Major Anatomic Features of the Eye

Figure 2.1 illustrates schematically the major components of the human eye, which resembles that of most other primates. The sclera is a tough outer coat that is fibrous in humans but contains bone or cartilage in some other vertebrate species. The cornea is continuous with the sclera and provides the first element of the refracting media that bend the light to form an image on the retina. The lens lies behind the iris and in front of the vitreous humor, which fills the greater part of the globe. Aqueous humor fills the posterior chamber (the space between the lens and iris) and the anterior chamber (the space between the iris and the cornea). The posterior and anterior chambers are continuous through the pupil, the aperture formed by the iris.

The general features of the retina, the multilayered neural structure lining the back of the eyeball, can be visualized in the living eye with an ophthalmoscope or special camera (Figure 2.2). Axons leave the retina through the optic disc or optic papilla and enter the optic nerve to reach the brain. At the posterior pole of the eye, the retina thins to form the fovea, an area specialized for high-acuity vision. The visual axis is an imaginary line from the fovea through the center of the pupil (Figure 2.1). Behind the retina is the pigment epithelium, which is separated from the sclera by the vascular choroid.

This chapter provides an overview of the projections from the retina to the brain in vertebrates and reviews the key terms used in describing the pathway. The major components of the pathway and their functions are examined in greater detail in subsequent chapters.

The Visual Fields

The central projections of the two eyes map the visible world onto the brain. To understand this process, it is important to know how the visual field of each eye is described and how the projections from the two eyes are combined in the central pathways. The retina of each eye is conventionally divided into nasal and temporal parts, on the basis of proximity to the nose or temporal bone, respectively. Similarly, the visual field of each eye is divided into nasal and temporal parts, and because of the inversion of the retinal image by the eye's optics, the nasal visual field is imaged on the temporal retina, and the temporal field on the nasal retina. Figure 4.1 schematizes the projections of the visual fields in an animal whose eyes are located at the sides of its head. In such lateral-eyed animals, the axons from one retina generally cross completely in the optic chiasm, so that the input from that eye is directed at the contralateral hemisphere of the brain.

Figure 4.2 illustrates diagrammatically the monocular visual fields as they would appear to a frontal-eyed human observer, left eye (oculus sinister, O.S.) on the left, right eye (oculus dexter, O.D.) on the right.

When the eyes face the front, the central part of the visual field is imaged on both retinas (see Figure 4.4). This bestows certain advantages for depth perception, but also creates a formidable problem for the brain: how to ensure that the two retinal images are transformed to yield a unified perception of the part of the visual field seen by both eyes. Failure to achieve this, which sometimes happens in pathological conditions of the nervous system, results in diplopia, the perception that there are two objects when there really is only one. Diplopia can be demonstrated by pushing gently on the skin at the side of one eye to misalign the two visual axes.

Binocular Single Vision

The encoding of the two retinal images of a single object to yield a unique perception results in perceptual fusion of the two images. In discussing fusion, it is important to distinguish between it and two other phenomena, fixation and focus. If the visual axis of one eye is directed at an object so that the image is positioned on the fovea, the eye is said to fixate the object. It is possible to deliberately place an image outside the fovea, but the term “fixation” is generally used to mean foveal fixation. The fixated object will be in focus only if its distance from the eye and the power of the eye's optics permit the formation of a crisp retinal image.

Morphologic and physiologic studies have identified many regions of the cerebral cortex that are involved in vision. All of these are, in some sense, “Visual cortex,” but this term also has more restricted meanings. “Primary visual cortex” refers to a region of distinctive cytoarchitecture that the anatomist Brodmann designated area 17. In primates, this is the principal target of the geniculo-cortical projection. Echoing this fact, as well as its appellation of primary visual cortex, area 17 is sometimes designated VI. The term “striate cortex” arises from the presence in humans of the stria of Gennari, a prominent horizontal band in area 17 that stains heavily for myelin and is visible to the naked eye in fresh tissue. It is also called the calcarine cortex because it lies adjacent to the calcarine sulcus. Visually responsive regions outside area 17 are collectively called extrastriate areas and will be treated later in this chapter.

Effects of Lesions in Striate Cortex

Humans with complete destruction of the striate cortex on one side cease to perceive stimuli in the contralateral visual field. Partial lesions result in localized scotomata, which may be more or less “dense” depending on how much function remains. Sometimes vision is reduced to detection of motion or the presence of light. When the striate cortex and nearby regions are ablated in nonhuman primates, severe deficits are observed in tasks that presumably require visual perception. Ablation of visual cortex in other animals does not always produce such striking deficits.

This textbook is an attempt to answer a question: What would I want a student to know about the visual system before beginning work in my laboratory? Draft versions have been used for several years in an undergraduate course at Brown University. Inevitably, the content and approach of the book have been colored by my expectations of students in that course and by my own particular interests. It is assumed that students will have had an introductory course on the nervous system and will be acquainted with the fundamentals of cellular neurophysiology and the general organization of the vertebrate central nervous system. Minimal knowledge of physics is assumed, so some time will be spent on the elementary principles of optics as they apply to visual systems. Although the book is intended primarily for undergraduates, it can provide useful background for beginning graduate students if supplemented by material from the research literature.

The text is organized into three parts. Part I treats the eye as an imageforming organ and provides an overview of the projections from the retina to key visual structures of the brain. Part II examines the functions of the retina and its central projections in greater detail, building on the introductory material of Part I. Part III treats certain special topics in vision that require this detailed knowledge of the structure and properties of the retina and visual projections.

Photoreceptor Anatomy

Figure 5.1 illustrates the basic components of vertebrate photoreceptors. The outer segment is a specialized cilium containing large numbers of disc-like expansions of the cell membrane. The outer segment is connected by the ciliary stalk to the inner segment, a structure that acts as a light pipe, guiding incident photons to the light-sensitive pigments. The inner segment also contains large numbers of mitochondria that house part of the biochemical machinery required to meet the metabolic needs of the photoreceptor. An axon-like process of variable length connects the cell body to the synaptic terminal, where contact is made with the next elements of the visual pathway. Vertebrate retinas generally possess two types of photoreceptors, called rods and cones, after the shapes of their outer segments. The receptor schematized in Figure 5.1 is a rod. As the name implies, the outer segments of cones taper toward the tip.

The electron micrograph of a rhesus monkey's cone in Figure 5.2 shows the ciliary stalk and part of the outer segment with its stack of discs, including discs newly forming near the ciliary stalk (arrow). The photopigments, which absorb light and initiate the visual process, form a major structural element in these membranous discs. Also visible in the figure are the mitochondria packing the inner segment. In cones, the disc membranes are continuous over the surface of the outer segment and present one face to the extracellular space. Rods differ in that the newly formed discs pinch off from the plasma membrane and are stacked like poker chips inside the more or less cylindrical outer segment.

This chapter introduces certain physical principles that are important to an understanding of how images are formed by optical systems. We then treat the structures and mechanisms in the human eye that produce the retinal image and determine its quality.

It is useful to begin by briefly discussing light as an oscillating electromagnetic field, because many properties of optical systems such as that of the eye depend on the nature of these fields. An electromagnetic field arises from the motion of a charge and propagates away in all directions perpendicular to the charge's axis of movement. Figure 3.1 A illustrates this schematically for a charge oscillating sinusoidally in the plane of the page. The sinusoidal wave depicted represents only the electric field produced by the moving charge; at right angles to the electric field, normal to the plane of the page, is an oscillating magnetic field. Seen from above (Figure 3.IB), the electromagnetic field, represented here by the positive peaks of its electric component, propagates away from the charge as a succession of curved wave fronts that can be treated as planar at some distance from the source (right side of Figure 3.IB). Depending on the situation, it is convenient to think of light either as an advancing wave front or as a ray, the latter usually being represented by an arrow normal to the advancing wave front.

Scatter, Interference, and Transparency

When a propagating wave front of light encounters matter, charges in the matter experience the alternating electromagnetic field, and some are set in motion.

Eyes admit light from a limited range of directions, so it is important that an animal be able to redirect its gaze to examine its surroundings. This is achieved by movements of the body, the head, and usually the eyes as well. Animals also use vision to guide movements of the body, and one would like to understand the way in which visual sensory information is transformed into motor commands. The relative simplicity of ocular movements, as compared, for instance, to movements of the arm, makes them useful for the study of such sensorimotor transformations.

The angle over which an animal can sweep its direction of gaze by moving its eyes alone is called its oculomotor range. This varies from species to species. The oculomotor range of a cat is about 50°, and that of macaque monkeys and humans about 90°. Owls rotate their tubular eyes only about 3° in the orbits, but a very mobile head compensates for this. Chameleons can rotate their turret-like eyes independently. Invertebrates employ a variety of mechanisms to explore their visual environments. Compound eyes that are fixed to the exoskeleton are moved by head or body movements. Jumping spiders are able to move their retinas behind the fixed lenses of their ocelli, and certain copepods also have mobile ommatidia and secondary lenses that scan the image created by stationary optics at the body surface. Decapod crustaceans, such as lobsters and crabs, can move their stalked eyes in drifts, tremors, and saccades independently of head and body movements.

Cell Types and Laminae of the Vertebrate Retina

The retina is a part of the brain that is displaced into the periphery during embryonic development (see Chapter 2). Because it is relatively accessible, retinal tissue provides a useful experimental model of brain circuitry. Some of the most significant advances in our understanding have come from studies of the retinas of cold-blooded vertebrates, which contain large neurons amenable to intracellular recording and staining. Mud puppies, turtles, frogs, and fish have been particularly rich sources of information. The cells of the mammalian retina are more difficult to study, but much work has been done in primates, cats, rabbits, and rats. Although some general patterns of organization have emerged, it is clear that no retina is exactly like any other, not even among mammals. This must be kept in mind when extrapolating from the wealth of comparative data to mammalian retinas, and particularly primate retinas.

The lamination of the retina is a guide to the locations of the various cell types and to the regions in which they make synaptic contacts. The somata or perikarya of the photoreceptors form the outer nuclear layer (Figure 6.1), and their inner and outer segments lie between this layer and the pigment epithelium. Axonal processes of the photoreceptors extend toward the outer plexiform layer, where they establish contacts with bipolar cells and horizontal cells. The somata of bipolar cells and horizontal cells share the inner nuclear layer with those of amacrine cells, interplexiform cells, and Müller cells (glial cells unique to the retina).

The physicist Richard Feynman once illustrated the extraordinary nature of vision as follows: We are immersed in a sea of electromagnetic waves whose lengths vary over a huge range (Figure 1.1). These waves interact with each other and with objects around us to present a cacophony of electromagnetic signals to our eyes. Through a tiny aperture, about 2 mm in diameter, the eye selects a small fraction of these wavelengths and, together with the brain, reconstructs the position, shape, color, and motion of each object we see around us. Feynman compared the situation to that of a water bug floating on the surface at one corner of a swimming pool. The only information available to the bug comes from the movements of its body caused by the waves that reach it. Were the bug able to reconstruct from these waves the positions and motions of all the people entering, leaving, and swimming in the pool, it would be doing something similar to what the eye and brain do with the minuscule electromagnetic disturbances passing through the pupil.

Why does the eye normally respond only to electromagnetic energy with wavelengths in the range 400–700 nm (1 nm = 10-9 m)? To answer this question, one must ask what electromagnetic energy was available to the earliest living forms that developed vision. The major source of such energy reaching the surface of the earth is the sun, which emits radiation with the spectrum shown in Figure 1.2.

Introduction

Numerous authors writing under the influence of Pavlov's (1928) seminal contribution have stressed the importance of individual differences in personality (or “temperament”) to the explanation of OCD and other dysthymic disorders (for example, neurotic depression, phobias, etc.). Most notable among these authors is Eysenck, through whose work (e.g., 1952, 1979) this personality theory approach is linked to the behavioural/learning account of OCD and phobias (see Chapter 2). A brief outline of this approach, along with some points of general relevance to it, will be followed by more detailed discussions of two recent contributions from this school – those of Gray (1982) and Claridge (1985) – and, in particular, the accounts these authors offer of OCD.

Eysenck's account, and suggested modifications of it

As discussed in Section 2.1, Eysenck considers OCD and phobias to result from the operation of conditioning mechanisms. Consistent with this, he holds that those people who are most inclined to develop conditioned responses (argued to be those who tend toward neurotic introversion) are those in whom these disorders are most likely to be observed.

Gray (1970) suggests, among other modifications of Eysenck's account, that it may only be in settings involving signals of “frustrative non-reward” or punishment that neurotic introverts are more inclined to develop conditioned responses.

Gray (1979, 1982) also denies, as does (to some extent) Claridge (1985), that it is the hypothesised greater inclination among neurotic introverts to develop conditioned responses that explains most cases of OCD and phobias.

Introduction

The standard diagnostic criteria for OCD have been challenged, and an alternative analysis has been proposed that suggests that no single feature or collection of features is both common and peculiar to all instances of the disorder. Consistent with this position, it was also argued that there is no single way in which OCD may be distinguished either from phobias or from delusional states; and various ways in which OCD may be so distinguished were presented.

The difficulties encountered by the theoretical approaches to OCD that have been reviewed are perhaps more striking than their successes, at least if one attempts to regard any of these approaches as providing a full explanation of the disorder. Nonetheless, some of the accounts that have been considered certainly offer observations and suggestions that concern some OCD patients and that may well be of importance to any valid account of these patients’ psychopathology that eventually emerges. The following observations have been presented as being of possible theoretical importance to an explanation of OCD:

1. OBSERVATION (1) Evolutionary influences may have a role in selecting the content of some OCD symptoms (stressed by some behavioural writers and some of the Pavlovian personality theorists).

2. OBSERVATION (2). The basal ganglia (among other possible biological factors) may have a role in producing at least some cases of OCD.

3. OBSERVATION (3). A neurotic temperament is displayed by many OCD patients (stressed by the Pavlovian personality theorists).

4. OBSERVATION (4). OCD is co-morbid with certain other disorders (stressed by both the Pavlovian personality theorists and Janet's account).

5. […]