Electrodes and the recording of the human electroretinogram (ERG)

INTERNATIONAL JOURNAL OF PSYCHOPHYSIOLOGY International

Electrodes

Journal

of Psychophysiology

and the recording

16 (1994) 131-136

of the human electroretinogram

(ERG)

Colin Barber Medical Physics Department,

*

Queen’s Medical Centre, Unicersity Hospital, Nottingham (Accepted

17 January

NG7 ZUH, UK

1994)

Abstract The development of electrodes for recording the human electroretinogram the different types in use are described and evaluated. The relation performance for examining it.

the dipole

model of the origin of electroretinographic

Key wouds: Electrode; Electroretinogram;

Dipole; Contact-glass;

1. Introduction Electroretinography in man is founded upon the electrical accessibility of the retina. The millions of photoreceptors and the intricate layered neuronal architecture of the retina are separated from the outside world by relatively well-conducting media. Thus, an electrode on the cornea is optimally positioned to detect current flow from the proximal retina. The distal surface is well supplied with blood via the richly vascularised pigment epithelium, and so a reference electrode located on soft tissue nearby has a good electrical connection with it. Hence a pair of external electrodes may, to a good approximation, be consid-

* Tel.: (0602) 709131; Fax: (0602) 422745. 0167.8760/94/$07.00 0 1994 Elsevier SD1 0167-8760(94)00010-C

Science

is reviewed. The salient features of

of different signals and suggestions

types is used as a basis are made for imposing

Fibre; Foil; Cornea1

ered to pick up the potential difference across the retinal layer. The major effort in designing ERG electrodes has been, in the first instance, to make them comfortable and stable. More recently, with the advent of the pattern ERG (PERG), the requirements of a general-purpose ERG electrode have been extended to include the retention of clear vision. This has led to the development and clinical use of a wide variety of electrode types, including skin electrodes. These various types differ significantly in their area, location and nature of electrical contact. These differences suggest that a reconsideration of the basic assumptions regarding the eye as a current source may be appropriate; particularly the validity of considering the retina as a dipole, and the stationarity of this dipole in different states of adaptation.

B.V. All rights reserved

132

C. Rarher / It~ternational

Journal

2. Making contact with the cornea The method of making an electrical connection with the cornea has changed little in principle since the young British physicist Dewar [I] measured the first human ERG in 1877. His method, which only worked with the subject supine, was to construct a small trough of clay around the margin of the orbit and fill it with saline solution. Into this he dipped a metallic electrode. For a reference electrode, the subject put his hand in a large clay trough filled with saline; an arrangement which may have been borrowed from contemporary methods of recording the electrocardiogram. The principle of making contact with the highly sensitive cornea1 surface by means of a saline bridge has remained: only the design of the container has advanced. Hartline [2] made an improvement by using goggles to contain the saline, thus permitting the subject to remain upright. The most significant advance was made independently by Riggs [31 and Karpe [4] who mounted the metallic electrode on a contact glass. They produced an elcctrode which was markedly superior in terms of baseline stability and which gave a good signalto-noise ratio. The metallic electrode (generally silver/silver chloride) was carried on an arm which projected from the contact glass, thus raising the possibility that the effective contact might be limited to a particular location on the cornea, which might vary from one electrode to another. An extensive series of investigations by Sundmark [5], using a contact glass fitted with multiple metallic electrodes around its diameter, established that the potentials are of constant amplitude across the cornea. It was not clear, though, whether this was intrinsically so, or whether it was due to the saline bridge between eye and lens. Improved designs of contact glass electrode were produced by Henkes [6], also by Burian and Allen [7]. They became, and remain, the electrodes of choice for clinical work, the former being particularly popular in Europe and the latter in the USA. This fact notwithstanding, numerous “improved” contact glass electrodes were introduced in the following years. The main improvements

of Psychophysiology

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sought were an increase in stability and greater comfort for the subject. One way forward was effectively to make the saline viscous. Jacobson [8] used saline in methyl cellulose and many workers used the hydrophilic gel (then being introduced for soft contact lenses) soaked in saline. This offered the appealing combination of both a stable saline bridge and increased user comfort. It was, unfortunately, a difficult material with which to work and no satisfactory method was ever found to attach a lead to it. Thus, Dawson et al. [9] used it as a cushion beneath a conventional glass electrode, whilst Schloessler and Jones [IO] simply trapped a fine platinum or gold wire between a pair of soft lenses. A similar but more complicated approach was followed by Barber et al. 1111 who spin-polymerised a layer of hydrophilic gel onto the inside of a hard lens, into which a carbon ring electrode had been set. This had the advantage that it was free from photo-voltaic artefact, which can be seriously intrusive in a bright flash ERG. At around the same time, Sieving et al. [12] proposed using a cotton wick with a Burian-Allen electrode for the bright-flash ERG. There had been a number of earlier experiments to overcome the problem of the photo-voltaic artefact; probably the best was simply to use black paint on the electrode-bearing tube [13]. A serious problem with any of the gel-type electrodes is that of sterilisation. They are very difficult to sterilise and, even in pre-AIDS times, this was a cause for concern. The only practical procedure is to regard them as single-use electrodes, and this is the approach that has been adapted in more recent gel-based electrodes [14,15]. This single-use approach has also been developed “hard” contact adopted in recently lens electrodes [ 161.

3. Retaining

clear vision

The contact glass electrodes described above were designed for measuring a flash ERG; optical quality was not important. Some versions even

C. Barber / Intrrnutional Journal of Psychophysiolo~ 16 (1994) ISI -136

used translucent material designed to increase light scatter and thus increase the uniformity of the stimulus across the retina. Some contact-glass electrodes were made in fenestrated versions [ 171, but generally they were not successful. If the fenestration was large the cornea became dry, whilst, if it was very small, it was difficult to keep it properly aligned. Plano lenses could be made to carry the electrode, but the differing radii of curvature of individual eyes meant that the bridging saline produced liquid lenses of differing powers. The only really effective way of retaining clear vision whilst using a contact glass electrode was described by Bloom and Sokol [lg]. They used a soft lens under a Burian-Allen contact glass and then corrected the vision by means of an external lens in a trial frame. This was effective, but too tedious and time consuming for routine clinical use. Their aim in developing this procedure was to record the ERG to a checkerboard-patterned stimulus [19]; then a relatively novel method of obtaining an ERG from primarily the macular region. The present clinical popularity and usefulness of the pattern ERG is due mainly to the introduction of a completely new kind of cornea1 electrode, which obviated the need for the lengthy procedure described above. Generically this is known as the foil/fibre type of electrode and there are several different versions. Their unifying characteristic is that they are small, lightweight devices which contact the cornea without covering the pupil. Contact is made over a restricted area, which differs somewhat between versions but is always much less than the whole-cornea contact achieved with a contact glass electrode. Thus they rely on the assumption that the cornea is an equipotential surface. Interestingly, despite their popularity for PERG recording, they were initially developed as more comfortable electrodes for long-term recording of the flash ERG. The earliest reported [20] utilised aluminiumcoated mylar film which was bent into a J-shaped curve with its short end resting lightly against the cornea. In use, the aluminium coating proved electrically unstable and this design was soon superseded by gold-coated mylar [21,22], which has gained wide acceptance. A different ap-

133

proach was followed by Dawson et al. [23] who used a technique reminiscent of the old saline wick electrodes, but with a low-mass silver-impregnated fibre which floats on the cornea and is barely perceptible. This is known as the DTL electrode and it is also in common use. Yet another approach utilised a lightweight electrode which hooked over the lower lid [24,25]. The latter workers used carbon fibre as the conducting material, thus retaining the freedom from the photo-voltaic artefact. Later workers developed variations on the construction [26] or method of usage [27] of particular types of electrodes, illustrating a continuing need for laboratories to develop their skills in applying the electrode of their choice. There is still no universally-accepted and foolproof cornea1 electrode. A completely different approach to retaining clear vision, and one that has particular advantages in recording the ERG from a traumatised eye, is to use an electrode which does not make direct contact with the cornea, but is affixed to the skin close to the eye. The possibility of using this technique was demonstrated early on [28] and it has been used clinically for both flash [29] and pattern [30] ERGS. The positioning of the electrodes is obviously very important, as is the direction of the gaze of the subject [31]. Generally, the lower eyelid is accepted as the best location for the recording electrode [32], with the subject being instructed to maintain a forward gaze. The reference electrode is placed either on the outer canthus (which undoubtedly picks up some retinal signal) or on the mastoid (which has a larger muscle path between the electrodes and can introduce more noise). The signal-to-noise ratio is intrinsically poor and averaging is necessary to achieve a good signal-to-noise ratio, even with the flash ERG. Thus it is difficult to obtain a fully dark-adapted ERG. Proponents of the technique argue that, although the sequence of stimuli necessary for averaging destroys total dark adaptation, it does offer a stable state of adaptation for recording if the responses to the first few flashes (which can be regarded as adapting flashes) are discarded. Whatever the merits of the argument, the use of skin electrodes in traumatised eyes and in measuring paediatric ERGS is

134

C. Barber/International

Table 1 Electrode

characteristics,

Electrode

type

Contact Lens JET C-Glide Gold foil DTL Skin

Extracted

from Robhins

Journal

and Turner

Contact Lens JET C-Glide Goldfoil DTL Skin

was a Henkea

type.

Movement

Artefacts

Single response signal:noise

b-wave %

signaknoise

b-wave %

Fair (anaesthetic) Fair (anaesthetic) Fair Good Good Good

Fair Fair Easy Fair Easy Fair

Good Good Fair Fair Fair Poor

Good Good Fair Fair Fair Poor

105:l 40: 1 25:l 2O:l 5:1 3:l

100 (525 PV) 7h 67 57 19 I2

> 1OO:l > 1OO:l 85:l 4O:l 30: I 2O:l

IO0 (450 FV) 81 94 44 33 9

of electrodes

Table 2 Amplitudes recorded by various electrodes. (1993). The contact lens used for comparison len type. type

lens used for comparison

Placement

Early comparisons, such as those carried out by the 1961 ISCERG Standardisation Committee found virtually no difference in performance between all the types available then. This is not, perhaps, surprising, since the differences between the various contact glasses were essentially of detail. The situation now is that there are significant differences between the different kinds of foil/fibre electrodes, bigger differences between them and traditional cornea1 electrodes and bigger differences again with skin electrodes. A number of studies have addressed the issue, concentrating on factors such as ease of placement, electrode (and baseline) stability, user comfort, size of signal, noise level and so on. A wide survey of electrode types, under a variety of stimulus conditions (though with data from only a

Electrode

(1988). The contact

16 (1994) 131-136

Comfort

likely to increase and so some standard for averaged “dark-adapted” ERGS should be developed.

4. Comparison

of Psychophysiology

b-wave amplitude

From Kriss et al. was a Burian-Al-

Averaged

response

single subject) was carried out by Robbins and Turner [33]. An extract from their findings, summarised in Table 1, illustrates that there is no ideal electrode. Each have their merits and dcmerits and the electrode of choice depends on the particular application. More recently Kriss et al. [34] have surveyed the same electrode types with a particular emphasis on signal size. Their results, which are summarised in Table 2, show good agreement with those of Robbins and Turner in that the amplitude order of the electrode types is the same. There are, however, some more subtle differences. Under different conditions of adaptation the amplitude ratios between different types of electrode do not remain constant. It is particularly apparent if the other types are compared with skin electrodes. This finding is also seen in a comparison carried out by Wali and Leguire [35], who noted that the b-wave amplitude ratio between ERGS recorded using a gold foil electrode and a skin electrode increased with stimulus luminance, and varied from 1.83 to 7.68. Further work by Papakostopoulos et al. [36] has demonstrated a ratio between both a- and b-wave amplitudes in ERGS recording using C-glide and skin electrodes which varies from 4.0 in photopic conditions to 6.6 in scotopic conditions.

(%J

scotopic

photopic

100 (471 PV) 89 77 56 46 12

100 ( 125 PV) 93 78 60 60 14

5. Conclusions ERG electrodes have developed much in rccent years and there have been important advances in comfort and user tolerance. Along with development, there has come diversification and a certain amount of evidence, described above,

C. Barber/International

Journal

which suggests that some of the simplifying assumptions about the generation of the ERG should be re-examined. In particular the variation, if any, in potential across the cornea should be measured. Also, the modelling of the retina as a stationary cup-shaped dipole needs to be extended. At the least, the model should reflect the change in form of the dipole as the population of active cells changes with differing stages of dark adaptation. Riemslag [37] has pointed out some additional correction factors that should be taken into account: a vector summation should be made across the globe, the length of the elements should be taken into account, and the commonly used density function should be transformed from millimetres of eccentricity into degrees of visual angle. In this way the recently developed ERG electrodes may contribute, not only to better clinical recordings - more comfortable, more noise-free and so on - but also to a better understanding of the origins of the ERG.

Acknowledgements The author expresses his thanks to Chris Hogg of the Electrodiagnostic Department, Moorfields Eye Hospital, London, UK, for helpful comments during the preparation of this manuscript.

References [l] Dewar. J. (1877) The physiological action of light. Nature, 15: 4333435. [2] Hartline, H.K. (1925) The electrical response to illumination of the eye in intact animals, includina the human subject, and in decerebrate preparations. Am. J. Physiol., 73: 600-611, and reproducible records [31 Riggs, L.A. (1941) Continuous of the electrical activity of the human retina. Proc. Sot. Exp. Biol. Med., 4X: 204-207. [41 Karpe, G. (1945) The basis of clinical electroretinography. Acta Ophthalmol., 24 (SuppI.): l-118. E. (1962) ERG recording with different types t51 Sundmark, of contact glass. Acta Ophthalmol., 70 (SuppI.): 62-69. in [a Henkes, H.E. (1951) The use of electroretinography measuring the effect of vasodilation. Angiology, 2: 12512X.

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[7] Burian, H. and Allen. L. (1954) A speculum contact lens electrode for electroretinography. Electroenceph. Clin. Neurophysiol., 6: 509-51 I. [Xl Jacobson, J. (1955) A new contact lens electrode for clinical electroretinography. Arch. Ophthalmol., 54: Y40941. [9] Dawson, W.W.. Zimmermann. T.J. and Houde, W.L. (1974) A method for more comfortable electroretinography. Arch. Ophthalmol., 91: l-2. [lo] Schoessler, J.P. and Jones, R. (1975) A new cornea1 electrode for electroretinography. Vision Res., 15: 2YY301. [ll] Barber, C., Cotterill, D.J. and Larke, J.R. (1977) A new contact lens electrode. Dot. Ophthalmol., 13: 3X5-392. [12] Sieving, PA., Fishman, G.A. and Maggiano, J (1978) Cornea1 wick electrode for recording bright flash electroretinograrns and early receptor potential. Arch. Ophthalmol.. 96(5): X99-900. [13] Best, W. (lY53) Das menschliche Elektroretinogram wahrend der Dunkeladaption. Acta Ophthalmol., 31: 71116. (141 Yanashima, K.. Okisaka, S.. Ingaki, Y. and Kenjyo, H. (1983) A new disposable ERG electrode using a hydrophilic soft contact lens with a high water content. Dot. Ophthalmol., 37: 343. I151 Honda, Y., Nao-i, N., Kim, S-Y., Sakaue, E. and Nambo, M. (1986) New disposable ERG electrode made of anomalous polyvinyl alcohol gel. Dot. Ophthalmol., 63: 2033207. [I61 Grounauer, P.A. (1982) The new single use ERG cornea1 contact lens electrode and its clinical application. Dot. Ophthalmol., 31: XYYY3. 1171 Jacobson, J., Romaine, II.H., Halberg, G.P. and Stephens. G. (1958) The electrical activity of the eye during accommodation. Am. J. Ophthalmol., 46: 231-23X. [1X] Bloom, B.H. and Sokol, S. (1977) A cornea1 electrode for patterned stimulus electroretinography. Am. J. Ophthalmol.. 60: 121-126. 1191 Sokol, S. and Bloom, B.H. (1977) Macular ERGS elicited by checkerboard pattern stimuli. Dot. Ophthalmol.. 13: 299-305. [20] Chase, W.W., Fradkin, N.E. and Tsuda S. (1976) A new electrode for electroretinography. Am. J. Optom. Physiol. Opt.. 53tlO): 66X-671. 1211Borda, R.P.. Gilliam, R.M. and Coats. A.C. (1978) Goldcoated mylar electrode for electroretinography. Dot. Ophthalmol., 15: 339-343. W Arden, G.B., Carter, R.M., Hogg, C., Siegel. I.M. and Margolis, S. (1979) A gold foil electrode; extending the horizons for clinical electroretinography. Invest. Ophthalmol. Vis. Sci.. 1X(4): 421-426. 1231Dawson. W.W., Trick, G.L. and Litzkow. C.C. (1979) Improved electrode for elcctroretinography. Invest. Ophthalmol. Vis. Sci., 18: 98X-991. 1241Cummings, R.W. and Kaluzne, S.J. (19781 An improved electrode for electroretinography; design and standardisation. Am. J. Optom. Physiol. Opt., 55tlO): 719-724.

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[25] Barber, C. and Tolia, J. (1985) The carbon-glide electrode for pattern and flash electroretinography. Presented at the 23rd ISCEV Symposium, Mie, Japan. [26] Vaegan (1984) An improved method of constructing pattern electroretinogram electrodes. Dot. Ophthalmol., 40: 287-291. [27] Thompson, D.A. and Drasdo, N. (1987) An improved method for using the DTL fibre in electroretinography. Ophthalmol. Physiol. Opt., 7: 315-319. [28] Tepas, D.I. and Armington, J.C. (1962) Electroretinograms from non-cornea] electrodes. Invest. Ophthalmol., 1: 784-786. [29] Adachi-Usami, E. and Chiba, Y. (1971) The clinical ERG detected with skin electrodes. Acta Sot. Ophthalmol. Jap., 75: 1056-1061. I301 Adachi-Usami, E., Murayama, K. and Kuroda, N. (1984) Pattern ERGS recorded with skin electrodes. Fol. Ophthalmol. Jap., 35: 1528-1532. [31] Noonan, B.D., Wilkus, R.J.. Chatrian, G.E. and Lettich, E. (1973) The influence of direction of gaze on the human electroretinogram recorded from periorbital elec-

[32]

[33] [34]

[35]

[36]

[37]

trodes: a study utilizing a summating technique. Electroenceph. Clin. Neurophysiol.. 35: 495-502. Adachi-Usami, E., Kuroda, N. and Nakajima, I. (19x3) Distribution of pattern-evoked potentials in the facial area. Am. J. Ophthalmol.. 96: 734-739. Robbins, J. and Turner, J. (1988) Assessment of various types of electrode in clinical ERG. Impulse, 5: 2-5. Kriss, A., Esakowitz, I. and Shawkat, F. (1993) Comparison of flash ERGS recorded from Burian-Allen, JET, C-Glide, gold foil and skin electrodes. Eye, 7: 169-171. Wali, N. and Leguire, L.E. (1991) Dark-adapted luminance response functions with skin and cornea] electrodes. Dot. Ophthalmol., 76: 367-375. Papakostopoulos, D., Barber, C. and Dean-Hart, C. (1993) The sampling properties of different types of ERG electrodes. Clin. Vis. Sci., 8: 481-48X. Riemslag, F.C.C. (1993) Interpretation of the ganzfeld ERG; contributions of the central and peripheral parts of the visual field. Presented at the 1st European ISCEV Conference, Nottingham, UK.