Neural control of voluntary movement initiation

Science

Volumn 274, Issue 5286, 1996, Pages 427-430

  Hanes, Doug P ^a   Schall, Jeffrey D ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; MATHEMATICAL MODEL; MOTOR CONTROL; MOTOR CORTEX; NONHUMAN; PRIORITY JOURNAL; REACTION TIME; RHESUS MONKEY; VOLUNTARY MOVEMENT;

ACTION POTENTIALS; ANIMALS; COMPUTER SIMULATION; FRONTAL LOBE; LINEAR MODELS; MACACA MULATTA; MODELS, NEUROLOGICAL; NEURONS; PATCH-CLAMP TECHNIQUES; PSYCHOMOTOR PERFORMANCE; REACTION TIME; SACCADES; STOCHASTIC PROCESSES; SYNAPTIC TRANSMISSION;

ANIMALIA; MACACA MULATTA;

EID: 0029806801     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.274.5286.427     Document Type: Article

References (31)

1. H. L. F. von Helmholtz, Philos. Mag, (English translation) 6, 313 (1853); R. D. Luce, Response Times: Their Role in Inferring Elementary Mental Organization (Oxford Univ. Press, New York, 1986); D. E. Meyer, A. M. Osman, D. E. Irwin, S. Yantis, Biol. Psychol. 26, 3 (1988).
2. H. L. F. von Helmholtz, Philos. Mag, (English translation) 6, 313 (1853); R. D. Luce, Response Times: Their Role in Inferring Elementary Mental Organization (Oxford Univ. Press, New York, 1986); D. E. Meyer, A. M. Osman, D. E. Irwin, S. Yantis, Biol. Psychol. 26, 3 (1988).
3. H. L. F. von Helmholtz, Philos. Mag, (English translation) 6, 313 (1853); R. D. Luce, Response Times: Their Role in Inferring Elementary Mental Organization (Oxford Univ. Press, New York, 1986); D. E. Meyer, A. M. Osman, D. E. Irwin, S. Yantis, Biol. Psychol. 26, 3 (1988).
4. V. B. Brooks, The Neural Basis of Motor Control (Oxford Univ. Press, New York, 1986).
5. R. H. Wurtz and M. E. Goldberg, The Neurobiology of Saccadic Eye Movements (Elsevier, New York, 1989); R. H. S. Carpenter, Eye Movements (Macmillan, London, 1991); J. D. Schall, in Vision and Visual Dysfunction, vol. 4 of The Neural Basis of Visual Function, A. G. Leventhal, Ed. (Macmillan, London, 1991), pp. 388-442.
6. R. H. Wurtz and M. E. Goldberg, The Neurobiology of Saccadic Eye Movements (Elsevier, New York, 1989); R. H. S. Carpenter, Eye Movements (Macmillan, London, 1991); J. D. Schall, in Vision and Visual Dysfunction, vol. 4 of The Neural Basis of Visual Function, A. G. Leventhal, Ed. (Macmillan, London, 1991), pp. 388-442.
7. R. H. Wurtz and M. E. Goldberg, The Neurobiology of Saccadic Eye Movements (Elsevier, New York, 1989); R. H. S. Carpenter, Eye Movements (Macmillan, London, 1991); J. D. Schall, in Vision and Visual Dysfunction, vol. 4 of The Neural Basis of Visual Function, A. G. Leventhal, Ed. (Macmillan, London, 1991), pp. 388-442.
8. R. H. S. Carpenter, Movements of the Eyes (Pion, London, 1988); R. Ratcliff, Psychol. Rev. 85, 59 (1978); J. L. McClelland, ibid. 86, 287 (1979); R. H. S. Carpenter and M. L. L. Williams, Nature 377, 59 (1995).
9. R. H. S. Carpenter, Movements of the Eyes (Pion, London, 1988); R. Ratcliff, Psychol. Rev. 85, 59 (1978); J. L. McClelland, ibid. 86, 287 (1979); R. H. S. Carpenter and M. L. L. Williams, Nature 377, 59 (1995).
10. R. H. S. Carpenter, Movements of the Eyes (Pion, London, 1988); R. Ratcliff, Psychol. Rev. 85, 59 (1978); J. L. McClelland, ibid. 86, 287 (1979); R. H. S. Carpenter and M. L. L. Williams, Nature 377, 59 (1995).
11. R. H. S. Carpenter, Movements of the Eyes (Pion, London, 1988); R. Ratcliff, Psychol. Rev. 85, 59 (1978); J. L. McClelland, ibid. 86, 287 (1979); R. H. S. Carpenter and M. L. L. Williams, Nature 377, 59 (1995).
12. G. R. Grice, Psychol. Rev. 75, 359 (1968); T. A. Nazir and A. M. Jacobs, ibid. 53, 281 (1991). Hybrid models have also been formulated [A. Pacut, biol. Cyber. 28, 63 (1977)].
13. G. R. Grice, Psychol. Rev. 75, 359 (1968); T. A. Nazir and A. M. Jacobs, ibid. 53, 281 (1991). Hybrid models have also been formulated [A. Pacut, biol. Cyber. 28, 63 (1977)].
14. G. R. Grice, Psychol. Rev. 75, 359 (1968); T. A. Nazir and A. M. Jacobs, ibid. 53, 281 (1991). Hybrid models have also been formulated [A. Pacut, biol. Cyber. 28, 63 (1977)].
15. Several lines of evidence document the role of the FEF, located in the rostral bank of the arcuate sulcus in monkeys, in gaze control (3). The FEF projects heavily to subcortical oculomotor structures. Microstimulation with very low current evokes eye movements, and acute inactivation prevents monkeys from making eye movements [E. C. Dias, M. Kiesau, M. A. Segraves, J. Neurophysiol. 74, 2744 (1995)].
16. D. P. Hanes, K. G. Thompson, J. D. Schall, Exp. Brain Res. 103, 85 (1995).
17. Physiological recording techniques have been described (7). Monkeys were seated within a magnetic field to monitor eye position by means of a scleral search coil. Experiments were under computer control (PDP 11/83) to present stimuli, deliver a juice reward, and sample and store eye position (250 Hz) and unit activity (1000 Hz). Visual stimuli were presented on a color video monitor (47° by 60°). Animals were cared for in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals and the guidelines of the Vanderbilt Animal Care and Use Committee.
18. G. D. Logan and W. B. Cowan, Psychol. Rev. 91, 295 (1984); D. P. Hanes and J. D. Schall, Visual Neurosei. 12, 929 (1995).
19. G. D. Logan and W. B. Cowan, Psychol. Rev. 91, 295 (1984); D. P. Hanes and J. D. Schall, Visual Neurosei. 12, 929 (1995).
20. Movement-related activity was distinguished from visually evoked activity by a memory-guided saccade task. In this task, the target was flashed for 100 ms while the monkey was required to maintain fixation on the central spot for another 500 to 1000 ms. When the fixation spot disappeared, reward was contingent on the monkey making a saccade to the remembered location of the target. Once the saccade was made, the target reappeared to provide feedback and a target for the monkey to fixate.
21. d ≈ 20 ms [R. J. Sayer, M. J. Friedlander, S. J. Redman, J. Neurosci. 10, 826 (1990)]. This asymmetric function that represents the actual postsynaptic influence of each cell has two advantages. First, each spike exerts influence only forward in time. Second, time constants that are comparable with physiologically measured values were used.
22. Several physiological findings delimit the interval during which FEF activity could contribute to the commitment to produce a saccadic eye movement. Omnipause neurons in the brainstem, which gate saccade initiation, cease discharging 8 to 10 ms before saccade initiation [J. A. Buttner-Ennever, B. Cohen, M. Pause, W. Fries, J. Comp. Neurol. 267, 307 (1988)], and the transduction time from FEF movement cells to the omnipause cells is around 4 ms [M. A. Segraves, J. Neurophysiol. 68, 1967 (1992)]. According to these times, then, the FEF cannot influence saccade initiation later than 12 to 14 ms before the movement begins. Also, the modal time of burst onset within FEF movement cells is 10 ms before saccade initiation (7). Finally, the minimum latency of the saccades evoked by electrical stimulation of FEF is around 20 ms [C. J. Bruce, M. E. Goldberg, C. Bushnell, G. B. Stanton, J. Neurophysiol. 54, 714 (1985)]. The results of the analysis we report did not change when the level of activation was measured 20 to 30 or 0 to 10 ms before saccade initiation.
23. Several physiological findings delimit the interval during which FEF activity could contribute to the commitment to produce a saccadic eye movement. Omnipause neurons in the brainstem, which gate saccade initiation, cease discharging 8 to 10 ms before saccade initiation [J. A. Buttner-Ennever, B. Cohen, M. Pause, W. Fries, J. Comp. Neurol. 267, 307 (1988)], and the transduction time from FEF movement cells to the omnipause cells is around 4 ms [M. A. Segraves, J. Neurophysiol. 68, 1967 (1992)]. According to these times, then, the FEF cannot influence saccade initiation later than 12 to 14 ms before the movement begins. Also, the modal time of burst onset within FEF movement cells is 10 ms before saccade initiation (7). Finally, the minimum latency of the saccades evoked by electrical stimulation of FEF is around 20 ms [C. J. Bruce, M. E. Goldberg, C. Bushnell, G. B. Stanton, J. Neurophysiol. 54, 714 (1985)]. The results of the analysis we report did not change when the level of activation was measured 20 to 30 or 0 to 10 ms before saccade initiation.
24. Several physiological findings delimit the interval during which FEF activity could contribute to the commitment to produce a saccadic eye movement. Omnipause neurons in the brainstem, which gate saccade initiation, cease discharging 8 to 10 ms before saccade initiation [J. A. Buttner-Ennever, B. Cohen, M. Pause, W. Fries, J. Comp. Neurol. 267, 307 (1988)], and the transduction time from FEF movement cells to the omnipause cells is around 4 ms [M. A. Segraves, J. Neurophysiol. 68, 1967 (1992)]. According to these times, then, the FEF cannot influence saccade initiation later than 12 to 14 ms before the movement begins. Also, the modal time of burst onset within FEF movement cells is 10 ms before saccade initiation (7). Finally, the minimum latency of the saccades evoked by electrical stimulation of FEF is around 20 ms [C. J. Bruce, M. E. Goldberg, C. Bushnell, G. B. Stanton, J. Neurophysiol. 54, 714 (1985)]. The results of the analysis we report did not change when the level of activation was measured 20 to 30 or 0 to 10 ms before saccade initiation.
25. All trials for a neuron were rank ordered by reaction time and were split into equal groups containing at least 10 trials on the basis of reaction time. Thus, the first group consisted of the trials with the 10 shortest reaction times, and so on. The number of reactiontime groups varied across cells because of different trial numbers. If the total number of no-signal trials was less than 50, the number of trials in each saccade latency group was set so that five saccade latency groups were generated.
26. An algorithm was applied to each trial to identify periods of activity in which more spikes occurred than would be predicted from a random Poisson process having the overall average rate of the trial [C. R. Legéndy and M. Salcman, J. Neurophysiol. 53, 926 (1985); (7)]. For each group of reaction time trials, the mode of the distribution of response beginning times was determined.
27. 2 of the linear regression on the activation function was 0.79 (minimum = 0.34, maximum = 0.99). A Durbin-Watson test for autocorrelation of the residuals provided another test of the goodness of fit of the neural activation function with a tine. For only 12 of the 190 saccade latency groups was there a significant autocorrelation between the residuals. The fact that a linear function provided such a good fit to the actration function is further evidence against the variable threshold model that posits a decelerating accumulator function.
28. The magnitude of the lateralized readiness potential at movement initiation does not vary with reaction time [G. Gratton, M. G. H. Coles, E. Sirevaag, C. W. Eriksen, E. Donchin, J. Exp. Psychol. Human Percept Perform. 14, 331 (1988)], and the lateralized readiness potential does not reach a critical threshold level in signal-inhibit trials (R. DeJong, M. G. H. Coles, G. D. Logan, G. Gratton, ibid. 16, 164 (1990)].
29. The magnitude of the lateralized readiness potential at movement initiation does not vary with reaction time [G. Gratton, M. G. H. Coles, E. Sirevaag, C. W. Eriksen, E. Donchin, J. Exp. Psychol. Human Percept Perform. 14, 331 (1988)], and the lateralized readiness potential does not reach a critical threshold level in signal-inhibit trials (R. DeJong, M. G. H. Coles, G. D. Logan, G. Gratton, ibid. 16, 164 (1990)].
30. ON), specified by the Poisson spike-train analysis, was held constant across simulated trials. The trigger threshold (A') was held constant across simulated trials at the average threshold activation measured across all reaction time groups collected for that cell (for example, Fig. 3D). The rate of growth of the simulated accumulator function (r) was selected on each simulated trial from a Gaussian distribution. The mean and SD of the sampled Gaussian distribution were derived from the rates of growth of the activation functions across the reaction-time groups collected for that cell (for example, Fig. 3E).
31. We thank O. Armstrong and D. King for assistance with data acquisition and analysis and N. Bichot, R. Blake, R. Carpenter, K. Cave, J. Kaas, J. Lappin, and K. Thompson for helpful discussion and comments on the manuscript. Supported by National Institute of Mental Health grants F31-MH11178 to D.P.H. and R01-MH55806 to J.D.S. and National Eye Institute (of NIH) grant P30-EY08126 to the Vanderbilt Vision Research Center. J.D.S. is a Kennedy Center Investigator.