Journal of Neurophysiology, Vol 76, Issue 2 825-848, Copyright © 1996 by APS

ARTICLES

Neurons in the supplementary eye field of rhesus monkeys code visual targets and saccadic eye movements in an oculocentric coordinate system

G. S. Russo and C. J. Bruce
Section of Neurobiology, Yale University School of Medicine, New Haven, Connecticut 06520-8001, USA.

1. We investigated whether neurons in the supplementary eye field (SEF) of macaque monkeys code saccadic eye movements in oculocentric coordinates (relative to the current direction of fixation) or in craniocentric coordinates (relative to the head). Craniocentric coding in SEF had been previously suggested by the convergent appearance of electrically elicited saccades originating at different orbital positions. 2. We primarily studied SEF neurons that started responding before the beginning of saccades because such presaccadic activity is likely related to saccade generation and metrics. Using a memory-saccade task, we classified the presaccadic activity of each neuron as either purely visual related, purely movement related, or both visual and movement related. 3. We then mapped the response fields (receptive fields and movement fields) of SEF neurons from different orbital positions. When mapped relative to a central fixation point, the strongest responses for a given SEF neuron invariably occurred for a particular polar direction with fairly symmetrical declines for departures from that direction. When tested using other fixation point locations, their strongest responses almost always continued to occur for stimuli having the same polar direction relative to each fixation point tested, and thus they appeared to code both stimulus direction and saccade direction in an oculocentric coordinate system. 4. The effect of eye position on SEF presaccadic activity was quantified in two ways by computing, for each neuron, 1) an "intersection distance," the eccentricity of the point where extensions of the neuron's optimal polar directions measured at two eccentric orbital positions converged, and 2) an "orbital perturbation index" such that an index of 0 corresponded to no change in the neuron's optimal polar direction across different orbital positions (i.e., perfectly oculocentric response fields) and an index of 1 corresponded to optimal polar directions that converged to the same craniocentric goal regardless of initial eye position (i.e., perfectly craniocentric response fields). For neurons with both visual and movement responses, these measures were calculated separately for each type of activity using tasks that temporally separated the visual cue presentation and the saccade to it. 5. Almost all of the intersection distances were well beyond the oculomotor range (+/- 50 degrees) of the monkey (38/39 for movement activity and 62/66 for visual activity). The median intersection distance for visual activity was very large (274 degrees), and the median for movement activity was slightly divergent (beyond infinity). Thus SEF neurons rarely showed a conspicuous convergence of response field direction. 6. Likewise, the mean orbital perturbation indexes were very small (-0.04 +/- 0.21, mean +/- SD, for movement activity and 0.09 +/- 0.15 for visual activity), also indicating that SEF neurons code stimuli and saccades in an oculocentric manner. 7. For neurons with both visual and movement activities, the orbital perturbation indexes of the two activities were not significantly correlated (r = 0.16), even though their characteristic directions (optimal polar direction estimated from the center of the screen) were almost the same (circular correlation, r+ = 0.97). The lack of a significant correlation between the visual and movement activity orbital perturbation indexes is consistent with the hypothesis that most of the variation in this index represents statistically independent errors of measurement. Conversely, the strong covariation of visual and movement activity characteristic directions indicates that directional preference is a fundamental functional property of SEF presaccadic activity.(ABSTRACT TRUNCATED)

This article has been cited by other articles:

				C. de Hemptinne, P. Lefevre, and M. Missal Neuronal Bases of Directional Expectation and Anticipatory Pursuit J. Neurosci., April 23, 2008; 28(17): 4298 - 4310. [Abstract] [Full Text] [PDF]

				J. A. Cromer and D. M. Waitzman Comparison of Saccade-Associated Neuronal Activity in the Primate Central Mesencephalic and Paramedian Pontine Reticular Formations J Neurophysiol, August 1, 2007; 98(2): 835 - 850. [Abstract] [Full Text] [PDF]

				A. G. Constantin, H. Wang, J. C. Martinez-Trujillo, and J. D. Crawford Frames of Reference for Gaze Saccades Evoked During Stimulation of Lateral Intraparietal Cortex J Neurophysiol, August 1, 2007; 98(2): 696 - 709. [Abstract] [Full Text] [PDF]

				D. E. Moorman and C. R. Olson Combination of Neuronal Signals Representing Object-Centered Location and Saccade Direction in Macaque Supplementary Eye Field J Neurophysiol, May 1, 2007; 97(5): 3554 - 3566. [Abstract] [Full Text] [PDF]

				D. E. Moorman and C. R. Olson Impact of Experience on the Representation of Object-Centered Space in the Macaque Supplementary Eye Field J Neurophysiol, March 1, 2007; 97(3): 2159 - 2173. [Abstract] [Full Text] [PDF]

				T. A. Knight and A. F. Fuchs Contribution of the Frontal Eye Field to Gaze Shifts in the Head-Unrestrained Monkey: Effects of Microstimulation J Neurophysiol, January 1, 2007; 97(1): 618 - 634. [Abstract] [Full Text] [PDF]

				J. Park, M. Schlag-Rey, and J. Schlag Frames of Reference for Saccadic Command Tested By Saccade Collision in the Supplementary Eye Field J Neurophysiol, January 1, 2006; 95(1): 159 - 170. [Abstract] [Full Text] [PDF]

				M. A. Smith and J. D. Crawford Distributed Population Mechanism for the 3-D Oculomotor Reference Frame Transformation J Neurophysiol, March 1, 2005; 93(3): 1742 - 1761. [Abstract] [Full Text] [PDF]

				C. Constantinidis and X.-J. Wang A Neural Circuit Basis for Spatial Working Memory Neuroscientist, December 1, 2004; 10(6): 553 - 565. [Abstract] [PDF]

				K. Takeda and S. Funahashi Population Vector Analysis of Primate Prefrontal Activity during Spatial Working Memory Cereb Cortex, December 1, 2004; 14(12): 1328 - 1339. [Abstract] [Full Text] [PDF]

				M.R.G. Brown, J.F.X. DeSouza, H. C. Goltz, K. Ford, R. S. Menon, M. A. Goodale, and S. Everling Comparison of Memory- and Visually Guided Saccades Using Event-Related fMRI J Neurophysiol, February 1, 2004; 91(2): 873 - 889. [Abstract] [Full Text] [PDF]

				M. Isoda and J. Tanji Contrasting Neuronal Activity in the Supplementary and Frontal Eye Fields During Temporal Organization of Multiple Saccades J Neurophysiol, November 1, 2003; 90(5): 3054 - 3065. [Abstract] [Full Text] [PDF]

				J. C. Martinez-Trujillo, E. M. Klier, H. Wang, and J. D. Crawford Contribution of Head Movement to Gaze Command Coding in Monkey Frontal Cortex and Superior Colliculus J Neurophysiol, October 1, 2003; 90(4): 2770 - 2776. [Abstract] [Full Text] [PDF]

				J. C. Martinez-Trujillo, H. Wang, and J. D. Crawford Electrical Stimulation of the Supplementary Eye Fields in the Head-Free Macaque Evokes Kinematically Normal Gaze Shifts J Neurophysiol, June 1, 2003; 89(6): 2961 - 2974. [Abstract] [Full Text] [PDF]

				N. Fujii, H. Mushiake, and J. Tanji Distribution of Eye- and Arm-Movement-Related Neuronal Activity in the SEF and in the SMA and Pre-SMA of Monkeys J Neurophysiol, April 1, 2002; 87(4): 2158 - 2166. [Abstract] [Full Text] [PDF]

				L. Tremblay, S. N. Gettner, and C. R. Olson Neurons With Object-Centered Spatial Selectivity in Macaque SEF: Do They Represent Locations or Rules? J Neurophysiol, January 1, 2002; 87(1): 333 - 350. [Abstract] [Full Text] [PDF]

				G. S. Russo and C. J. Bruce Supplementary Eye Field: Representation of Saccades and Relationship Between Neural Response Fields and Elicited Eye Movements J Neurophysiol, November 1, 2000; 84(5): 2605 - 2621. [Abstract] [Full Text] [PDF]

				C. R. Olson, S. N. Gettner, V. Ventura, R. Carta, and R. E. Kass Neuronal Activity in Macaque Supplementary Eye Field During Planning of Saccades in Response to Pattern and Spatial Cues J Neurophysiol, September 1, 2000; 84(3): 1369 - 1384. [Abstract] [Full Text] [PDF]

				C. R. Olson and L. Tremblay Macaque Supplementary Eye Field Neurons Encode Object-Centered Locations Relative to Both Continuous and Discontinuous Objects J Neurophysiol, April 1, 2000; 83(4): 2392 - 2411. [Abstract] [Full Text] [PDF]

				R. F. Lewis, B. M. Gaymard, and R. J. Tamargo Efference Copy Provides the Eye Position Information Required for Visually Guided Reaching J Neurophysiol, September 1, 1998; 80(3): 1605 - 1608. [Abstract] [Full Text] [PDF]

				N. Fujii, H. Mushiake, and J. Tanji Intracortical Microstimulation of Bilateral Frontal Eye Field J Neurophysiol, April 1, 1998; 79(4): 2240 - 2244. [Abstract] [Full Text] [PDF]