Ann 0101 88 :1979
MONOCULAR NYSTAGMIC RESPONSES TO CALORIC STIMULATION JAMES W. WOLFE,
PhD
SAN ANTONIO, TEXAS Twenty-five normal subjects and 173 clinical patients received standard bithermal caloric testing. Vestibular nystagmus was evaluated for cumulative slow phase velocity from the summated horizontal eye recording and independent recording of the left and right eye. These data revealed that cold water stimulation produced more intense activation of the ipsilateral eye. Simultaneous closed-circuit video and D.C. electro-oculographic recordings from eight normal rhesus monkeys in response to cold water irrigations confirmed the fact that this stimulus leads to differential activation of the extraocular muscles. A possible explanation for this finding is discussed.
In the mid-1800s, Hering published numerous works on the innervation of the extraocular muscles.':" His major point was that there is a balance in the excitatory-inhibitory input to the extraocular muscles and that the eyes do not always move symmetrically. Unfortunately, over the past 100 years, Hering's law has become synonymous with the concept that the eyes always move conjugately. An even further assumption is that reflexive eye movements are completely conjugate in nature. These interpretations have been applied to the field of electronystagmography (ENG) in an almost blanket manner. Eye movement recordings in clinical ENG studies are usually made by placing electrodes at the outer canthus in line with the electrical dipole of each eye; these signals are then applied to the inputs of a differential amplifier. Since the output of the amplifier is essentially the sum of the differences, only eye movements in the horizontal plane will be registered. However, there is no way of knowing if the eyes are moving in the same manner, or even if they are moving in the same direction. The present studies were designed to investigate responses from each eye, independently, while also monitoring
the summated (differential) binocular response. METHODS AND MATERIALS The evaluations were carried out with 198 human subjects and six infrahuman primates (rhesus monkeys). The human subjects were divided into the following categories: 1. Twenty-five "normal" young men ranging in age from 19 to 23 years. Each individual was given a complete ENT examination to rule out any gross abnormalities related to VIII nerve function. 2. One hundred and seventy-three clinical patients who were referred to our facility with various ENT problems for caloric testing. All subjects and patients completed a detailed questionnaire related to their vestibular problems and either had received, or were given, audiometric evaluation. A standard caloric test employing water at temperatures of 30 C and 44 C was used with all subjects. Each stimulus consisted of 250 cc of water delivered over a 40-second period. Eye movements were recorded using conventional silver-silver chloride electrodes which were placed at the outer canthi for the summated record, with additional electrodes located nasally in the horizontal plane of each eye for the independent recording of the left and right eye movements. A pair of electrodes was also placed above and below the right eye in order to record vertical movements. Eye movement potentials were amplified with a 3-second time constant and written out on a Beckman Dynograph Recorder. In addition, a number of records were obtained using D.C. recording techniques in order to determine eye position. Calibrations for the summated, left,
From the Vestibular Function, Otolaryngology Branch, Clinical Sciences Division, USAF School of Aerospace Medicine, San Antonio, Texas.
79
JAMES W. WOLFE
80
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COLO lFT ~UM
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I.r
I
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RT
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Fig. 1. Nystagmic responses from a normal subject showing differences in amplitude and velocity following caloric stimulation. and right eye were obtained before each caloric irrigation by having the subject fixate on lights which were 10° apart and automatically flashed from left to right about the center position. All irrigations were performed in reduced red light with the subject's eyes closed except for a 10-second period when the subject was required to fixate on a small light as a test for fixation suppression. The subjects were also kept in red light during the 5-minute interval between tests in an attempt to minimize changes in the corneo-retinal potential due to light and dark adaptation. Each record was hand-scored by the same technician in the following manner: an average of ten nystagmic beats were measured for slow-phase velocity during the period of maximum response, typically from 70-80 seconds after the beginning of the stimulus. The slow phase velocities for the left and right eye were measured during the same time segment. These data were then keypunched and statistically analyzed by an IBM 360 computer. The rhesus monkeys were instrumented with restraint pedestals and silver-silver chloride electrodes were implanted in the outer canthi and medially for the D.C. recording of summated, left, and right eye movements. A closed circuit infrared video camera and recorder system was also used to record the eye movements in response to caloric irrigation. In some animals, a split screen recording technique was employed to simultaneously obtain the electrical and visual representation on a composite video tape. In this manner, the actual position of the eyes could be compared to the electrical record.
RESULTS
It was quite evident on a purely qualitative basis that conjugate and symmetrical eye movements during caloric irrigation were the exception rather than the rule. Figure 1 shows the nystagmic responses from a normal subject. It is clearly apparent during the cold left response that the left eye has almost twice the amplitude and slow phase velocity of the right eye. This same situation is also seen with cold right stimulation: the ipsilateral eye shows approximately twice the amplitude and slow phase velocity as the contralateral eye. During the period of response to warm water, the eyes tend to be more conjugate, although the warm left stimulus led to a slightly higher velocity in the right eye. A more extreme difference between the two eyes in response to caloric stimulation is shown in Figure 2. Following irrigation with cold water, the ipsilateral eye is essentially producing the summated record; however, the warm stimulus leads to reversal and the contralateral eye reflects the greater magnitude of response. This patient was a 62-year-old male who had experienced a severe acute attack of vertigo with nausea and vomiting two months
MONOCULAR CALORIC RESPONSES
81
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Fig. 2. Nystagmic responses from a clinical patient showing marked asymmetry of each eye.
prior to this test. At the time of the test, the patient had been asymptomatic for approximately six weeks. However, he did have a low-intensity (7° / sec) left beating nystagmus in the left lateral position. Based on [ongkees' formula," he also had a minimal (22%) directional preponderance to the left. That this type of response was related to the nature of the stimulus, rather than the clinical pathology, is supported by the fact that normals could give this same pattern of responses.
:# 1159 POSITIONAL LFT LATERAL SUM~--~--'-v·--""-v
RT
'D"L 'SEC
Fig. 3. Nystagmic responses from a clinical patient in the left lateral position.
The records from some patients showed results which were opposite to the previous cases; i.e., the subjects had a greater response from the contralateral eye during cold irrigation, which reversed to the ipsilateral side in response to the warm stimulus. The fact that one does not need a caloric stimulus to generate asymmetrical or disconjugate eye movements is clearly evident in Figure 3. As can be seen, this 49-year-old female had a positional nystagmus in the left lateral position that was being produced by the left eye; the summated record indicates a lower amplitude since the right eye is actually beating in the opposite direction. This patient had a three-yearhistory of dizziness which was aggravated by walking and a minimal hightone hearing loss. On a purely qualitative basis, it became evident that one could obtain almost any permutation of the nystagmic responses. The records also indicated that the cold stimulus appeared to pro-
82
JAMES W. WOLFE
opposite effect from that of the cold stimulus.
N=134 NORMALS Olff (R-l) Cl -15.1 CR 16.1 Wl 1.7 WR l.l
lEFT EYE RIGHT EYE --SUM - . - . >
~
~
P c.001 P cOOl NS NS
40
~ 30
~ 20 10 L - _ - , - - - - ----,
Cl
---T--
CR
Wl
--;I~---
WR
Fig. 4. Mean slow phase velocities for each stimulus condition for all patients; note that the ipsilateral eye shows ahnost twice the velocity of the contralateral eye following cold irrigation: (R-L), right minus left.
duce greater asymmetry than the warm. Therefore, it became obvious that only statistical analysis of a fairly large population would reveal the true relationships between the stimulus and the response. The first consideration was what percentage of the normal subjects and patients had only one eye moving during any of the stimulus conditions. Only two of the normal subjects had one eye that did not move during the warm or cold stimulation. Those patients with a bilateral hearing loss showed the greatest percentage of monocular responses under these same conditions. Since there were no significant differences in the caloric responses in the hearing loss left, right, or bilateral groups, their data were combined. When all hearing losses were combined, the data showed that over 39% of these patients had one eye that did not move during the various stimulations. Of those patients that had normal hearing and a major complaint of dizziness, 26% had only one eye moving during one or more of the caloric stimulations.
In all groups, cold water clearly produced a response decrement in the contralateral eye. The number of patients with monocular responses to warm stimulation was somewhat less and appeared to be more evenly distributed. There was a tendency for the ipsilateral eye to show more of a decrement, the
Analysis of the slow phase velocities for the summated, left and right eye data from the 134 patients classified as normal (directional preponderance < 20%; unilateral weakness 20%) within the 173 total patient population in this study. Figure 5 shows N=39 ABNORMAlS Olff(R-l) Cl -16.5 P
MONOCULAR NYSTAGMIC RESPONSES TO CALORIC STIMULATION JAMES W. WOLFE,
PhD
SAN ANTONIO, TEXAS Twenty-five normal subjects and 173 clinical patients received standard bithermal caloric testing. Vestibular nystagmus was evaluated for cumulative slow phase velocity from the summated horizontal eye recording and independent recording of the left and right eye. These data revealed that cold water stimulation produced more intense activation of the ipsilateral eye. Simultaneous closed-circuit video and D.C. electro-oculographic recordings from eight normal rhesus monkeys in response to cold water irrigations confirmed the fact that this stimulus leads to differential activation of the extraocular muscles. A possible explanation for this finding is discussed.
In the mid-1800s, Hering published numerous works on the innervation of the extraocular muscles.':" His major point was that there is a balance in the excitatory-inhibitory input to the extraocular muscles and that the eyes do not always move symmetrically. Unfortunately, over the past 100 years, Hering's law has become synonymous with the concept that the eyes always move conjugately. An even further assumption is that reflexive eye movements are completely conjugate in nature. These interpretations have been applied to the field of electronystagmography (ENG) in an almost blanket manner. Eye movement recordings in clinical ENG studies are usually made by placing electrodes at the outer canthus in line with the electrical dipole of each eye; these signals are then applied to the inputs of a differential amplifier. Since the output of the amplifier is essentially the sum of the differences, only eye movements in the horizontal plane will be registered. However, there is no way of knowing if the eyes are moving in the same manner, or even if they are moving in the same direction. The present studies were designed to investigate responses from each eye, independently, while also monitoring
the summated (differential) binocular response. METHODS AND MATERIALS The evaluations were carried out with 198 human subjects and six infrahuman primates (rhesus monkeys). The human subjects were divided into the following categories: 1. Twenty-five "normal" young men ranging in age from 19 to 23 years. Each individual was given a complete ENT examination to rule out any gross abnormalities related to VIII nerve function. 2. One hundred and seventy-three clinical patients who were referred to our facility with various ENT problems for caloric testing. All subjects and patients completed a detailed questionnaire related to their vestibular problems and either had received, or were given, audiometric evaluation. A standard caloric test employing water at temperatures of 30 C and 44 C was used with all subjects. Each stimulus consisted of 250 cc of water delivered over a 40-second period. Eye movements were recorded using conventional silver-silver chloride electrodes which were placed at the outer canthi for the summated record, with additional electrodes located nasally in the horizontal plane of each eye for the independent recording of the left and right eye movements. A pair of electrodes was also placed above and below the right eye in order to record vertical movements. Eye movement potentials were amplified with a 3-second time constant and written out on a Beckman Dynograph Recorder. In addition, a number of records were obtained using D.C. recording techniques in order to determine eye position. Calibrations for the summated, left,
From the Vestibular Function, Otolaryngology Branch, Clinical Sciences Division, USAF School of Aerospace Medicine, San Antonio, Texas.
79
JAMES W. WOLFE
80
#1275 WARM lFT
COLO lFT ~UM
,.
I.r
I
lFT
'1·.,·'.4,""
RT
20L
2 SEC
COLO RT
SUM
WARM RT
.,'''''''.''.
lFT
RT
Fig. 1. Nystagmic responses from a normal subject showing differences in amplitude and velocity following caloric stimulation. and right eye were obtained before each caloric irrigation by having the subject fixate on lights which were 10° apart and automatically flashed from left to right about the center position. All irrigations were performed in reduced red light with the subject's eyes closed except for a 10-second period when the subject was required to fixate on a small light as a test for fixation suppression. The subjects were also kept in red light during the 5-minute interval between tests in an attempt to minimize changes in the corneo-retinal potential due to light and dark adaptation. Each record was hand-scored by the same technician in the following manner: an average of ten nystagmic beats were measured for slow-phase velocity during the period of maximum response, typically from 70-80 seconds after the beginning of the stimulus. The slow phase velocities for the left and right eye were measured during the same time segment. These data were then keypunched and statistically analyzed by an IBM 360 computer. The rhesus monkeys were instrumented with restraint pedestals and silver-silver chloride electrodes were implanted in the outer canthi and medially for the D.C. recording of summated, left, and right eye movements. A closed circuit infrared video camera and recorder system was also used to record the eye movements in response to caloric irrigation. In some animals, a split screen recording technique was employed to simultaneously obtain the electrical and visual representation on a composite video tape. In this manner, the actual position of the eyes could be compared to the electrical record.
RESULTS
It was quite evident on a purely qualitative basis that conjugate and symmetrical eye movements during caloric irrigation were the exception rather than the rule. Figure 1 shows the nystagmic responses from a normal subject. It is clearly apparent during the cold left response that the left eye has almost twice the amplitude and slow phase velocity of the right eye. This same situation is also seen with cold right stimulation: the ipsilateral eye shows approximately twice the amplitude and slow phase velocity as the contralateral eye. During the period of response to warm water, the eyes tend to be more conjugate, although the warm left stimulus led to a slightly higher velocity in the right eye. A more extreme difference between the two eyes in response to caloric stimulation is shown in Figure 2. Following irrigation with cold water, the ipsilateral eye is essentially producing the summated record; however, the warm stimulus leads to reversal and the contralateral eye reflects the greater magnitude of response. This patient was a 62-year-old male who had experienced a severe acute attack of vertigo with nausea and vomiting two months
MONOCULAR CALORIC RESPONSES
81
#855 WARM LFT
COLO LFT SUM V-A~JwA~~.J LFT
vJ\}\'J"!\f\J~
RT
20"L 2 SEC
WARM RT
COLD RT SUM
LFT r
I
' ,
1
RT
,1
I ~
:~
','
Fig. 2. Nystagmic responses from a clinical patient showing marked asymmetry of each eye.
prior to this test. At the time of the test, the patient had been asymptomatic for approximately six weeks. However, he did have a low-intensity (7° / sec) left beating nystagmus in the left lateral position. Based on [ongkees' formula," he also had a minimal (22%) directional preponderance to the left. That this type of response was related to the nature of the stimulus, rather than the clinical pathology, is supported by the fact that normals could give this same pattern of responses.
:# 1159 POSITIONAL LFT LATERAL SUM~--~--'-v·--""-v
RT
'D"L 'SEC
Fig. 3. Nystagmic responses from a clinical patient in the left lateral position.
The records from some patients showed results which were opposite to the previous cases; i.e., the subjects had a greater response from the contralateral eye during cold irrigation, which reversed to the ipsilateral side in response to the warm stimulus. The fact that one does not need a caloric stimulus to generate asymmetrical or disconjugate eye movements is clearly evident in Figure 3. As can be seen, this 49-year-old female had a positional nystagmus in the left lateral position that was being produced by the left eye; the summated record indicates a lower amplitude since the right eye is actually beating in the opposite direction. This patient had a three-yearhistory of dizziness which was aggravated by walking and a minimal hightone hearing loss. On a purely qualitative basis, it became evident that one could obtain almost any permutation of the nystagmic responses. The records also indicated that the cold stimulus appeared to pro-
82
JAMES W. WOLFE
opposite effect from that of the cold stimulus.
N=134 NORMALS Olff (R-l) Cl -15.1 CR 16.1 Wl 1.7 WR l.l
lEFT EYE RIGHT EYE --SUM - . - . >
~
~
P c.001 P cOOl NS NS
40
~ 30
~ 20 10 L - _ - , - - - - ----,
Cl
---T--
CR
Wl
--;I~---
WR
Fig. 4. Mean slow phase velocities for each stimulus condition for all patients; note that the ipsilateral eye shows ahnost twice the velocity of the contralateral eye following cold irrigation: (R-L), right minus left.
duce greater asymmetry than the warm. Therefore, it became obvious that only statistical analysis of a fairly large population would reveal the true relationships between the stimulus and the response. The first consideration was what percentage of the normal subjects and patients had only one eye moving during any of the stimulus conditions. Only two of the normal subjects had one eye that did not move during the warm or cold stimulation. Those patients with a bilateral hearing loss showed the greatest percentage of monocular responses under these same conditions. Since there were no significant differences in the caloric responses in the hearing loss left, right, or bilateral groups, their data were combined. When all hearing losses were combined, the data showed that over 39% of these patients had one eye that did not move during the various stimulations. Of those patients that had normal hearing and a major complaint of dizziness, 26% had only one eye moving during one or more of the caloric stimulations.
In all groups, cold water clearly produced a response decrement in the contralateral eye. The number of patients with monocular responses to warm stimulation was somewhat less and appeared to be more evenly distributed. There was a tendency for the ipsilateral eye to show more of a decrement, the
Analysis of the slow phase velocities for the summated, left and right eye data from the 134 patients classified as normal (directional preponderance < 20%; unilateral weakness 20%) within the 173 total patient population in this study. Figure 5 shows N=39 ABNORMAlS Olff(R-l) Cl -16.5 P
