Neural mechanisms underlying target selection with saccadic eye movements

Prog Brain Res. 2005:149:157-71. doi: 10.1016/S0079-6123(05)49012-3.

Abstract

In exploring the visual scene we make about three saccadic eye movements per second. During each fixation, in addition to analyzing the object at which we are looking, a decision has to be made as to where to look next. Although we perform this task with the greatest of ease, the computations to perform the task are complex and involve numerous brain structures. We have applied several investigative tools that include single-cell recordings, microstimulation, pharmacological manipulations and lesions to learn more about the neural control of visually guided eye saccadic movements. Electrical stimulation of the superior colliculus (SC), areas V1 and V2, the lateral intraparietal sulcus (LIP), the frontal eye fields (FEF) and the medial eye fields (MEF) produces saccadic eye movements at low current levels. After ablation of the SC, electrical microstimulation of V1, V2, and LIP no longer elicits saccadic eye movements whereas stimulation of the FEF and MEF continues to be effective. Ablation of the SC but not of the FEF eliminates short-latency saccadic eye movements to visual targets called "express saccades," whereas lesions of the FEF selectively interfere with target selection. Bilateral removal of both the SC and the FEF causes major, long lasting deficits: all visually elicited saccadic eye movements are eliminated. In intact monkeys, subthreshold electrical microstimulation of the FEF and MEF as well as the lower layers of V1 and V2 and of some subregions of LIP greatly facilitates the choice of targets presented in the receptive fields of the stimulated neurons. By contrast, stimulation of the upper layers of V1 and V2 and other sub-regions of LIP produces a dramatic interference in target selection. Examination of the role of inhibitory circuits in eye-movement generation reveals that local infusion of muscimol, a GABA (gamma-aminobutyric acid) agonist, or bicuculline, a GABA antagonist, interferes with target selection in V1. On the other hand, infusion of bicuculline into the FEF produces facilitation in target choice and irrepressible saccades. It appears therefore that inhibitory circuits play a central role in visual analysis in V1 and in the generation of saccadic eye movements in the FEF. It is proposed that two major streams can be discerned in visually guided eye-movement control, the posterior from occipital and parietal cortex that reaches the brainstem via the SC and the anterior from the FEF and MEF that has direct access to the brainstem oculomotor centers.

Publication types

  • Research Support, N.I.H., Extramural
  • Review

MeSH terms

  • Animals
  • Cerebral Cortex / anatomy & histology
  • Cerebral Cortex / physiology*
  • Fixation, Ocular / physiology*
  • Haplorhini
  • Humans
  • Interneurons / metabolism
  • Nerve Net / anatomy & histology
  • Nerve Net / physiology*
  • Neural Inhibition / physiology
  • Psychomotor Performance / physiology*
  • Saccades / physiology*
  • Superior Colliculi / physiology
  • Visual Pathways / anatomy & histology
  • Visual Pathways / physiology*
  • gamma-Aminobutyric Acid / metabolism

Substances

  • gamma-Aminobutyric Acid