Shared motor error for multiple eye movements

Science

Volumn 276, Issue 5319, 1997, Pages 1693-1695

  Krauzlis, R J ^a,b   Basso, M A ^a   Wurtz, R H ^a  

^a NATIONAL EYE INSTITUTE   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; EYE MOVEMENT; MOTOR SYSTEM; NONHUMAN; OCULOMOTOR NERVE; PRIORITY JOURNAL; SACCADIC EYE MOVEMENT; SUPERIOR COLLICULUS;

ANIMALS; EYE MOVEMENTS; FIXATION, OCULAR; MACACA MULATTA; MOTOR NEURONS; PURSUIT, SMOOTH; SACCADES; SUPERIOR COLLICULUS; VISUAL PATHWAYS;

ANIMALIA; PRIMATES;

EID: 0030748934     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.276.5319.1693     Document Type: Article

References (21)

1. S. Zeki, A Vision of the Brain (Blackwell Scientific, Oxford, 1993); D. C. Van Essen and J. L. Gallant, Neuron 13, 1 (1994).
2. S. Zeki, A Vision of the Brain (Blackwell Scientific, Oxford, 1993); D. C. Van Essen and J. L. Gallant, Neuron 13, 1 (1994).
3. W. Singer and C. M. Gray, Annu. Rev. Neurosci. 18, 555 (1995).
4. For reviews, see R. J. Leigh and D. S. Zee, Eds., The Neurology of Eye Movements (Davis, Philadelphia, PA, 1991).
5. The latency of saccadic and pursuit eye movements is similarly reduced in the "gap paradigm" in both monkeys and humans [R. J. Krauzlis and F. A. Miles, Vision Res. 36, 1973 (1996); J. Neurophysiol. 76, 2822 (1996)]. These data have been interpreted as evidence that there are shared inputs for the initiation of the two types of eye movements. Earlier studies have shown, for example, that lesions of the middle temporal area affect both the speed of pursuit and the amplitude of saccades in response to moving targets [W. T. Newsome, R. H. Wurtz, M. R. Dursteler, A. Mikami, J. Neurosci. 5, 825 (1985); P. H. Schiller and K. Lee, Visual Neurosci. 11, 229 (1994)], but these effects have been interpreted as overlap in sensory processing rather than in movement preparation.
6. The latency of saccadic and pursuit eye movements is similarly reduced in the "gap paradigm" in both monkeys and humans [R. J. Krauzlis and F. A. Miles, Vision Res. 36, 1973 (1996); J. Neurophysiol. 76, 2822 (1996)]. These data have been interpreted as evidence that there are shared inputs for the initiation of the two types of eye movements. Earlier studies have shown, for example, that lesions of the middle temporal area affect both the speed of pursuit and the amplitude of saccades in response to moving targets [W. T. Newsome, R. H. Wurtz, M. R. Dursteler, A. Mikami, J. Neurosci. 5, 825 (1985); P. H. Schiller and K. Lee, Visual Neurosci. 11, 229 (1994)], but these effects have been interpreted as overlap in sensory processing rather than in movement preparation.
7. The latency of saccadic and pursuit eye movements is similarly reduced in the "gap paradigm" in both monkeys and humans [R. J. Krauzlis and F. A. Miles, Vision Res. 36, 1973 (1996); J. Neurophysiol. 76, 2822 (1996)]. These data have been interpreted as evidence that there are shared inputs for the initiation of the two types of eye movements. Earlier studies have shown, for example, that lesions of the middle temporal area affect both the speed of pursuit and the amplitude of saccades in response to moving targets [W. T. Newsome, R. H. Wurtz, M. R. Dursteler, A. Mikami, J. Neurosci. 5, 825 (1985); P. H. Schiller and K. Lee, Visual Neurosci. 11, 229 (1994)], but these effects have been interpreted as overlap in sensory processing rather than in movement preparation.
8. The latency of saccadic and pursuit eye movements is similarly reduced in the "gap paradigm" in both monkeys and humans [R. J. Krauzlis and F. A. Miles, Vision Res. 36, 1973 (1996); J. Neurophysiol. 76, 2822 (1996)]. These data have been interpreted as evidence that there are shared inputs for the initiation of the two types of eye movements. Earlier studies have shown, for example, that lesions of the middle temporal area affect both the speed of pursuit and the amplitude of saccades in response to moving targets [W. T. Newsome, R. H. Wurtz, M. R. Dursteler, A. Mikami, J. Neurosci. 5, 825 (1985); P. H. Schiller and K. Lee, Visual Neurosci. 11, 229 (1994)], but these effects have been interpreted as overlap in sensory processing rather than in movement preparation.
9. D. L. Sparks and L. E. Mays, Annu. Rev. Neurosci. 13, 309 (1990).
10. D. P. Munoz and D. Guitton, J. Neurophysiol. 66, 1624 (1991).
11. D. P. Munoz and R. H. Wurtz, ibid. 67, 1000 (1992); ibid. 70, 559 (1993).
12. D. P. Munoz and R. H. Wurtz, ibid. 67, 1000 (1992); ibid. 70, 559 (1993).
13. We recorded from 31 neurons in the rostral SC of two rhesus monkeys (Maccaca mulatta) and obtained similar results in both monkeys, although not all experiments were performed on each cell. The monkeys were trained to look at and follow small (0.3°) spots of light projected onto a featureless background. At the end of individual trials lasting 1 to 2 s, monkeys were given a liquid reinforcement if they maintained their eye position near the target (within 2° for stationary targets and 5° for moving ones). The eye movement and single unit data were acquired with standard methods (7). All experimental protocols were approved by the Institutional Animal Care and Use Committee of the National Eye Institute and complied with the Public Health Service Policy on the humane care and use of laboratory animals.
14. The measurement interval started 100 ms after the change in target location and lasted either for 100 ms or until 8 ms before any corrective saccade, whichever came first. This interval was selected to reduce the inclusion of transient activity that was overtly related to the visual stimulus or to subsequent saccadic eye movements. These measurements were therefore taken in a time period that largely excluded the saccade-related activity reported in earlier studies (7).
15. Linear regressions were performed on the data from each of 19 neurons; 5 of these showed a significant relation (P < 0.05). The absence of a correlation in the remaining neurons may have resulted from the narrow range of eye positions fostered by this experiment and the inability to control the inferred location of the target after it was extinguished.
16. Neurons that decreased their firing rate during contraversive pursuit tended to be tuned for motor errors near zero or slightly ipsilateral (mean, 0.10° ipsilateral; n = 5), whereas neurons that increased their firing rate during contraversive pursuit tended to be tuned for larger contralateral errors (mean, 1.54° contralateral; n = 11).
17. Seventy milliseconds was chosen on the basis of the observed latency of the response to target steps.
18. Each millisecond sample of firing rate recorded during pursuit was assigned to a bin according to motor error; these bins matched the 21 amplitudes of motor error obtained with target steps during fixation (Fig. 1).
19. E. G. Freedman and D. L. Sparks, Soc. Neurosci. Abstr. 20, 142 (1994).
20. W. Werner, Eur. J. Neurosci. 5, 335 (1993).
21. We thank R. Desimone, L. Stone, and our colleagues at the Laboratory of Sensorimotor Research for their comments on an earlier draft of this paper and the Laboratory of Diagnostic Radiology Research for providing magnetic resonance images.