H. K. Hartline

Spatial and Temporal Aspects of Retinal Inhibitory Interaction

The inhibitory interaction among neural elements in the compound eye of Limulus was investigated by recording impulses from two or more optic nerve fibers simultaneously. The inhibitory influences are exerted mutually and recurrently, with an appreciable time delay, over a network of interconnections among the interacting elements.Under steady conditions of retinal illumination the activity of any group of interacting elements may be described by a set of simultaneous equations, one equation for each element. In each equation the activity of the particular element represented is expressed as the resultant of the excitatory stimulus to it and the opposing inhibitory influences exerted on it by all the others. By also taking account of the time required for an inhibitory effect exerted by one element to act upon another, this quantitative description may be extended to include transient phenomena associated with changes in the pattern of retinal illumination.The influences exerted over the inhibitory network give rise to maxima and minima in the optic nerve responses to spatial patterns of illumination, and to fluctuations in the responses to temporal patterns. The spatial and temporal properties of the responses of the population of interacting elements are analogous to a number of familiar phenomena in human vision and may offer an explanation for them. These properties also lend support to the view that inhibition may play a role in the generation of the transient “on” and “off” responses observed in a wide variety of visual systems.

Inhibitory Interaction in the Retina of Limulus

The interplay of excitation and inhibition lies at the foundation of nervous integrative function. Modern neurophysiology builds on Sherrington’s analysis of motor function, extending his concepts to all the sensory systems and to the infinite complexity of the higher nervous centers (cf. Granit, 1966). Antagonistic processes in vision recall Hering; the role of inhibition in vision was clearly recognized by Mach. Sherrington (1897) himself ventured into this field, but it was Granit’s work that played an essential role in introducing Sherringtonian concepts in the study of retinal function. “The retina is a nervous center” writes Granit, quoting Cajal, and this he proceeds to confirm, exhibiting the interplay of excitation and inhibition in the retinal action potential and in the unitary discharges of retinal ganglion cells.

Fourier analysis of dynamics of excitation and inhibition in the eye of Limulus: amplitude, phase and distance.

Abstract Three basic processes—excitation, self-inhibition and lateral inhibition govern the dynamics of the neural network in the lateral eye of Limulus . Experiments show that all lateral inhibition may be represented by a single transfer function scaled by the summed lateral inhibitory coefficients. Discharges of impulses from three units were recorded simultaneously. Results: 1. (1) Variation in amplitude of excitation produces proportional variation in amplitude of lateral inhibition on a neighboring unit at a fixed distance but no phase shift. 2. (2) The amplitude of lateral inhibition varies with distance to the units affected, but there is no phase shift.

INHIBITORY INTERACTION IN THE RETINA: TECHNIQUES OF EXPERIMENTAL AND THEORETICAL ANALYSIS*

This paper describes the use of a small general purpose digital computer (Control Data Corporation 160-A) as an aid to experimental and theoretical studies of nervous interactions in visual systems. The experimental work has been primarily concerned with the inhibitory interaction in the lateral eye of the horseshoe crab, Limulus polyphemus. The theoretical work has been concerned with developing models of the spatial and dynamical properties of the interactions in this eye, and with the application of these models to the study of the vertebrate retina and to the explanation of more complex visual phenomena encountered in human psychophysib. The earlier experimental work on steady state properties of the eye of Limulus was amenable to relatively simple techniques of data collection such as gated counters and photography. For reviews of this work see Hartline, Ratliff, and Miller (1961) and Ratliff (1961). The work is now being extended to the dynamical properties of the eye. For a review of some of the preliminary observations on dynamics see Ratliff, Hartline, and Miller (1963). In the case of dynamics, the continuous, impulse-by-impulse, collection of very large volumes of data is required. I t is also necessary to have immediate information on the course of the experiment so that adjustments can be made in procedures. The computer is therefore employed at all levels of the study; namely, data collection, data storage, data processing, model simulation, and comparison of experimental and theoretical results. Complete descriptions of the experimental procedure and results of previous studies are readily available in the references cited above, and therefore we will limit ourselves to a short summary as a background to the discussion of the computer techniques. The anatomy of the Limulus lateral eye has been extensively studied by Miller (1957, 1958). FIGURE 1 is a composite three-dimensional light micrograph of a portion of the eye. The upper horizontal plane contains the facets (F) of the corneal surface (c). Light enters more or less perpendicularly to this plane. The upper vertical plane is a view of the longitudinal aspect of the functional units or ommatidia. Each unit has a crystalline cone lens (cc) which focuses an image onto the rhabdom ( r ) . The rhabdom is formed from the convergence of the microvillous borders of a dozen or more retinular cells ( R ) . These retinular cells are radially arranged around the distal process (D. P.)

THE PROCESSING OF VISUAL INFORMATION IN A SIMPLE RETINA

Our lighted surroundings give us an infinite variety of ever-changing patterns of light and shade and color. Imaged on the mosaic of photoreceptors in our retinas, these are translated into patterns of nervous activity, transformed and utilized in various ways by our nervous system to become ultimately the patterns in our brains that underlie visual responses and visual experience. Our own visual system, and those of all other vertebrates and of higher invertebrates, are extremely complex. Even the first steps of visual processing, in the retina, are only slowly being unraveled. It has been useful to search for simpler visual systems. The lateral eye of the common horseshoe crab, Lirnulus, provides such a system. We and our collcagues have been studying it over a nunibers of years.’,.’ The two lateral eyes of Lirriulus are compound, coarsely faceted, rigidly fixed in the shell, each with a long optic nerve running to the central optic lobes of the brain. Behind each facet is a cluster of about 12 receptor cells, and (usually) one eccentrically placed bipolar neuron. Each such “omniatidiuni” acts as a single receptor unit. From the large axon of the eccentric cell can be recorded electrically trains of nerve impulses elicited by illuminating the receptor unit. The individual receptor units are studied either by restricting illumination to each corresponding facet, by dissecting their individual nerve fibers from the optic nerve, or by impaling the eccentric cell in an onimatidiuni by a niicropipette electrode. Illuminated steadily, an isolated receptor unit responds with a steady discharge of impulses, which appear on record as spikelike “action potentials” of uniform amplitude. The rate of impulse “firing” is approximately linear with the logarithm of the light intensity. A range of 1 0 in intensity elicits frequencies of firing that range from a few impulses per second to 60 or 70. There is thus considerable “data compression” by the receptor. Abrupt changes in intensity are accented transiently: Light suddenly turned on elicits a strong initial outburst of neural discharge, which subsides in a second or so to a steady level. Such “sensory adaptation” to a greater or lesser degree is alniost universal for sense organs. In the visual receptor, such adaptation is in part a property of the transducing mechanism (light to receptor excitation). There is, however, a large component of “neural adaptation,” which in Lir?icrIus is a negative feedback-“self inhibition”-exerted on the eccentric cell by its own discharge. The receptor units in the eye of LirnuIus are interconnected by a network of nerve-fiber branches that constitute a true “retina,” rich in synaptic interconnections. This plexus lies just back of the layer of ommatidia. Functionally, the receptor units do not act entirely independently, but interact with one another. These interactions, exerted laterally over the fibers of the plexus, provide another step of data processing in this eye. The influence that the receptor units exert on one another mutually is inhibitory. This is a contrast-enhancing mechanism. The rate of impulse dis-