Elsevier

Current Opinion in Neurobiology

Volume 9, Issue 6, 1 December 1999, Pages 698-707
Current Opinion in Neurobiology

Review
Conceptual issues related to the role of the superior colliculus in the control of gaze

https://doi.org/10.1016/S0959-4388(99)00039-2Get rights and content

Abstract

Various conceptual issues have been brought into focus by recent experiments studying the role of the superior colliculus in the control of coordinated movements of the eyes and head, the interaction of saccadic and vergence movements, and cognitive processes influencing the initiation and execution of saccades.

Introduction

In primates, photoreceptor cones are concentrated in and around the fovea, and visual acuity falls off sharply as a function of the distance of the image from the fovea. Nonetheless, we rarely notice gradations in spatial resolution when perceiving our environment. The photoreceptors are mounted on a mobile platform, and coordinated movements of the eyes and head implement high spatial frequency samples of the visual environment by shifting the line-of-sight from one part of the visual scene to another. Understanding the strategies and mechanisms by which gaze shifts are used to sample the visual environment and the perceptual processes that integrate information obtained from successive samples is as critical to a complete description of visual perception as is an understanding of events taking place at the retina.

The superior colliculus (SC), a midbrain structure, plays an important role in triggering and organizing orienting movements and is a useful model system for studying the neural computations involved in the translation of sensory signals into motor commands. The body of this review focuses on conceptual issues emerging from a subset of recent papers 1•, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13•, 14, 15••, 16•, 17•, 18, 19•, 20, 21, 22, 23, 24, 25, 26••, 27••, 28••, 29, 30•, 31, 32, 33, 34, 35, 36, 37, 38•, 39•, 40•. Recent work in other important areas (e.g. anatomical studies of the intrinsic and extrinsic connections of collicular neurons 41, 42, 43, 44•, 45, 46, 47•, 48, 49•, 50•, 51, 52, 53, 54, 55, 56, 57, 58, 59••, 60•, 61••, electrophysiological and lesion studies of collicular function 62•, 63••, 64, 65, 66•, 67•, 68, 69, 70, 71, 72, 73•, 74, 75•, 76, 77, 78, 79•, 80•, 81, 82, 83, 84, 85, 86•, 87, 88, the signals carried over afferent and efferent pathways 89•, 90•, 91, and the development and testing of models of collicular function 92•, 93•, 94•, 95•) is listed in the bibliography. Research related to the development of the SC and the development and coordination of sensory and motor maps is periodically reviewed in the Development section of this journal, published every February.

Section snippets

The collicular motor map

What is represented in the collicular map? How is it represented? The SC (or optic tectum) contains a motor map for controlling orienting movements. Local electrical stimulation of the SC in a variety of animals, including primates, produces orienting responses that may involve coordinated movements of the eyes, head, and body (see 1•, 2 and references therein). These stimulation experiments indicate that the SC is involved in the generation of eye, head and body movements, but they provide

Transformation of collicular signals — a neural uncertainty problem?

Much remains to be learned about how the movement-related signals observed in the SC are transformed into those required by the motoneuron pools innervating the extraocular and neck muscles. The physiological and morphological bases for synergistic movements of the eyes and head during orienting responses are well established (see 18, 19• and references therein). For example, signals carried by reticulospinal neurons are related to both neck muscle activity and eye position, and they are

Coping with cognition

Several cognitive processes influence the probability of occurrence, latency, accuracy and speed of saccadic eye movements (see 31, 32 for reviews). Many of these processes probably alter the excitability of neurons (including those in the SC) involved in controlling saccadic movements. Indeed, variations in the discharge pattern of collicular neurons have been ascribed to a number of ‘cognitive’ states: such as spatial attention 33, 34, motor memory [35], response selection [36], motor

Conclusions

Although it has been known for more than 50 years that microstimulation of the SC produces coordinated movements of the eyes and head, it is surprisingly difficult, for technical reasons, to learn how these movements are represented at the level of individual collicular neurons. At this point, the limited pertinent data suggest that the activity of individual collicular neurons specifies a change in gaze. There is no unequivocal evidence that cellular activity specifies movements of the eyes or

Acknowledgements

Most of the concepts considered in this review have been discussed extensively during weekly journal club meetings in my laboratory. It would be difficult to know the actual source of some of the ideas, but Jamie Nichols would probably receive credit for the notion of motor equivalence classes or ‘motomeres’, and Ed Freedman and I have had extensive discussions about ‘neural uncertainty’. Ellen Barton, Raj Gandhi, Paul Glimcher, Laurent Goffart, Jenni Groh, Rimas Kalesnykas, and Terry Stanford

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

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