The Electric Signals Originating in the Eye
Fig. 28.3 An illustration of the electro-oculogram (EOG) signal generated by horizontal movement of the eyes. The polarity of the signal is positive at the electrode to which the eye is moving.
Fig. 28.4 An illustration of the eye movement response to a step stimulus (i.e., a spot of light whose horizontal position instantaneously shifts). After a latency the eye rapidly moves toward the new position, undershoots, and moves a second time. The movements are illustrative of saccades, and the parameters include latency, amplitude, velocity, duration, overshooting, and undershooting.
Fig. 28.6 The cells of the retina and their response to a spot light flash. The photoreceptors are the rods and cones in which a negative receptor potential is elicited. This drives the bipolar cell to become either depolarized or hyperpolarized. The amacrine cell has a negative feedback effect. The ganglion cell fires an action pulse so that the resulting spike train is proportional to the light stimulus level.
The second maxima, which is corneo-positive, is the b-wave. To explain its origin we need to note that in the inner retinal layers there are Müler's cells. These cells are glial cells and have no synaptic connection to the retinal cells. The transmembrane potential of Müler's cells depends on its potassium Nernst potential, which is influenced by changes in the extracellular potassium. The latter is increased by the release of potassium when the photoreceptors are stimulated. In addition, the ganglion cell action pulse is associated with a potassium efflux. (The aforementioned electrophysiological events follow that described in Chapters 3 and 4.) The consequence of these events is to bring about a Müler's cell response. And it is the latter that is the source of the b-wave. Müler's cells can contribute to a b-wave from either cone or rod receptors separately.
The c-wave is positive like the b-wave, but otherwise is considerably slower. It is generated by the retinal pigment epithelium (RPE) as a consequence of interaction with the rods.
The oscillatory potentials shown in Figure 28.6 are small amplitude waves that appear in the light-adapted b-wave. Although they are known to be generated in the inner retinal layer and require a bright stimulus, the significance of each wave is unknown. Some additional details are found in the paper by Charles (1979).
In retrospect, the sources that are responsible for the ERG and that lie within and behind the retina, are entirely electrotonic. They constitute a specific example of the receptor and generator potentials described and discussed in Chapter 5. This contrasts with the sources of the ECG in that the latter, which arise from cardiac muscle cells, are generated entirely from action pulses. Nevertheless, as described in Chapters 8 and 9, a double layer source is established in a cell membrane whenever there is spatial variation in transmembrane potential. Such spatial variation can result from a propagating action pulse and also from a spreading electrotonic potential. In both cases currents are generated in the surrounding volume conductor and the associated potential field may be sampled with surface electrodes that register the EOG and ERG. An examination of the ERG volume conductor is given below.
The aqueous humor and vitreous body were assumed to constitute a single region of uniform conductivity since, in fact, they have nearly the same conductivity (σ1).
The sclera (σ2).
The extraocular region was considered to have a uniform conductivity, much the same as simplified models of the ECG consider the torso uniform (σ3).
The lens (σ4).
The cornea (σ5).
The air in front of the eye, which has a conductivity of zero (σ6).
The model includes the R-membrane, which lies at the same radius as the retina and continues to the cornea. This membrane was treated as a distribution of parallel RC elements (RR, RC).
The retina itself was assumed to be the location of a uniform double layer source, considered to extend over a hemisphere.
|Parameter||Structure||Value in model||Dimension|
|σ1||Aqueous & Vitreous||1.0||57 [S/cm]|
|σ2||Sclera||0.01 ... 0.15||57 [S/cm]|
|σ3||Extraocular||0.0005 ... 0.06||57 [S/cm]|
|σ4||Lens||0.08 ... 0.3||57 [S/cm]|
|σ5||Cornea||0.03 ... 0.86||57 [S/cm]|
|RR||R-membrane resistinv.||1.67 ... 6.25||1/57 [Ω/cm²]|
|RC||1/(2πCs)||27.8 ... 58.8||1/57 [Ω/cm²]|
Note: C is the R-membrane capacitance. Division of σi by 57 gives conductivity in [S/cm]. Multiplication of RR, RC, and RXC by 57 gives resistivity in [Ωcm²].|
Source: Doslak, Plonsey, and Thomas (1980).
Fig. 28.7 The two-dimensional model depicting the ERG source and volume conductor inhomogeneities. The retina and R-membrane impedance are represented together by double layer and RR and RC, respectively. The other parameters correspond to the conductivities and are listed in Table 28.1.
In the model described by Figure 28.7 we seek the potential Φ that satisfies
|2Φ = 0||(28.1)|
namely, Laplace's equation subject to the following boundary conditions: At all passive interfaces between regions of different conductivity the normal component of current density is continuous and the electric potential is continuous. For the retinal double layer, the normal component of current density is continuous, but the potential is discontinuous across this source by a value equal to the double layer strength (expressed in volts). Finally, for the R-membrane, the current density is also continuous, but there is a discontinuity in potential; this is given by the product of membrane impedance (Ωcm²) and the normal component of current density. Doslak, Plonsey, and Thomas (1980) solved this by locating a system of nodal points over the entire region and then using the method of finite differences and overrelaxation. Mathematical details are contained in Doslak, Plonsey, and Thomas (1982). The model was used by Doslak and Hsu (1984) to study the effect of blood in the vitreous humor on the ERG magnitude. They were able to establish that little effect on ERG magnitude could be expected from this condition.
du Bois-Reymond EH (1848): Untersuchungen Ueber Thierische Elektricität, Vol. 1, 56+743 pp. G Reimer, Berlin.
Carpenter RHS (1988): Movements of the Eyes, 2nd ed., 593 pp. Pion, London.
Charles S (1979): Electrical signals of the retinal microcircuitry. In Physiology of the Human Eye and Visual System, ed. RE Records, pp. 319-27, Harper & Row, Hagerstown.
Clark JW (1978): The electroretinogram. In Medical Instrumentation, ed. JG Webster, pp. 177-84, Houghton Mifflin, Boston.
Dewar J, McKendrick JG (1873): On the physiological action of light. Proc. Roy. Soc. (Edinburgh) 8: 179-82.
Doslak MJ (1988): Electroretinography. In Encyclopedia of Medical Devices and Instrumentation, Vol. 2, ed. JG Webster, pp. 1168-80, John Wiley, New York.
Doslak MJ, Hsu P-C (1984): Application of a bioelectric field model of the ERG to the effect of vitreous haemorrhage. Med. & Biol. Eng. & Comput. 22: 552-7.
Doslak MJ, Plonsey R, Thomas CW (1980): The effects of variations of the conducting media inhomogeneities on the electroretinogram. IEEE Trans. Biomed. Eng. 27: 88-94.
Doslak MJ, Plonsey R, Thomas CW (1982): Numerical solution of the bioelectric field. Med. & Biol. Eng. & Comput. 19: 149-56.
Granit R (1955): Receptors and Sensory Perception, 369 pp. Yale University Press, New Haven.
Holmgren F (1865): Method att objectivera effecten af ljusintryck på retina. Uppsala Läk. För. Förh. 1: 184-98.
Levick WR, Dvorak DR (1986): The retina - From molecules to networks. Trends Neurosci. 9: 181-5.
Oster PJ, Stern JA (1980): Electro-oculography. In Techniques in Psychophysiology, ed. I Martin, PH Venables, pp. 276-97, John Wiley, New York.
Rahko T, Karma P, Torikka T, Malmivuo JA (1980): Microprocessor-based four-channel electronystagmography system. Med. & Biol. Eng. & Comput. 18:(1) 104-8.
Rodieck RW (1973): The Vertebrate Retina, 1044 pp. Freeman, San Francisco.
Stockwell CW (1988): Nystagmography. In Encyclopedia of Medical Devices and Instrumentation, Vol. 3, ed. JG Webster, pp. 2090-4, John Wiley, New York.
Wiesel TN, Brown KT (1961): Localization of origins of electroretinogram components by intraretinal recording in the intact cat eye. J. Physiol. (Lond.) 158: 257-80.
Young LR, Sheena D (1975): Eye movement measurement techniques. Amer. Physiologist 30: 315-30. (Reprinted in: Encyclopedia of Medical Devices and Instrumentation, Webster, JG, ed., J. Wiley & Sons, New York, vol. 2., pp. 1259-1269, 1988).
Young LR, Sheena D (1988): Eye-movement measurement techniques. In Encyclopedia of Medical Devices and Instrumentation, ed. JG Webster, pp. 1259-69, John Wiley, New York.
Berthoz A, Melvill Jones G (1985): Adaptive mechanisms in gaze control. In Reviews of Oculomotor Research, Vol. 1, ed. DA Robinson, H Collewjin, p. 386, Elsevier, Amsterdam.
Büttner-Ennever JA (1989): Neuroanatomy of the oculomotor system. In Reviews of Oculomotor Research, Vol. 2, ed. DA Robinson, H Collewjin, p. 478, Elsevier, Amsterdam.
Kowler E (1990): Eye movements and their role in visual and cognitive processes. In Reviews of Oculomotor Research, Vol. 4, ed. DA Robinson, H Collewjin, p. 496, Elsevier, Amsterdam.
Wurtz RH, Goldberg ME (1989): The neurobiology of saccadic eye movements. In Reviews of Oculomotor Research, Vol. 3, ed. DA Robinson, H Collewjin, Elsevier, Amsterdam.