Elsevier

Neuroscience

Volume 198, 15 December 2011, Pages 205-212
Neuroscience

System
Review
Exploring the role of the substantia nigra pars reticulata in eye movements

https://doi.org/10.1016/j.neuroscience.2011.08.026Get rights and content

Abstract

Experiments that demonstrated a role for the substantia nigra in eye movements have played an important role in our understanding of the function of the basal ganglia in behavior more broadly. In this review we explore more recent experiments that extend the role of the substantia nigra pars reticulata from a simple gate for eye movements to include a role in cognitive processes for eye movements. We review recent evidence suggesting that basal ganglia nuclei beyond the substantia nigra may also play a role in eye movements and the cognitive events leading up to the production of eye movements. We close by pointing out some unresolved questions in our understanding of the relationship of basal ganglia nuclei and eye movements.

This article is part of a Special Issue entitled: Function and Dysfunction of the Basal Ganglia.

Highlights

▶Substantia nigra pars reticulata—a saccadic gate? ▶The substantia nigra—movement or cognition? ▶Eye movements—beyond the substantia nigra.

Section snippets

Overview

Saccadic eye movements are rapid movements of the eyes that reorient the line of sight. Many regions within the forebrain, midbrain, and hindbrain are involved in the generation and control of saccades. Information from the cerebral cortex is sent to the midbrain superior colliculus (colliculus) and pontine nuclei through at least two pathways. One pathway arises from cerebral cortical neurons and targets the colliculus and pons directly (Fries, 1984, Harting et al., 1992). These cortical

Substantia nigra pars reticulata—a saccadic gate?

The relationship between saccadic eye movements and neuronal activity in the nigra was first documented with recordings performed in cat and monkey (Hikosaka and Wurtz, 1983a, Hikosaka and Wurtz, 1983b, Hikosaka and Wurtz, 1983c, Hikosaka and Wurtz, 1983d, Joseph and Boussaoud, 1985). Based on this work, the standard model is that the role of the nigra in saccades is to provide tonic inhibition to the superior colliculus, which when released, permits collicular output neurons to send command

The substantia nigra—movement and cognition?

A larger question is the extent to which the basal ganglia should be considered a motor circuit, as opposed to a cognitive circuit. In light of the nigra's putative preference for memory-guided saccades, and related lines of evidence that the basal ganglia may be preferentially involved in movements that are generated by internal rather than external cues (Wichmann and Kliem, 2004, Turner and Anderson, 2005), it may be more accurate to think of the network as communicating cognitive goals to

Eye movements—beyond the nigra

Many advances in our knowledge of basal ganglia circuitry have taken place in recent years. Anatomically based models emphasizing the dichotomy between the direct and indirect striato-nigral/pallidal pathways are being updated with models that emphasize the reciprocal and branching nature of the projections between basal ganglia structures. Similarly, physiological models based on increases and decreases in discharge rates are being replaced with models emphasizing the temporal structure of

Conclusions and future directions

A recurring theme in this review has been the diversity of signals found in the nigra and other basal ganglia structures. It is clear that the system is more complex than described in early articles. A major challenge is to understand the implications of this diversity at the structure-function level. Is it a general rule that different signals go to different targets, as suggested by the elegant work of Jiang et al. (2003)? This is attractive in that it implies a simple channeling of like

Acknowledgments

The work in our laboratories is supported by NIH EY13692, EY019663, NS065776 (M.A.B.), EY017592 (M.A.S.), NCRR P51 RR000167 awarded to the Wisconsin National Primate Research Center and an NIH core grant in Vision Research P30 EY0166665.

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