Journal of Neurophysiology, Vol 39, Issue 4 745-765, Copyright © 1976 by APS

ARTICLES

Organization of monkey superior colliculus: enhanced visual response of superficial layer cells

R. H. Wurtz and C. W. Mohler

1. Cells in the superficial layers of monkey superior colliculus respond more vigorously to a spot of light falling in their receptive fields when the monkey uses that spot of light as the target for a saccadic eye movement. Our purpose in these experiments was to investigate the characteristics of this enhancement effect. While monkeys fixated, we determined the response of a cell to a stimulus falling in its receptive field. Then we determined the response of the cell to the same stimulus when the monkey made a saccade to the stimulus or near to it. 2. The enhancement of the visual response is spatially limited. The receptive field of a cell always shows enhancement throughout its extent and frequently shows a slight expansion. Saccades made near to a stimulus in the visual receptive field, but not to it, also lead to an enhancement of that visual stimulus; an area around the excitatory center of the receptive field where such enhancement occurs was referred to as the enhancement field of the cell. An enhanced response in one part of the visual field was not accompanied by depressed responses associated with saccades to other parts of the visual field. 3. The enhancement effect is temporally limited; it begins 200-300 ms before the eye movement, as determined by the increasing response to 50-ms light pulses presented at varying intervals before the eye movement. The degree of enhancement intensifies when the visual stimulus is turned on closer in time to the onset of the saccade. A buildup of the enhancement also occurs on successive trials as does the response of eye movement-related cells in the intermediate layers. 4. The enhancement response is not present in the upper quarter-millimeter of the superficial layers, suggesting that the effect is not present in retinal afferents which terminate primarily in this area of the superficial layers. The enhancement effect is seen throughout the visual field; the foveal area was not tested. 5. In order to determine the relation of the enhancement effect to the monkey's behavioral response, we required the monkey to make a hand response rather than an eye movement-response to the visual stimuli. Cells did not show a clear enhancement with such a hand response. Results of these experiments indicate that the enhancement effect is dependent on the type of response the monkey makes to the stimulus and is probably specifically related to eye movements. Since the enhancement of visual response seems likely to be related specifically to eye movements both on physiological and behavioral grounds, the response-free term "attention" is probably inappropriate for the phenomenon. 6. The hypothesis advanced in the preceding paper that eye movement-related activity from intermediate and deep colliculus layers is directed upward to converge with visually related activity in the superficial layers is extended to include an input from cells in these deeper layers (or their afferents) to the superficial layer cells...

This article has been cited by other articles:

				X. Li and M. A. Basso Preparing to Move Increases the Sensitivity of Superior Colliculus Neurons J. Neurosci., April 23, 2008; 28(17): 4561 - 4577. [Abstract] [Full Text] [PDF]

				J. Cavanaugh, B. D. Alvarez, and R. H. Wurtz Enhanced performance with brain stimulation: attentional shift or visual cue? J. Neurosci., November 1, 2006; 26(44): 11347 - 11358. [Abstract] [Full Text] [PDF]

				M. Wei and D. E. Angelaki Foveal Visual Strategy during Self-Motion Is Independent of Spatial Attention J. Neurosci., January 11, 2006; 26(2): 564 - 572. [Abstract] [Full Text] [PDF]

				Y. Saito and T. Isa Organization of Interlaminar Interactions in the Rat Superior Colliculus J Neurophysiol, May 1, 2005; 93(5): 2898 - 2907. [Abstract] [Full Text] [PDF]

				M. C. Dorris, R. M. Klein, S. Everling, and D. P. Munoz Contribution of the Primate Superior Colliculus to Inhibition of Return J. Cogn. Neurosci., November 1, 2002; 14(8): 1256 - 1263. [Abstract] [Full Text] [PDF]

				R. M. McPeek and E. L. Keller Saccade Target Selection in the Superior Colliculus During a Visual Search Task J Neurophysiol, October 1, 2002; 88(4): 2019 - 2034. [Abstract] [Full Text] [PDF]

				D. M. Clower, R. A. West, J. C. Lynch, and P. L. Strick The Inferior Parietal Lobule Is the Target of Output from the Superior Colliculus, Hippocampus, and Cerebellum J. Neurosci., August 15, 2001; 21(16): 6283 - 6291. [Abstract] [Full Text] [PDF]

				B. J. Casey, K. M. Thomas, T. F. Welsh, R. D. Badgaiyan, C. H. Eccard, J. R. Jennings, and E. A. Crone Dissociation of response conflict, attentional selection, and expectancy with functional magnetic resonance imaging PNAS, July 18, 2000; 97(15): 8728 - 8733. [Abstract] [Full Text] [PDF]

				G. Ozen, G. J. Augustine, and W. C. Hall Contribution of Superficial Layer Neurons to Premotor Bursts in the Superior Colliculus J Neurophysiol, July 1, 2000; 84(1): 460 - 471. [Abstract] [Full Text] [PDF]

				M. A. Basso and R. H. Wurtz Modulation of Neuronal Activity in Superior Colliculus by Changes in Target Probability J. Neurosci., September 15, 1998; 18(18): 7519 - 7534. [Abstract] [Full Text] [PDF]

				P. H. Lee, M. C. Helms, G. J. Augustine, and W. C. Hall Role of intrinsic synaptic circuitry in collicular sensorimotor integration PNAS, November 25, 1997; 94(24): 13299 - 13304. [Abstract] [Full Text] [PDF]

				M. L. Platt and P. W. Glimcher Responses of Intraparietal Neurons to Saccadic Targets and Visual Distractors J Neurophysiol, September 1, 1997; 78(3): 1574 - 1589. [Abstract] [Full Text] [PDF]

				Duhamel JR, C. Colby, and M. Goldberg The updating of the representation of visual space in parietal cortex by intended eye movements Science, January 3, 1992; 255(5040): 90 - 92. [Abstract] [PDF]

				C.L. Colby The Neuroanatomy and Neurophysiology of Attention J Child Neurol, January 1, 1991; 6(1_suppl): S90 - S118. [Abstract] [PDF]

				S. Wise and R Desimone Behavioral neurophysiology: insights into seeing and grasping Science, November 4, 1988; 242(4879): 736 - 741. [Abstract] [PDF]

				N. Gaither and B. Stein Reptiles and mammals use similar sensory organizations in the midbrain Science, August 10, 1979; 205(4406): 595 - 597. [Abstract] [PDF]