 0.74 0.763−13.0 9.95 0.3831.6 0.92 0.0950.43 0.799 1.0000.01 0.008 0.139−0.55 4.382 1.0000.00 0.011 1.0000.27 0.141 0.132
        CU3.1 9.81 1.000−1.6 1.24 0.4251.2 6.90 1.000−1.8 1.32 0.302−2.25 2.621 1.000−0.04 0.040 0.959−0.21 0.397 1.000−0.02 0.029 1.000−0.27 0.179 0.282
        C−41.3 4.25 0.000−0.8 0.52 0.145−20.0 7.23 0.000−0.4 0.87 1.000−1.71 0.958 0.076−0.02 0.016 0.1512.05 1.406 0.2570.02 0.024 1.000−0.10 0.065 0.354
        CD2.4 10.06 1.000−2.6 1.24 0.0238.9 9.07 1.000−2.0 1.29 0.1510.19 2.339 1.000−0.01 0.014 1.0001.99 2.120 1.000−0.02 0.012 0.2710.06 0.204 1.000
        ID−7.3 8.02 1.0000.2 1.13 1.000−10.6 6.24 0.099−1.1 1.01 0.869−0.68 0.792 1.0000.01 0.012 0.623−0.27 0.256 0.8440.00 0.013 1.0000.22 0.157 0.780
    • The left column indicates Monkeys Y and G targets (I, ipsilateral; IU, ipsilateral upward; CU, contralateral upward; C, contralateral; CD, contralateral downward; ID, ipsilateral downward). The top rows indicate the properties of a movement parameter (mean, variance, saccade-reach correlation coefficient), the task condition (EH, eye–hand task; HO, hand-only task; EO, eye-only task), and effectors (saccade and reach). Correlation coefficients between saccade and reach were measured only in the eye–hand task. Each triplet of numbers represents the mean, SE, and p value for the difference in the corresponding property of a movement parameter between all control and inactivation trials. A positive difference in means indicates an increase by inactivation. Triplets with a consistent, significant effect in both monkeys are bold. Triplets with a significant effect only in one monkey are italicized.

    • View popup
    Table 3.

    The reach and saccade reaction times in the eye-hand task

    MonkeyReach reaction time (ms, mean ± SD)Saccade reaction time (ms, mean ± SD)
    ControlInactivationControlInactivation
    Y
        I268 ± 3.3271 ± 2.5220 ± 2.1223 ± 3.4
        IU300 ± 3.1296 ± 2.8219 ± 2.4222 ± 4.2
        CU302 ± 2.6302 ± 2.3218 ± 3.6210 ± 2.5
        C289 ± 3.0305 ± 5.4220 ± 4.9237 ± 6.1
        CD256 ± 2.5269 ± 4.5396 ± 7.5378 ± 8.6
        ID250 ± 6.1252 ± 2.1312 ± 5.2290 ± 4.8
    G
        I368 ± 3.8358 ± 3.2245 ± 2.8221 ± 2.7
        IU400 ± 9.6427 ± 14.5229 ± 4.4230 ± 3.9
        CU438 ± 10.9433 ± 8.7282 ± 6.7273 ± 6.5
        C412 ± 3.6388 ± 4.3268 ± 2.9252 ± 2.3
        CD409 ± 8.0441 ± 17.5283 ± 5.5314 ± 7.2
        ID467 ± 16.7482 ± 17.1255 ± 5.3250 ± 5.0
    • The means were computed across all control versus inactivation trials, for each target and each monkey. Means with a significant difference between control and inactivation (permutation test, p < 0.05 corrected for multiple comparison; see Table 2 for the statistical tests on the difference) were italicized.

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Spatial and Temporal Eye–Hand Coordination Relies on the Parietal Reach Region
Eun Jung Hwang, Markus Hauschild, Melanie Wilke, Richard A. Andersen
Journal of Neuroscience 17 September 2014, 34 (38) 12884-12892; DOI: 10.1523/JNEUROSCI.3719-13.2014

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Spatial and Temporal Eye–Hand Coordination Relies on the Parietal Reach Region
Eun Jung Hwang, Markus Hauschild, Melanie Wilke, Richard A. Andersen
Journal of Neuroscience 17 September 2014, 34 (38) 12884-12892; DOI: 10.1523/JNEUROSCI.3719-13.2014
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Keywords

  • inactivation
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