Interaction of the frontal eye field and superior colliculus for saccade generation.

Both the frontal eye field (FEF) in the prefrontal cortex and the superior colliculus (SC) on the roof of the midbrain participate in the generation of rapid or saccadic eye movements and both have projections to the premotor circuits of the brain stem where saccades are ultimately generated. In the present experiments, we tested the contributions of the pathway from the FEF to the premotor circuitry in the brain stem that bypasses the SC. We assayed the contribution of the FEF to saccade generation by evoking saccades with direct electrical stimulation of the FEF. To test the role of the SC in conveying information to the brain stem, we inactivated the SC, thereby removing the circuit through the SC to the brain stem, and leaving only the direct FEF-brain stem pathway. If the contributions of the direct pathway were substantial, removal of the SC should have minimal effect on the FEF stimulation, whereas if the FEF stimulation were dependent on the SC, removal of the SC should alter the effect of FEF stimulation. By acutely inactivating the SC, instead of ablating it, we were able to test the efficiency of the direct FEF-brain stem pathway before substantial compensatory mechanisms could mask the effect of removing the SC. We found two striking effects of SC inactivation. In the first, we stimulated the FEF at a site that evoked saccades with vectors that were very close to those evoked at the site of the SC inactivation, and with such optimal alignment, we found that SC inactivation eliminated the saccades evoked by FEF stimulation. The second effect was evident when the FEF evoked saccades were disparate from those evoked in the SC, and in this case we observed a shift in the direction of the evoked saccade that was consistent with the SC inactivation removing a component of a vector average. Together these observations lead to the conclusion that in the nonablated monkey the direct FEF-brain stem pathway is not functionally sufficient to generate accurate saccades in the absence of the indirect pathway that courses from the FEF through the SC to the brain stem circuitry. We suggest that the recovery of function following SC ablation that has been seen in previous studies must result not from the use of an already functioning parallel pathway but from neural plasticity within the saccadic system.

[1]  A. Fuchs,et al.  Eye movements evoked by stimulation of frontal eye fields. , 1969, Journal of neurophysiology.

[2]  R. Wurtz,et al.  Activity of superior colliculus in behaving monkey. II. Effect of attention on neuronal responses. , 1972, Journal of neurophysiology.

[3]  P. Schiller,et al.  Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. , 1972, Journal of neurophysiology.

[4]  D. Robinson.  Eye movements evoked by collicular stimulation in the alert monkey. , 1972, Vision research.

[5]  R. Wurtz,et al.  Activity of superior colliculus in behaving monkey. IV. Effects of lesions on eye movements. , 1972, Journal of neurophysiology.

[6]  Peter H. Schiller,et al.  The effect of superior colliculus ablation on saccades elicted by cortical stimulation , 1977, Brain Research.

[7]  Peter H. Schiller,et al.  Paired stimulation of the frontal eye fields and the superior colliculus of the rhesus monkey , 1979, Brain Research.

[8]  J. L. Conway,et al.  Deficits in eye movements following frontal eye-field and superior colliculus ablations. , 1980, Journal of neurophysiology.

[9]  G. Leichnetz,et al.  The prefrontal cortico-oculomotor trajectories in the monkey A possible explanation for the effects of stimulation/lesion experiments on eye movement , 1981, Journal of the Neurological Sciences.

[10]  J. E. Albano,et al.  Visuomotor deficits following ablation of monkey superior colliculus. , 1982, Journal of neurophysiology.

[11]  E. G. Keating,et al.  Removing the superior colliculus silences eye movements normally evoked from stimulation of the parietal and occipital eye fields , 1983, Brain Research.

[12]  Hidehiko Komatsu,et al.  Projections from the functional subdivisions of the frontal eye field to the superior colliculus in the monkey , 1985, Brain Research.

[13]  R. Wurtz,et al.  Modification of saccadic eye movements by GABA-related substances. I. Effect of muscimol and bicuculline in monkey superior colliculus. , 1985, Journal of neurophysiology.

[14]  C. Bruce,et al.  Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. , 1985, Journal of neurophysiology.

[15]  C. Bruce,et al.  Primate frontal eye fields. I. Single neurons discharging before saccades. , 1985, Journal of neurophysiology.

[16]  F. Ottes,et al.  Visuomotor fields of the superior colliculus: A quantitative model , 1986, Vision Research.

[17]  L A Krubitzer,et al.  Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. cortical connections , 1986, The Journal of comparative neurology.

[18]  M. Goldberg,et al.  Functional properties of corticotectal neurons in the monkey's frontal eye field. , 1987, Journal of neurophysiology.

[19]  John H. R. Maunsell,et al.  The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey. , 1987, Journal of neurophysiology.

[20]  Hidehiko Komatsu,et al.  A grid system and a microsyringe for single cell recording , 1988, Journal of Neuroscience Methods.

[21]  E. G. Keating,et al.  Saccadic disorders caused by cooling the superior colliculus or the frontal eye field, or from combined lesions of both structures , 1988, Brain Research.

[22]  D. Sparks,et al.  Population coding of saccadic eye movements by neurons in the superior colliculus , 1988, Nature.

[23]  C. Bruce,et al.  Frontal eye field efferents in the macaque monkey: II. Topography of terminal fields in midbrain and pons , 1988, The Journal of comparative neurology.

[24]  D. Sparks,et al.  The deep layers of the superior colliculus. , 1989, Reviews of oculomotor research.

[25]  M. Schlag-Rey,et al.  Colliding saccades may reveal the secret of their marching orders , 1990, Trends in Neurosciences.

[26]  M. Schlag-Rey,et al.  How the frontal eye field can impose a saccade goal on superior colliculus neurons. , 1992, Journal of neurophysiology.

[27]  J. Lynch,et al.  Saccade initiation and latency deficits after combined lesions of the frontal and posterior eye fields in monkeys. , 1992, Journal of neurophysiology.

[28]  M. Segraves.  Activity of monkey frontal eye field neurons projecting to oculomotor regions of the pons. , 1992, Journal of neurophysiology.

[29]  S. Highstein,et al.  The anatomy and physiology of primate neurons that control rapid eye movements. , 1994, Annual review of neuroscience.

[30]  R. Wurtz,et al.  Saccade-related activity in monkey superior colliculus. II. Spread of activity during saccades. , 1995, Journal of neurophysiology.

[31]  M. Segraves,et al.  Acute activation and inactivation of macaque frontal eye field with GABA-related drugs. , 1995, Journal of neurophysiology.

[32]  R. Andersen,et al.  Multimodal representation of space in the posterior parietal cortex and its use in planning movements. , 1997, Annual review of neuroscience.

[33]  J. Schall.  Visuomotor Areas of the Frontal Lobe , 1997 .

[34]  Edward J. Tehovnik,et al.  Reversible inactivation of macaque frontal eye field , 1997, Experimental Brain Research.

[35]  J. Büttner-Ennever,et al.  Anatomical substrates of oculomotor control , 1997, Current Opinion in Neurobiology.

[36]  Michael A. Arbib,et al.  Colliding saccades evoked by frontal eye field stimulation: artifact or evidence for an oculomotor compensatory mechanism underlying double-step saccades? , 1997, Biological Cybernetics.

[37]  M. A. Basso,et al.  Modulation of Neuronal Activity in Superior Colliculus by Changes in Target Probability , 1998, The Journal of Neuroscience.

[38]  R. Wurtz,et al.  Reversible inactivation of monkey superior colliculus. I. Curvature of saccadic trajectory. , 1998, Journal of neurophysiology.

[39]  P. H. Schiller,et al.  The effects of frontal eye field and dorsomedial frontal cortex lesions on visually guided eye movements , 1998, Nature Neuroscience.

[40]  M. Segraves,et al.  Muscimol-induced inactivation of monkey frontal eye field: effects on visually and memory-guided saccades. , 1999, Journal of neurophysiology.

[41]  M. Goldberg,et al.  Space and attention in parietal cortex. , 1999, Annual review of neuroscience.

[42]  D P Munoz,et al.  Neuronal Correlates for Preparatory Set Associated with Pro-Saccades and Anti-Saccades in the Primate Frontal Eye Field , 2000, The Journal of Neuroscience.

[43]  R. Wurtz,et al.  Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus. , 2000, Journal of neurophysiology.