Reach plans in eye-centered coordinates

Science

Volumn 285, Issue 5425, 1999, Pages 257-260

  Batista, Aaron P ^a,c   Buneo, Christopher A ^c   Snyder, Lawrence H ^b,c   Andersen, Richard A ^c  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARM MOVEMENT; ARTICLE; EYE HAND COORDINATION; EYE POSITION; HAND MOVEMENT; MONKEY; NONHUMAN; PARIETAL LOBE; PRIORITY JOURNAL; TASK PERFORMANCE; VISUAL STIMULATION;

ANIMALS; ARM; FIXATION, OCULAR; MACACA MULATTA; MOTOR ACTIVITY; MOTOR CORTEX; NEURAL PATHWAYS; NEURONS; NEURONS, AFFERENT; PARIETAL LOBE; PSYCHOMOTOR PERFORMANCE; SACCADES; VISUAL PATHWAYS; VISUAL PERCEPTION;

ANIMALIA;

EID: 0033538555     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.285.5425.257     Document Type: Article

References (39)

1. M. Jeannerod, The Neural and Behavioral Organization of Goal-Directed Movements (Oxford Univ. Press, New York, 1988).
2. L. H. Snyder, A. P. Batista, R. A. Andersen, Nature 386, 167 (1997).
3. A. Murata et al., J. Neurophysiol. 75, 2180 (1996).
4. C. L. Colby, Neuron 20, 15 (1998); G. Rizzolatti, L. Riggio, B. Sheliga, in Attention and Performance, C. Umiltà and M. Moskovitch, Eds. (MIT Press, Cambridge, MA, 1994), vol. 15, pp. 231-265.
5. C. L. Colby, Neuron 20, 15 (1998); G. Rizzolatti, L. Riggio, B. Sheliga, in Attention and Performance, C. Umiltà and M. Moskovitch, Eds. (MIT Press, Cambridge, MA, 1994), vol. 15, pp. 231-265.
6. Recording sites were mapped onto the cortical surface in one animal (2); the other three animals are involved in other experiments. A nuclear yellow dye injection was made into a site where saccade-selective neurons were identified. This injection was visualized in the lateral bank of the intraparietal sulcus (area LIP). From the position of the dye injection and four pins marking the position of the recording chamber, PRR recording sites were localized to a region medial and posterior to LIP, presumably overlapping with areas V6A (26) and MIP (19, 27). Neurons were first examined in a delayed reach and saccade paradigm to determine their specificity for these two movement types (2). Eye movements were recorded with scleral search coils. Saccades and reaches were made to a vertically oriented 3 × 4 array of touch-sensitive buttons placed 24 cm in front of the animal. Each button was 3.7 cm in diameter and contained a red and a green light-emitting diode (LED) behind a translucent window 1.2 cm in diameter. A trial began with illumination of a red and a green LED at the button located straight ahead. The animal would look at and touch this button. A cue was presented (300 ms for monkeys D, G, and O; 150 ms for monkey C) at one of the eight locations surrounding the straight-ahead button, 18° or 26° from it. A red cue signaled an eventual saccadic eye movement [delayed saccade (DS) task], and a green cue signaled a reach [delayed reach (DR) task]. After a delay period (800 ms or longer), the central LEDs were extinguished as a "go" signal. The animal then made a saccade or reached to the remembered location of the target. Importantly, during saccade trials, the monkey could not move its hand, and, during reach trials, the animal had to maintain fixation at the location of the now-extinguished red LED. The contralateral limb was used in all experiments. The animal's room was dark; there was no vision of the hand during the reach. To test whether neurons were reach specific, delay period activity (from 100 ms after the cue was extinguished until the go signal) of the reach and saccade tasks was compared. If the greatest reach planning response was significantly larger than the greatest saccade planning response (Mann-Whitney test, P < 0.05), the neuron was considered reach-specific. Only reach specific neurons were analyzed further.
7. The coordinate frame (CF) task was a variant of the delayed reach task. Four conditions with different eye and initial hand positions were used. In two conditions, the red LED instructing visual fixation was at the button located straight ahead, and the green LED instructing the initial button press was 18° (36° for 11 neurons in monkey C) to the left or right In these two conditions, target buttons were at identical locations in eye-centered coordinates but at different locations in arm-centered coordinates. In the other two conditions, the green LED was at the straight-ahead button, and the red LED was 18° to the left or right. In these conditions, target locations were identical in arm-centered coordinates but different in eye-centered coordinates. Reaches were typically made to between 8 and 11 buttons. The four conditions were otherwise identical to the delayed reach task. For each neuron, the four conditions were randomly interleaved for five repetitions of reaches to each target.
8. l are the average firing rates for reaches to target i, with the eyes fixating to the left (x) or to the right (y) with the same initial hand position. For most cells, there were between 8 and 11 overlapping locations. If there were fewer than 3 overlapping locations, the cell was not included in the correlation analysis.
9. Ninety-one percent of neurons in monkey D (42 tested), 78% in monkey O (18 tested), and 71% in monkey C (14 tested) showed a greater correlation in eye-centered coordinates than in limb-centered coordinates.
10. L. E. Mays and D. L. Sparks, J. Neurophysiol. 43, 207 (1980); J. W. Gnadt and R. A. Andersen, Exp. Brain Res. 70, 216 (1988); J.-R. Duhamel, C. L. Colby, M. E. Goldberg, Science 255, 90 (1992); M. F. Walker, E. J. Fitzgibbon, M. E. Goldberg, J. Neurophysiol. 73, 1988 (1995); M. S. A. Graziano, X. T. Hu, C. G. Gross, Science 277, 239 (1997).
11. L. E. Mays and D. L. Sparks, J. Neurophysiol. 43, 207 (1980); J. W. Gnadt and R. A. Andersen, Exp. Brain Res. 70, 216 (1988); J.-R. Duhamel, C. L. Colby, M. E. Goldberg, Science 255, 90 (1992); M. F. Walker, E. J. Fitzgibbon, M. E. Goldberg, J. Neurophysiol. 73, 1988 (1995); M. S. A. Graziano, X. T. Hu, C. G. Gross, Science 277, 239 (1997).
12. L. E. Mays and D. L. Sparks, J. Neurophysiol. 43, 207 (1980); J. W. Gnadt and R. A. Andersen, Exp. Brain Res. 70, 216 (1988); J.-R. Duhamel, C. L. Colby, M. E. Goldberg, Science 255, 90 (1992); M. F. Walker, E. J. Fitzgibbon, M. E. Goldberg, J. Neurophysiol. 73, 1988 (1995); M. S. A. Graziano, X. T. Hu, C. G. Gross, Science 277, 239 (1997).
13. L. E. Mays and D. L. Sparks, J. Neurophysiol. 43, 207 (1980); J. W. Gnadt and R. A. Andersen, Exp. Brain Res. 70, 216 (1988); J.-R. Duhamel, C. L. Colby, M. E. Goldberg, Science 255, 90 (1992); M. F. Walker, E. J. Fitzgibbon, M. E. Goldberg, J. Neurophysiol. 73, 1988 (1995); M. S. A. Graziano, X. T. Hu, C. G. Gross, Science 277, 239 (1997).
14. L. E. Mays and D. L. Sparks, J. Neurophysiol. 43, 207 (1980); J. W. Gnadt and R. A. Andersen, Exp. Brain Res. 70, 216 (1988); J.-R. Duhamel, C. L. Colby, M. E. Goldberg, Science 255, 90 (1992); M. F. Walker, E. J. Fitzgibbon, M. E. Goldberg, J. Neurophysiol. 73, 1988 (1995); M. S. A. Graziano, X. T. Hu, C. G. Gross, Science 277, 239 (1997).
15. The IS task was a modification of the CF task. Five hundred milliseconds into the delay period, the visual fixation point jumped. The monkey responded by making a saccade to the new location of the red LED. Another 600 ms of delay period ensued before both fixation LEDs were extinguished to trigger the reach. This task was interleaved with the two conditions of the CF task depicted in Fig. 1, C and D. In one of these conditions gaze was directed at the initial eye position for the IS trials. In the other condition, gaze was directed at the final eye position for the IS trials. The delay epochs for the two CF conditions were lengthened to 1100 ms to more closely match the overall delay period in the IS task. In all three tasks the initial hand position was at the center button, so the same reach was always performed. Typically, 10 repetitions of each task were performed.
16. Neurons that showed a significantly different response (Mann-Whitney test, P < 0.05) during the final 500 ms of the delay period for the two CF conditions were analyzed further. A cell was considered to update if its response during the 500 ms after the saccade and before the reach in the IS task was significantly greater (Mann-Whitney test, P < 0.05) than its response during the 500 ms before the reach for the CF condition with the target out of the response field. Fifteen neurons from monkey D, 16 from monkey O, and 3 from monkey G were studied.
17. D. Y. P. Henriques et al., J. Neurosci. 18, 1583 (1998); P. Vetter, S. J. Goodbody, D. M. Wolpert, J. Neurophysiol. 81, 935 (1999); J. F. Soechting, S. I. H. Tillery, M. Flanders, J. Cognit. Neurosci. 2, 32 (1990); J. McIntyre, F. Stratta, F. Lacquaniti, J. Neurophysiol. 78, 1601 (1997).
18. D. Y. P. Henriques et al., J. Neurosci. 18, 1583 (1998); P. Vetter, S. J. Goodbody, D. M. Wolpert, J. Neurophysiol. 81, 935 (1999); J. F. Soechting, S. I. H. Tillery, M. Flanders, J. Cognit. Neurosci. 2, 32 (1990); J. McIntyre, F. Stratta, F. Lacquaniti, J. Neurophysiol. 78, 1601 (1997).
19. D. Y. P. Henriques et al., J. Neurosci. 18, 1583 (1998); P. Vetter, S. J. Goodbody, D. M. Wolpert, J. Neurophysiol. 81, 935 (1999); J. F. Soechting, S. I. H. Tillery, M. Flanders, J. Cognit. Neurosci. 2, 32 (1990); J. McIntyre, F. Stratta, F. Lacquaniti, J. Neurophysiol. 78, 1601 (1997).
20. D. Y. P. Henriques et al., J. Neurosci. 18, 1583 (1998); P. Vetter, S. J. Goodbody, D. M. Wolpert, J. Neurophysiol. 81, 935 (1999); J. F. Soechting, S. I. H. Tillery, M. Flanders, J. Cognit. Neurosci. 2, 32 (1990); J. McIntyre, F. Stratta, F. Lacquaniti, J. Neurophysiol. 78, 1601 (1997).
21. F. Lacquaniti et al., Cereb. Cortex 5, 391 (1995).
22. J.-R. Duhamel et al., Nature 389, 845 (1997).
23. M. S. A. Graziano, G. S. Yap, C. G. Gross, Science 266, 1054 (1994).
24. L. Fogassi et al., J. Neurophysiol. 76, 141 (1996).
25. H. Mushiake, Y. Tanatsugu, J. Tanji, ibid. 78, 567 (1997); D. Boussaoud, C. Jouffrais, F. Bremmer, ibid. 80, 1132 (1998).
26. H. Mushiake, Y. Tanatsugu, J. Tanji, ibid. 78, 567 (1997); D. Boussaoud, C. Jouffrais, F. Bremmer, ibid. 80, 1132 (1998).
27. C. Cavada and P. S. Goldman-Rakic, J. Comp. Neurol. 287, 422 (1989); G. J. Blatt, R. A. Andersen, G. R. Stoner, ibid. 299, 421 (1990).
28. C. Cavada and P. S. Goldman-Rakic, J. Comp. Neurol. 287, 422 (1989); G. J. Blatt, R. A. Andersen, G. R. Stoner, ibid. 299, 421 (1990).
29. P. B. Johnson et al., Cereb. Cortex 6, 1047 (1996).
30. D. Zipser and R. A. Andersen, Nature 331, 679 (1988).
31. P. Sabes and M. I. Jordan, J. Neurosci. 17, 7119 (1997).
32. A. P. Georgopoulos et al., Exp. Brain Res. 49, 327 (1983).
33. R. Held and A. V. Hein, Percept. Motor Skills 8, 87 (1958).
34. D. M. Clower et al., Nature 383, 618 (1996).
35. D. H. Ballard et al., Philos. Trans. R. Soc. London Ser. B 337, 331 (1992).
36. C. Galletti et al., Eur. J. Neurosci. 9, 410 (1997).
37. C. L. Colby and J.-R. Duhamel, Neuropychologia 29, 517 (1991).
38. All spike density histograms were constructed by convolving spike trains with a triangular kernel, as described by D. W. Scott [Ann. Statist. 13, 1024 (1985)].
39. Supported by the Sloan Center for Theoretical Neurobiology and the National Eye Institute. We thank Yale Cohen, Alexander Grunewald, and Philip Sabes for helpful discussions. We also thank Betty Gillikin and Viktor Shcherbatyuk for technical assistance, Janet Baer and Janna Wynne for veterinary care, and Cierina Reyes for administrative assistance.