IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. BME-22, NO. 3, MAY 1975
202
utility of beat frequency measures [8] and total amplitude of deviation by slow phase measures [9]. These variables are also provided by the program. Consequently, the use of the computer program promises to provide consistent and reliable measures of a battery of variables during clinical ENG testing. In addition, the computer can be programmed to provide values for the caloric test which indicate the presence of reduced vestibular responses or directional preponderance. In summary, the application of this computer program to clinical electronystagmography promises an improvement in accuracy and breadth of evaluation with a reduction of time required for record interpretation. The program operation is discussed in more detail in [10]. A listing of the program is available from the authors upon request. The routine currently is written in assembly language of PDP-8 minicomputers. Machine language implementation is probably necessary to achieve the speed required for on-line operation. Flow charts presented in [71 enable the program to be converted by other users to alternate program languages. AcKNOWLEDGMENT
The authors wish to acknowledge the helpful advice provided by their colleagues C. M. Oman and S. Yasui.
[1] [21
[31 [41
[S] [61
[7]
[8] [9] [10]
-REFERENCES S. Yasui, "Nystagmus generation, visual oculomotor tracking, and velocity perception," Ph.D. dissertation, Department of Aeronautics and Astronautics, M.I.T., Cambridge, Mass., 1973. J. R. Tole and L. R. Young, "MITNYS. A hybrid program for online analysis of nystagmus," Aerospace Med., 42: 508-511, 1971. J. H. J. Allum, "A least mean squares cubic fit algorithm for online differentiation of sampled analog signals," 1973. D. A. Robinson, "Eye movement control in primates," Science, 161, 1219-1224, 1968. V. Honrubia, R. D. Katz, D. Strelioff et al., "'Computer analysis of induced vestibular nystagmus: Rotatory stimulation of normal cats," Ann Otol Rhin and Laryng, 80, Supp 3: 7-25, 1971. H. H. Kornhuber, "Physiologie und Klinik des zentralvestibularen Systems (blick-und stutzmotorik)," In: J Berendes, R Link und F Zollner: Hals-Nasen-Ohreneilkunde. Ein kurzgefasstes Handbuch in drei Banden, Bd III/Teil 3, S. 2150-2351, Stuttgart: Theime, 1963. J. H. J. Allum, "Flow Charts for MITNYS II," Man-Vehicle Lab, MIT, 1973. N. Torok, "Significance of frequency in caloric nystagmus," Acta Otolaryng, 36, 34, 1948. R. Jung and R. Mittermaier, "Zur objectiven Registrierung und Analyse verschiedener Nystagmusformen-vestibularen, optokinetischer und spontaner Nystagmus in ihren Wechselbeziehungen, Arch OhrNas Kehlkopfheil, 146: 410-439, 1939. J. H. J. Allum, and J. R. Tole, "Operational details of MITNYS-II. A digital prog.ram for on-line analysis of nystagmus," ManVehicle Laboratory Report, M.I.T., Cambridge, Mass., 1973.
Vertical and Horizontal Eye Movement Recording in the Unrestrained Cat GABRIEL M. GAUTHIER
I. INTRODUCTION WIDE variety of systems have been developed to monitor human eye movement (EM) as well as head movements (HM). Unfortunately very few of these techniques can be used to measure unrestrained animal's EM. Photographic methods allow one to measure EM and HM but require very long and tedious data analysis. Contact-lens systems, frequently used in human experiments requiring very accurate results, are difficult to use on animals due to calibration and lens stabilization problems (Fender, 1964 [1]). The infrared (IR) camera-television screen set-up, which detects the position of corneal features is an expensive device, and is not very accurate. Systems based on detection of IR light reflection by means of photosensors are very accurate, fairly inexpensive but are essentially limited to human applications since they Manuscript received January 31, 1974; revised July 13, 1974. The author is with the Laboratoire de Psychophysiologie, Universite necessitate the mounting of a cumbersome, fixed apparatus in front of the eye (Stark et al., 1962 [7], Young, 1963 [8], de Provence, Marseille, France.
Abstract-A simple electromagnetic system is described which allows simultaneous monitoring of vertical and horizontal eye movements in the unrestrained cat. A restricted magnetic fi'eld is induced through a coil fixed to the zygomatic bone, under the sIdn. The coil leads led subdermally to a skull implanted pedestal are connected to a 15000 Hz sine-wave generator. The induced fi'eld is detected through a small coil stitched to the side of the eyeball between the iris and medial rectus muscle attachment. The detecting coil leads are connected to the head pedestal connector, then sent to a detecting amplifier whose output is calibrated in volts per degrees of eye rotation. A second set of coils implanted perpendicular to the first provides eye movement monitoring in the other direction of space. The system has a 5% linearity in a 20 degree range and a sensitivity of 0.5 volts per degree. Low cost and simplicity of surgical implantation are other attractive features of this new eye movement monitor.
A
203
GAUTHIER: EYE MOVEMENT RECORDING
Hi
z
I H LANE/ P;LAN E 0 °- -
khz -
"~~'~j~niiJCO S(1t+A ..R.D.
,Is
D.C
D.C
Fig. 1. Eye movement monitor; theoretical principle. The current element Ids flowing in a coil centered at A in plane P creates a magnetic field HM at M. M is defined in space by the coordinate pairs (x, d) or (r, 0). The method is based on sensing the magnetic field created at M by the inducting coil at A. At M, the detecting coil is in a plane Q parallel to P, so that only HM± which is the component of HM perpendicular to Q is measured (Top left). HM±IHoL is plotted as a function of x/d (top right) where Ho1 is the value of HMI for x = 0. The curve shows an acceptable 10% linearity for x/d between 0.3 and 0.6. In the actual system the coil n detects the magnetic field induced by N. The output of n is amplified and amplitude detected; the final output is calibrated as a function of eyeball position (bottom drawing).
Gauthier, 1970 [3] ). Vision is reduced and normal movements impaired. However, such a system has been successfully used on unrestrained cats in our laboratory. This system allows EM detection independently of HM since the IR light source is mounted next to the detecting cells, directly on a fixation block cemented to the animal's skull. Electrooculogram techniques can be adapted to unrestrained animals but they are not accurate or stable, and cannot be precisely calibrated. We have developed a special technique to measure vertical eye movements (VEM) and horizontal eye movements (HEM) independently of HM in cat, monkey, rabbit and other laboratory animals of similar size. The method is based on the measure of the electromagnetic coupling between two coils, one fixed to the head, and a second moving with the eyeball. Two sets of coils allow a simultaneous monitoring of both
the surgical procedure, although delicate, is simple and can be carried out fairly quickly. The eye muscles are left untouched. The attachment to the eyeball of the detecting coil necessitates only a small incision of the conjunctiva between the limbus and the tendon attachment which remains untouched. The linear range within 5% exceeds 20 degrees. The sensitivity is of the order of 5 min of arc, and the bandwidth is about 750 Hz. II. METHODS Principle of the Technique The method is based on sensing the magnetic field HM induced at a point M in space by an inducting coil placed at A which lies in a plane P perpendicular to axis d (Fig. 1). M is at a distance r from A and 0 is the angle between r and d, the perpendicular to plane P. Let's assume an ideal inducting coil made of a loop s through which runs a current I. The current element I ds is equivalent to a magnetic dipole whose moment is mL = fI ds. L is the distance between the magnetic masses +m and -m, and ds is an infinitesimal line element. The integral is done around the whole loop s, (Fig. 1, top left). The magnetic potential OM induced in M is:
VEM and HEM. An electromagnetic technique was developed by Robinson (1963) [5] and adapted for monkey experiments by Fuchs and Robinson (1965) [2]. The results they obtained were excellent, but the implantation of the detecting coil necessitated a delicate surgical intervention. The muscle insertions had to be lifted to permit the placement of the detecting coil. Usually eye movements did not reveal any alterations of the muscular system. However, some operated monkeys suffered 47r kpl p2} from strabismus (Fuchs and Robinson, 1965 [2] ). A feature of or orientathe above technique is the fact that it measures the tion of the eye in space independently of HM. But this f 1 mL becomes an inconvenience when one desires to monitor eye =m r-2 COS 0 in unrestrained animal to the an with head position respect experiment. This deficiency does not exist in the system to be where PI-r - L/2 cos 0 and P2 r + L/2 cos 0 (see Fig. 1, presented. Besides, the simplicity of the technique is such that top left for symbol definitions).
IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, MAY 1975
204
The magnetic field HM induced at M is given by
-gradM OM. The magnetic field induced at M is to be sensed by a small coil (detecting coil). The detecting coil is to be placed in a plane Q parallel to plane P and at a distance d from it (Fig. 1, top left). Therefore the only component of HM sensed by the detecting coil is the component HM1 which is perpendicular to Q. HM
=
HM1 -44ir Is(x2 - 2d 2 ) (d 2 + x2 )-5/2 where
cosO =- and r2 =d2 +x2. r
If I is an alternating current, the magnetic field at every point of plane Q can be measured, after calibration, by the voltage induced in the detecting coil when placed at that particular point. Looking at the system in another way, and assuming cylindrical symmetry around the AO axis, one may determine the position of the detecting coil, that is, the distance x between 0 and M. In the cat, the distance between inducting coil and eyeball (distance d) can be 0.5 cm or less. Since the eyeball diameter is about 2 cm, an acceptable linear range (linearity error less than 10%) of 25 degrees of eye rotation can be expected for the system. This range corresponds to values of x/d between 0.3 and 0.6 (Fig. 1, top right drawing). With the coils described in the next paragraph, one may expect a signal of about 0.5 mV in the detecting coil.
Realization of the Eye Movement Monitor The inducting coil consists of about 600 turns of an 0.8 mm coated copper wire wound on a plastic cylindrical case 14 mm in diameter and 4 mm thick. Its resistance is about 600 Q2. The detecting coil to be attached to the eyeball is a 25 turn coil made with enamel coated copper wire 0.05 mm in diameter. The turns are built on a 2 mm rod, then delicately slid off the rod and coated with a thin layer of epoxy cement. The two leads are loosely twisted together to preserve maximum flexibility. The coil thus obtained has no support other than the layer of hard epoxy. It forms a core 2 mm in diameter and about 5 mm2 in cross section. The inducting coil is connected to a wave generator supplying a 25 V signal at 15,000 Hz. The detecting coil is connected to a dc amplifier (Fig. 1, bottom drawing) composed of two differential operational amplifiers with a total gain of 20,000. The signal is amplitude detected as it comes out of the first stage. The final output is thus a dc signal whose amplitude is proportional to the amplitude of the sinusoidal input signal and therefore proportional to the position of the detecting coil (eyeball position) with respect to the inducting coil (head position). A procedure to be described allows one to calibrate the output voltage in degrees of eyeball position. Vertical and horizontal eye positions can be simultaneously
detected. A second system identical to the one described above and completely independent gives the required information providing that it be set perpendicular to the first system. Surgical procedure: The cat is anesthetized with a 15 mg/kg injection of Ketamine (Imalgene), administered intramuscularly, and set in a conventional stereotaxic frame. The following procedure is done under aseptic conditions. A 6 cm long, 3 cm wide exposure of the skull is performed starting from the lambdoidal ridge. The bone is thoroughly cleaned and dried. A dozen 1 mm holes are drilled through the skull with an electric dental drill. Stainless steel screws 1.4 mm in diameter are driven through the bone leaving about 2 mm of the screw heads exposed. Care must be taken not to perforate the dura in both the drilling and screwing operations. Dental cement is used to cover the exposed skull surface burying the screw heads. This will be used as a base for placing the head restraints and connectors. Head restraint cylinders are cemented to the base (Fig. 2(a). This technique is derived from Sheatz (1961) [61, and Noda et al. 1965 [4]. The cylinders are subsequently used to immobilize the cat's head in a frame. Fixing of the head is desired if cats are to be trained to fixate or follow targets. Detecting coil implantation: A maximum eyeball surface is exposed by pulling the eyelids open with threads as shown in Fig. 2(a). The ends of a 25 cm long size 0 thread are stitched to the limbus-iris edge, one medially, one laterally [Fig. 2(a)] using a fine ophthalmic needle. The thread is passed around a 20 mm diameter pulley (Figs. 2 and 3) which is positioned so
(a)
(b) Fig. 2. Surgical implantation of the detection and induction coils. The upper drawing ilustrates the procedure. A, inducting coil; B, detecting coil; C, coil lead connector; D, calibration knob and pulley; E, head restraint cylinders. The bottom photograph shows a cat's left eyeball two weeks after surgery. The eyeball has been turned inward by pulling on a thin thread attached to the lateral limbus (Arrow A). The detecting coil appears by transparency under the conjunctiva
(Arrow B).
GAUTHIER: EYE MOVEMENT RECORDING
(a)
(b) Fig. 3. Eye movement monitor calibration. Both ends of a thread are attached to each side of the eyeball (see text) in a horizontal or vertical plan. The thread is looped on a pulley. A knob, calibrated in degrees, allows one to rotate the eyeball in its orbit. The output of the eye movement monitor amplifier can thus be calibrated in degrees. The induction coil can be mounted externally (a) or implanted chronically (b).
that the eyeball can be easily rotated without longitudinal pulling. A calibrated knob allows one to turn the eyeball inward to expose lateral scleral surface to facilitate the surgical approach and, later to calibrate the eye movement monitor. Two 2 mm crossed incisions are made in the conjunctiva between the iris edge and the lateral rectus attachment. The corners of the incisions are gently lifted to allow the positioning of the detecting coil directly against the sclera. Four fine nylon thread stitches placed with a fine ophthalmic needle anchor the coil to the sclera. The lips of the incisions are sutured together with catgut thread. The loosely twisted coil leads exit though the back of the incision, tangentially to the eyeball. A 1 mm hypodermic needle is used as a conduit to pass the coil leads subdermally from the lateral fornix to the skull where they are temporarily pasted to the pedestal base. Great care has to be taken to prevent tension or severe twisting of the leads in the orbit. After a few days, the conjunctival incisions heal and the detecting coil is tightly sealed to the eyeball as illustrated in Fig. 2(b). In this figure the right eyeball has been turned inward by pulling on a thin thread
205
attached to the lateral limbus (Arrow A). The detecting coil appears by transparence under the conjunctiva (Arrow B). Induction coil implantation: A horizontal 2 cm incision is made over the zygomatic arch, and the skin edges are freed to permit insertion of the coil through the incision. The induction coil is temporarily connected to the 15,000 Hz sinusoidal wave generator and the detection coil connected to the eye movement monitor amplifier. While the eyeball is at a zero resting position, the induction coil is slid longitudinally inside the incision. The range of best linearity of the measuring system is determined according to what was determined in Section II; that is, in the range HMilHoi between 0.87 and 0.52. A screw fixes the coil to the zygomatic bone, in the middle of the linear range. The coil leads are then subdermally slid to the top of the skull using the hypodermic needle as a conduit. The incision lips are sutured together and covered with antibacterial powder. Induction and detection coil leads are soldered to an 8 pin connector. The connector is then fixed with dental cement to the pedestal base, between the two head restraint cylinders (Fig. 2, top). Fig. 3(b) shows a cat 2 weeks after surgery. The incisions have healed. The induction coil is checked to be sure that it is securely anchored to the zygomatic bone. Here the cat has been anesthetized and set in the stereotaxic frame to allow the calibration to be checked. Both VEM and HEM can be simultaneously monitored. A second set of coils and a second channel of the amplifier detect VEM's. The detecting coil is affixed to the eyeball between the iris rim and the superior rectus tendon attachment. An induction coil identical to the first one is screwed to the skull in a horizontal plane directly over the eyeball. The leads of the vertical eye movement monitoring coils are connected to the other 4 pins of the connector. Calibration procedure: Before freeing the eye of the threads connected to the calibration set-up, calibration recordings are taken in a ±10 degree range centered around the zero resting position. The recordings obtained are presented in Fig. 4 together with the corresponding calibration curves. Simultaneous VEM and HEM recordings show that crosstalk between channels does not exceed 10 percent. Calibration ranges over ±12.5 degrees but the 5 percent linearity range does not exceed ±10 degrees. The cat eyeball is freed and ophthalmic antibacterial powder applied to the operated eye surface. After a 3 day recovery period during which penicillin is administered daily, the cat is ready for tracking experiments. External setting of the induction coil: In experiments in which the cat's head is restrained and the danger of its head hitting against obstacles is avoided, chronic implantation of the induction coils is not necessary. The coils are mounted [Fig. 3(a)] externally next to the zygomatic bone (HEM coil) and over the orbit (VEM coil). Calibration is done in a manner similar to that described above. However, the relative positions of the coils with respect to the pedestal have to be recorded so that they can be accurately repositioned before each recording session. Calibration is thus preserved.
206
IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, MAY 1975
r
+2.5
I
1
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0
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.
.
ui:CIZ
.
- 25. . +2.5. .
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.
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*
.
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~~~~~~~~~~~~~~~ 6fI rVI,
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,
4
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-
-
0 DETECTOR OUTPUT IN VOLTS
VERTICAL CALIBRATION
HORIZONTAL CALIBRATION
DETECTOR OUTPUT IN VOLTS
+
+
+
+
+
+
4.
+
RIGHT
LEFT _l o
_ S
10
5
DOWN _
+ POSITION IN DEGREES
UP I0
_5
0
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10
IN DEGREES
+ .-I
+
+
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Fig. 4. Calibration recording and corresponding curves. Top: Vertical and horizontal eye movement monitor outputs are recorded (ordinates) as a function of time as the eye position in vertical and horizontal planes is rotated by 2.5 degree steps over a ± 12.5 degree range centered around a zero resting position by manual rotation of the calibration knob. The records demonstrate cross-contamination between channels to be less than 10%. Bottom: vertical and horizontal calibration curves show a 5% linear range extending ± 10 degrees around a zero resting position.
In the trained cat, gross calibration can also be obtained independently of that provided by the implantation procedure. During a tracking session, the average amplitude of the performed saccades can be used to calibrate the eye movement
monitor.
III. RESULTS
After a 3 day recovery period, examination of the animal usually shows a slight inflammation of the conjunctiva where the coils were implanted. No impairment of the eye motility is observed either visually or on recording spontaneous eye
movements. There is no evidence of eye movement being mechanically limited. This problem, which may take place with Fuchs and Robinson's implants, does not develop here since the eye muscle system is never touched during the whole
surgical procedure. Fig. 5 shows simultaneous recordings of VEM and HEM using the above described system. The upper recordings were obtained with a 120 pulses per second, 3.2 V stimulus applied to the right (RC) and left (LC) vermian cerebellar surface of lobe VI. Essentially HEM were obtained. VEM were induced with the same stimulus applied to the midline area of the same lobe (Fig. 5, bottom left recordings). Spontaneous VEM and HEM were recorded (Fig. 5, bottom center) as well as those during ether induced nystagmus (Fig. 5, bottom right). Thus far 8 cats have been implanted. Two of them could not be used because the detecting coil leads broke, and one lost its pedestal 3 weeks after implantation. The remaining cats were recorded from every other day. One of them has been providing data for over one month. The same problem
IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. BME-22, NO. 3, MAY 1975
attractive features of the technique are its extremely low cost as compared to other systems, and the fact that the surgical procedure is fairly simple.
4.T*
VETICAL
*
.
EYE POSITl r IN DEGREES
__ ~~ .
HORtIZONTALO
ACKNOWLEDGMENT The author wishes to thank Prof. D. A. Robinson for reviewing and criticizing this note, Prof. M. Hugon for his encouragement and advice, and M. Volle for valuable technical assistance.
tC Cc
-_t L
STIMUSUS
VEItT
202
utility of beat frequency measures [8] and total amplitude of deviation by slow phase measures [9]. These variables are also provided by the program. Consequently, the use of the computer program promises to provide consistent and reliable measures of a battery of variables during clinical ENG testing. In addition, the computer can be programmed to provide values for the caloric test which indicate the presence of reduced vestibular responses or directional preponderance. In summary, the application of this computer program to clinical electronystagmography promises an improvement in accuracy and breadth of evaluation with a reduction of time required for record interpretation. The program operation is discussed in more detail in [10]. A listing of the program is available from the authors upon request. The routine currently is written in assembly language of PDP-8 minicomputers. Machine language implementation is probably necessary to achieve the speed required for on-line operation. Flow charts presented in [71 enable the program to be converted by other users to alternate program languages. AcKNOWLEDGMENT
The authors wish to acknowledge the helpful advice provided by their colleagues C. M. Oman and S. Yasui.
[1] [21
[31 [41
[S] [61
[7]
[8] [9] [10]
-REFERENCES S. Yasui, "Nystagmus generation, visual oculomotor tracking, and velocity perception," Ph.D. dissertation, Department of Aeronautics and Astronautics, M.I.T., Cambridge, Mass., 1973. J. R. Tole and L. R. Young, "MITNYS. A hybrid program for online analysis of nystagmus," Aerospace Med., 42: 508-511, 1971. J. H. J. Allum, "A least mean squares cubic fit algorithm for online differentiation of sampled analog signals," 1973. D. A. Robinson, "Eye movement control in primates," Science, 161, 1219-1224, 1968. V. Honrubia, R. D. Katz, D. Strelioff et al., "'Computer analysis of induced vestibular nystagmus: Rotatory stimulation of normal cats," Ann Otol Rhin and Laryng, 80, Supp 3: 7-25, 1971. H. H. Kornhuber, "Physiologie und Klinik des zentralvestibularen Systems (blick-und stutzmotorik)," In: J Berendes, R Link und F Zollner: Hals-Nasen-Ohreneilkunde. Ein kurzgefasstes Handbuch in drei Banden, Bd III/Teil 3, S. 2150-2351, Stuttgart: Theime, 1963. J. H. J. Allum, "Flow Charts for MITNYS II," Man-Vehicle Lab, MIT, 1973. N. Torok, "Significance of frequency in caloric nystagmus," Acta Otolaryng, 36, 34, 1948. R. Jung and R. Mittermaier, "Zur objectiven Registrierung und Analyse verschiedener Nystagmusformen-vestibularen, optokinetischer und spontaner Nystagmus in ihren Wechselbeziehungen, Arch OhrNas Kehlkopfheil, 146: 410-439, 1939. J. H. J. Allum, and J. R. Tole, "Operational details of MITNYS-II. A digital prog.ram for on-line analysis of nystagmus," ManVehicle Laboratory Report, M.I.T., Cambridge, Mass., 1973.
Vertical and Horizontal Eye Movement Recording in the Unrestrained Cat GABRIEL M. GAUTHIER
I. INTRODUCTION WIDE variety of systems have been developed to monitor human eye movement (EM) as well as head movements (HM). Unfortunately very few of these techniques can be used to measure unrestrained animal's EM. Photographic methods allow one to measure EM and HM but require very long and tedious data analysis. Contact-lens systems, frequently used in human experiments requiring very accurate results, are difficult to use on animals due to calibration and lens stabilization problems (Fender, 1964 [1]). The infrared (IR) camera-television screen set-up, which detects the position of corneal features is an expensive device, and is not very accurate. Systems based on detection of IR light reflection by means of photosensors are very accurate, fairly inexpensive but are essentially limited to human applications since they Manuscript received January 31, 1974; revised July 13, 1974. The author is with the Laboratoire de Psychophysiologie, Universite necessitate the mounting of a cumbersome, fixed apparatus in front of the eye (Stark et al., 1962 [7], Young, 1963 [8], de Provence, Marseille, France.
Abstract-A simple electromagnetic system is described which allows simultaneous monitoring of vertical and horizontal eye movements in the unrestrained cat. A restricted magnetic fi'eld is induced through a coil fixed to the zygomatic bone, under the sIdn. The coil leads led subdermally to a skull implanted pedestal are connected to a 15000 Hz sine-wave generator. The induced fi'eld is detected through a small coil stitched to the side of the eyeball between the iris and medial rectus muscle attachment. The detecting coil leads are connected to the head pedestal connector, then sent to a detecting amplifier whose output is calibrated in volts per degrees of eye rotation. A second set of coils implanted perpendicular to the first provides eye movement monitoring in the other direction of space. The system has a 5% linearity in a 20 degree range and a sensitivity of 0.5 volts per degree. Low cost and simplicity of surgical implantation are other attractive features of this new eye movement monitor.
A
203
GAUTHIER: EYE MOVEMENT RECORDING
Hi
z
I H LANE/ P;LAN E 0 °- -
khz -
"~~'~j~niiJCO S(1t+A ..R.D.
,Is
D.C
D.C
Fig. 1. Eye movement monitor; theoretical principle. The current element Ids flowing in a coil centered at A in plane P creates a magnetic field HM at M. M is defined in space by the coordinate pairs (x, d) or (r, 0). The method is based on sensing the magnetic field created at M by the inducting coil at A. At M, the detecting coil is in a plane Q parallel to P, so that only HM± which is the component of HM perpendicular to Q is measured (Top left). HM±IHoL is plotted as a function of x/d (top right) where Ho1 is the value of HMI for x = 0. The curve shows an acceptable 10% linearity for x/d between 0.3 and 0.6. In the actual system the coil n detects the magnetic field induced by N. The output of n is amplified and amplitude detected; the final output is calibrated as a function of eyeball position (bottom drawing).
Gauthier, 1970 [3] ). Vision is reduced and normal movements impaired. However, such a system has been successfully used on unrestrained cats in our laboratory. This system allows EM detection independently of HM since the IR light source is mounted next to the detecting cells, directly on a fixation block cemented to the animal's skull. Electrooculogram techniques can be adapted to unrestrained animals but they are not accurate or stable, and cannot be precisely calibrated. We have developed a special technique to measure vertical eye movements (VEM) and horizontal eye movements (HEM) independently of HM in cat, monkey, rabbit and other laboratory animals of similar size. The method is based on the measure of the electromagnetic coupling between two coils, one fixed to the head, and a second moving with the eyeball. Two sets of coils allow a simultaneous monitoring of both
the surgical procedure, although delicate, is simple and can be carried out fairly quickly. The eye muscles are left untouched. The attachment to the eyeball of the detecting coil necessitates only a small incision of the conjunctiva between the limbus and the tendon attachment which remains untouched. The linear range within 5% exceeds 20 degrees. The sensitivity is of the order of 5 min of arc, and the bandwidth is about 750 Hz. II. METHODS Principle of the Technique The method is based on sensing the magnetic field HM induced at a point M in space by an inducting coil placed at A which lies in a plane P perpendicular to axis d (Fig. 1). M is at a distance r from A and 0 is the angle between r and d, the perpendicular to plane P. Let's assume an ideal inducting coil made of a loop s through which runs a current I. The current element I ds is equivalent to a magnetic dipole whose moment is mL = fI ds. L is the distance between the magnetic masses +m and -m, and ds is an infinitesimal line element. The integral is done around the whole loop s, (Fig. 1, top left). The magnetic potential OM induced in M is:
VEM and HEM. An electromagnetic technique was developed by Robinson (1963) [5] and adapted for monkey experiments by Fuchs and Robinson (1965) [2]. The results they obtained were excellent, but the implantation of the detecting coil necessitated a delicate surgical intervention. The muscle insertions had to be lifted to permit the placement of the detecting coil. Usually eye movements did not reveal any alterations of the muscular system. However, some operated monkeys suffered 47r kpl p2} from strabismus (Fuchs and Robinson, 1965 [2] ). A feature of or orientathe above technique is the fact that it measures the tion of the eye in space independently of HM. But this f 1 mL becomes an inconvenience when one desires to monitor eye =m r-2 COS 0 in unrestrained animal to the an with head position respect experiment. This deficiency does not exist in the system to be where PI-r - L/2 cos 0 and P2 r + L/2 cos 0 (see Fig. 1, presented. Besides, the simplicity of the technique is such that top left for symbol definitions).
IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, MAY 1975
204
The magnetic field HM induced at M is given by
-gradM OM. The magnetic field induced at M is to be sensed by a small coil (detecting coil). The detecting coil is to be placed in a plane Q parallel to plane P and at a distance d from it (Fig. 1, top left). Therefore the only component of HM sensed by the detecting coil is the component HM1 which is perpendicular to Q. HM
=
HM1 -44ir Is(x2 - 2d 2 ) (d 2 + x2 )-5/2 where
cosO =- and r2 =d2 +x2. r
If I is an alternating current, the magnetic field at every point of plane Q can be measured, after calibration, by the voltage induced in the detecting coil when placed at that particular point. Looking at the system in another way, and assuming cylindrical symmetry around the AO axis, one may determine the position of the detecting coil, that is, the distance x between 0 and M. In the cat, the distance between inducting coil and eyeball (distance d) can be 0.5 cm or less. Since the eyeball diameter is about 2 cm, an acceptable linear range (linearity error less than 10%) of 25 degrees of eye rotation can be expected for the system. This range corresponds to values of x/d between 0.3 and 0.6 (Fig. 1, top right drawing). With the coils described in the next paragraph, one may expect a signal of about 0.5 mV in the detecting coil.
Realization of the Eye Movement Monitor The inducting coil consists of about 600 turns of an 0.8 mm coated copper wire wound on a plastic cylindrical case 14 mm in diameter and 4 mm thick. Its resistance is about 600 Q2. The detecting coil to be attached to the eyeball is a 25 turn coil made with enamel coated copper wire 0.05 mm in diameter. The turns are built on a 2 mm rod, then delicately slid off the rod and coated with a thin layer of epoxy cement. The two leads are loosely twisted together to preserve maximum flexibility. The coil thus obtained has no support other than the layer of hard epoxy. It forms a core 2 mm in diameter and about 5 mm2 in cross section. The inducting coil is connected to a wave generator supplying a 25 V signal at 15,000 Hz. The detecting coil is connected to a dc amplifier (Fig. 1, bottom drawing) composed of two differential operational amplifiers with a total gain of 20,000. The signal is amplitude detected as it comes out of the first stage. The final output is thus a dc signal whose amplitude is proportional to the amplitude of the sinusoidal input signal and therefore proportional to the position of the detecting coil (eyeball position) with respect to the inducting coil (head position). A procedure to be described allows one to calibrate the output voltage in degrees of eyeball position. Vertical and horizontal eye positions can be simultaneously
detected. A second system identical to the one described above and completely independent gives the required information providing that it be set perpendicular to the first system. Surgical procedure: The cat is anesthetized with a 15 mg/kg injection of Ketamine (Imalgene), administered intramuscularly, and set in a conventional stereotaxic frame. The following procedure is done under aseptic conditions. A 6 cm long, 3 cm wide exposure of the skull is performed starting from the lambdoidal ridge. The bone is thoroughly cleaned and dried. A dozen 1 mm holes are drilled through the skull with an electric dental drill. Stainless steel screws 1.4 mm in diameter are driven through the bone leaving about 2 mm of the screw heads exposed. Care must be taken not to perforate the dura in both the drilling and screwing operations. Dental cement is used to cover the exposed skull surface burying the screw heads. This will be used as a base for placing the head restraints and connectors. Head restraint cylinders are cemented to the base (Fig. 2(a). This technique is derived from Sheatz (1961) [61, and Noda et al. 1965 [4]. The cylinders are subsequently used to immobilize the cat's head in a frame. Fixing of the head is desired if cats are to be trained to fixate or follow targets. Detecting coil implantation: A maximum eyeball surface is exposed by pulling the eyelids open with threads as shown in Fig. 2(a). The ends of a 25 cm long size 0 thread are stitched to the limbus-iris edge, one medially, one laterally [Fig. 2(a)] using a fine ophthalmic needle. The thread is passed around a 20 mm diameter pulley (Figs. 2 and 3) which is positioned so
(a)
(b) Fig. 2. Surgical implantation of the detection and induction coils. The upper drawing ilustrates the procedure. A, inducting coil; B, detecting coil; C, coil lead connector; D, calibration knob and pulley; E, head restraint cylinders. The bottom photograph shows a cat's left eyeball two weeks after surgery. The eyeball has been turned inward by pulling on a thin thread attached to the lateral limbus (Arrow A). The detecting coil appears by transparency under the conjunctiva
(Arrow B).
GAUTHIER: EYE MOVEMENT RECORDING
(a)
(b) Fig. 3. Eye movement monitor calibration. Both ends of a thread are attached to each side of the eyeball (see text) in a horizontal or vertical plan. The thread is looped on a pulley. A knob, calibrated in degrees, allows one to rotate the eyeball in its orbit. The output of the eye movement monitor amplifier can thus be calibrated in degrees. The induction coil can be mounted externally (a) or implanted chronically (b).
that the eyeball can be easily rotated without longitudinal pulling. A calibrated knob allows one to turn the eyeball inward to expose lateral scleral surface to facilitate the surgical approach and, later to calibrate the eye movement monitor. Two 2 mm crossed incisions are made in the conjunctiva between the iris edge and the lateral rectus attachment. The corners of the incisions are gently lifted to allow the positioning of the detecting coil directly against the sclera. Four fine nylon thread stitches placed with a fine ophthalmic needle anchor the coil to the sclera. The lips of the incisions are sutured together with catgut thread. The loosely twisted coil leads exit though the back of the incision, tangentially to the eyeball. A 1 mm hypodermic needle is used as a conduit to pass the coil leads subdermally from the lateral fornix to the skull where they are temporarily pasted to the pedestal base. Great care has to be taken to prevent tension or severe twisting of the leads in the orbit. After a few days, the conjunctival incisions heal and the detecting coil is tightly sealed to the eyeball as illustrated in Fig. 2(b). In this figure the right eyeball has been turned inward by pulling on a thin thread
205
attached to the lateral limbus (Arrow A). The detecting coil appears by transparence under the conjunctiva (Arrow B). Induction coil implantation: A horizontal 2 cm incision is made over the zygomatic arch, and the skin edges are freed to permit insertion of the coil through the incision. The induction coil is temporarily connected to the 15,000 Hz sinusoidal wave generator and the detection coil connected to the eye movement monitor amplifier. While the eyeball is at a zero resting position, the induction coil is slid longitudinally inside the incision. The range of best linearity of the measuring system is determined according to what was determined in Section II; that is, in the range HMilHoi between 0.87 and 0.52. A screw fixes the coil to the zygomatic bone, in the middle of the linear range. The coil leads are then subdermally slid to the top of the skull using the hypodermic needle as a conduit. The incision lips are sutured together and covered with antibacterial powder. Induction and detection coil leads are soldered to an 8 pin connector. The connector is then fixed with dental cement to the pedestal base, between the two head restraint cylinders (Fig. 2, top). Fig. 3(b) shows a cat 2 weeks after surgery. The incisions have healed. The induction coil is checked to be sure that it is securely anchored to the zygomatic bone. Here the cat has been anesthetized and set in the stereotaxic frame to allow the calibration to be checked. Both VEM and HEM can be simultaneously monitored. A second set of coils and a second channel of the amplifier detect VEM's. The detecting coil is affixed to the eyeball between the iris rim and the superior rectus tendon attachment. An induction coil identical to the first one is screwed to the skull in a horizontal plane directly over the eyeball. The leads of the vertical eye movement monitoring coils are connected to the other 4 pins of the connector. Calibration procedure: Before freeing the eye of the threads connected to the calibration set-up, calibration recordings are taken in a ±10 degree range centered around the zero resting position. The recordings obtained are presented in Fig. 4 together with the corresponding calibration curves. Simultaneous VEM and HEM recordings show that crosstalk between channels does not exceed 10 percent. Calibration ranges over ±12.5 degrees but the 5 percent linearity range does not exceed ±10 degrees. The cat eyeball is freed and ophthalmic antibacterial powder applied to the operated eye surface. After a 3 day recovery period during which penicillin is administered daily, the cat is ready for tracking experiments. External setting of the induction coil: In experiments in which the cat's head is restrained and the danger of its head hitting against obstacles is avoided, chronic implantation of the induction coils is not necessary. The coils are mounted [Fig. 3(a)] externally next to the zygomatic bone (HEM coil) and over the orbit (VEM coil). Calibration is done in a manner similar to that described above. However, the relative positions of the coils with respect to the pedestal have to be recorded so that they can be accurately repositioned before each recording session. Calibration is thus preserved.
206
IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, MAY 1975
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Fig. 4. Calibration recording and corresponding curves. Top: Vertical and horizontal eye movement monitor outputs are recorded (ordinates) as a function of time as the eye position in vertical and horizontal planes is rotated by 2.5 degree steps over a ± 12.5 degree range centered around a zero resting position by manual rotation of the calibration knob. The records demonstrate cross-contamination between channels to be less than 10%. Bottom: vertical and horizontal calibration curves show a 5% linear range extending ± 10 degrees around a zero resting position.
In the trained cat, gross calibration can also be obtained independently of that provided by the implantation procedure. During a tracking session, the average amplitude of the performed saccades can be used to calibrate the eye movement
monitor.
III. RESULTS
After a 3 day recovery period, examination of the animal usually shows a slight inflammation of the conjunctiva where the coils were implanted. No impairment of the eye motility is observed either visually or on recording spontaneous eye
movements. There is no evidence of eye movement being mechanically limited. This problem, which may take place with Fuchs and Robinson's implants, does not develop here since the eye muscle system is never touched during the whole
surgical procedure. Fig. 5 shows simultaneous recordings of VEM and HEM using the above described system. The upper recordings were obtained with a 120 pulses per second, 3.2 V stimulus applied to the right (RC) and left (LC) vermian cerebellar surface of lobe VI. Essentially HEM were obtained. VEM were induced with the same stimulus applied to the midline area of the same lobe (Fig. 5, bottom left recordings). Spontaneous VEM and HEM were recorded (Fig. 5, bottom center) as well as those during ether induced nystagmus (Fig. 5, bottom right). Thus far 8 cats have been implanted. Two of them could not be used because the detecting coil leads broke, and one lost its pedestal 3 weeks after implantation. The remaining cats were recorded from every other day. One of them has been providing data for over one month. The same problem
IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. BME-22, NO. 3, MAY 1975
attractive features of the technique are its extremely low cost as compared to other systems, and the fact that the surgical procedure is fairly simple.
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ACKNOWLEDGMENT The author wishes to thank Prof. D. A. Robinson for reviewing and criticizing this note, Prof. M. Hugon for his encouragement and advice, and M. Volle for valuable technical assistance.
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