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Periodic Alternating Nystagmus in Humans With Albinism

Richard V. Abadi* and Eve Pascatf

Purpose. To quantify the spatial and temporal nature of congenital periodic alternating nystag-mus (PAN) and to test the hypothesis that PAN results from a temporal shift in the null zone.

Methods. Twenty-five subjects with oculocutaneous albinism (16 tyrosinase negative and 9tyrosinase positive) and 7 with ocular albinism (5 x-linked and 2 autosomal recessive) partici-pated in the study. Using infrared oculography, five features of the nystagmus were examined:amplitude, frequency, waveform, beat direction, and temporal nature of the cycle.

Results. Twelve subjects (37.5%) exhibited a PAN. The nystagmus waveforms encounteredduring the PAN active phases were either jerk-with-extended-foveation or pseudocycloid,whereas a variety of oscillations (including triangular and bidirectional) were evident duringthe quiet phases. For most of the 12 subjects, there was an asymmetric variation in nystagmusintensity during each PAN cycle. None of the 12 demonstrated a convergence null or anabnormal head posture.

Conclusions. PAN is not an uncommon oscillation among humans with albinism. Changes ingaze position markedly influenced the periodicity of the ongoing nystagmus, thus supportingthe hypothesis that PAN is the result of a temporal shift in the null zone. Invest OphthalmolVis Sci. 1994; 35:4080-4086.

X eriodic alternating nystagmus (PAN) is a rare butwell-recognized form of involuntary nystagmus. Essen-tially, it is a conjugate, horizontal jerk oscillation inwhich regular reversals in the direction of the fastcomponent are separated by brief "quiet" intervals.The time period of each cycle is variable (60 to 360seconds) and may be asymmetric, such that the nystag-mus beating in one direction is of longer durationthan that beating in the opposite direction. Withineach "active" phase, the amplitude, frequency, andslow-phase velocity progressively change, whereas dur-ing the quiet phase (the null zone), the eye move-ments are often pendular and of low intensity.

In PAN, the null zone may be considered to beequivalent to the neutral zone (i.e., the position wherethere is a change in beat direction) as long as thereis not a high-amplitude pendular nystagmus presentduring the neutral zone of the nystagmus.

Current literature indicates that the majority ofpeople with PAN have acquired this ocular motor in-

From the *Department of Oplometry and Vision Sciences, The University ofManchester Institute of Science and Technology, Manchester, England, and the"[Department of Vision Sciences, Glasgow Caledonian University, Glasgow, Scotland.Submitted for publication September 20, 1993; revised May 23, 1994; acceptedfune.23, 1994.Proprietary interest category: N.Reprint requests: Dr. Richard V. Abadi, Department of Optomelry and VisionSciences, UM1ST, P.O. Box 88, Manchester, M60 1QD, England.

stability after disease of the caudal brainstem or cere-bellum.1"4 In comparison, there have been very fewpublished reports of congenital PAN,5"12 and in onlyfive cases has PAN been described in association withalbinism.51011

In recent years, we have had the opportunity tostudy the oculomotor behavior of a large number ofpeople with albinism and have been surprised to dis-cover that a significant portion exhibited PAN.12"14 Itis the purpose of this paper to quantify for the firsttime the nature of the periodicity and explore thefactors that influence beat direction and other charac-teristics of the nystagmus. More specifically, we carriedout experiments to test the hypothesis that PAN couldbe explained on the basis of continuous and regularshifts in the null zone over time.b Thus, at the start ofa typical cycle, with the null zone located in centralgaze, the PAN would be in its quiet phase. Thereafter,as the null zone moves off in one direction, (for exam-ple, to the right), a left-beating nystagmus should de-velop. It should be therefore possible to bring abouta reemergence of the quiet phase by either lookingto the right or turning the head to the left. Our experi-ments, using step changes in gaze position and pro-longed, eccentric-fixation extended gaze, do indeedsuggest that PAN results from both a spatial and tem-poral shift in the null zone.

4080Investigative Ophthalmology & Visual Science, November 1994, Vol. 35, No. 12Copyright © Association for Research in Vision and Ophthalmology

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Periodic Alternating Nystagmus 4081

MATERIALS AND METHODS

Binocular, horizontal eye movements were recordedusing infrared oculography.12 Subjects were instructedto fixate on a stationary circular white target (0.5°)projected onto a large uniform field (172° horizontalX 50° vertical). The target had a luminance of 4.1candelas per m2, and low internal room illuminationprovided background screen illuminance of approxi-mately 0.4 cd/m2. Five directions of gaze were exam-ined (-20°, -10°, 0°, +10°, and +20°) for time periodsof up to 8 minutes for each gaze position. In addition,the subjects were instructed to change gaze positionin response to step changes in target position. Duringrecording sessions, head movements were minimizedby the use of a chin rest and forehead restraint. Fourfeatures of the nystagmus were examined: amplitude,frequency, waveform, and beat direction. Amplitudeof the nystagmus was denned as the peak-to-peak slow-phase displacement, frequency as the number of oscil-lations per second, and intensity as amplitude X fre-quency. The velocity components of the slow phaseswere analyzed, using methods that have been de-scribed previously,1516 so that a profile of the constit-uent slow-phase velocities could be built up. A covertest was carried out on each subject to determine if astrabismus was present and also to detect the presenceof either a latent or manifest latent nystagmus.

The subject sample was comprised of 32 peoplewith albinism 8 to 57 years of age, 14 males and 18females (see Table 1). There were four pairs of siblingsand one group of three sisters. Within this sample, 16subjects had tyrosinase-negative oculocutaneous albi-nism (TNOCA), nine had tyrosinase-positive oculocu-taneous albinism (TPOCA), five had x-linked ocularalbinism (XOA) and two had autosomal-recessive ocu-lar albinism (AROA). All the subjects underwent fullassessment to ensure exclusion of subjects with otherocular disorders associated with congenital nystagmus.Biochemical tests and clinical examination, in combi-nation with personal and family history details, wereused to aid diagnosis.1317 Binocular visual acuitieswere recorded using a high-contrast (90%) Bailey -Lovie chart located in the primary position. Visualacuity was recorded as the log of the minimum angleof resolution (logMAR) from 1.0 (Snellen equivalent6/60) to 0.0 (Snellen equivalent 6/6).

The tenets of the Declaration of Helsinki werefollowed in this research. Informed consent was ob-tained from all subjects after the nature and possibleconsequences of the study had been explained.

RESULTS

Periodic Alternating Nystagmus

Twelve of the 32 subjects with albinism exhibited aPAN (Table 1). These subjects came from all four

^ V W V / W V \ ^ W V V Y Y V > ^ ^

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18

FIGURE l. Eye movement recordings from a TNOCA withcongenital PAN. This trace (which is not continuous intime) illustrates the temporal change in nystagmus wave-form, amplitude, and frequency as the horizontal, involun-tary oscillation goes through its cycle. The left and rightbeating phases are separated by quiet phases.

major categories of albinism (four TNOCA, fourTPOCA, two XOA, and two AROA). Although therewas a 100% incidence of PAN in the AROA group, thesmall number of subjects here makes any conclusionspremature. None of the 12 exhibited a convergencenull or an abnormal head posture. The waveformsencountered during the PAN active phases were eitherjerk with extended foveation or pseudocycloid, al-though two of the subjects also demonstrated dual jerkoscillations on occasions. This in itself is not surprisingbecause the jerk with extended foveation and pseu-docycloid waveforms are the ones most commonlyfound in adults with congenital nystagmus.1218'19 Allsubjects with PAN had strabismus, and none exhibiteda latent or manifest latent nystagmus.20 The use ofbinocular eye movement recordings and the cover testexcluded the possibility that the change in beat direc-tion of the nystagmus was due to a change in eyefixation. The PAN was a genuine time-varying changein the nystagmus beat direction during primary posi-tion fixation. Visual acuities among the 12 subjectsranged from 0.90 to 0.54 logMAR.


4082 Investigative Ophthalmology & Visual Science, November 1994, Vol. 35, No. 12

Periodic Alternating Nystagmus Cycle

Eye movement recordings from these 12 subjects re-vealed many differences in the nystagmus parameters.The duration of each PAN cycle displayed both in-tersubject and intrasubject variation. For all 12 sub-jects, mean cycle length was 271 seconds, with maxi-mum and minimum times of 141 and 430 seconds.Examination of our subjects on more than one occa-sion highlighted individual variation; for example,one TNOCA exhibited PAN cycles lasting 164, 225,240, and 301 seconds during central gaze on fourseparate visits. Some PAN cycles were also markedlyasymmetric, with one active phase being of longer du-ration than the other. This was particularly true forone subject with ocular albinism who had a right-beat-ing phase of 282 seconds and a left-beating phase of126 seconds.

Previous reports have claimed that, within oneactive phase, the nystagmus amplitude and frequencyprogressively change.5'812 Typically, the intensity is lowat the start of each jerk phase, gradually builds up to

50-|

40

30'

20

10-

©

50 100 150

Time (s)

200 250 300

FIGURE 2. (a) The temporal profile of slow phase eye velocity(—) and intensity ( ) during one PAN cycle for a sub-ject. Positive and negative values of the slow-phase eye veloc-ity represent left-beating and right-beating phases of thenystagmus, respectively, (b) Temporal profile of the dura-tion of the low-velocity period (i.e., the percentage of slowphase time when velocity was ^10°/sec) during the samePAN cycle.

15 -i

10 -

5 -

Right Beating

fi.-145 -115 -85 -55 -25 5 35 65 95 125 155 185 215 245

Slow Phase Velocity ( 7s)

15-1

10-

5 -

Left Beating

mu.-145 -115 -85 -55 -25 5 35 65 95 125 155 185 215 245

Slow Phase Velocity (7s)

FIGURE 3. Velocity histograms illustrating the percentage dis-tribution of velocities which make up the right-beating andleft-beating slow phases of the same subject's PAN (see Fig.2). Each histogram represents data from 10 seconds of con-tinuous recording.

a midcycle maximum, and decreases until the quietphase is reached. This periodicity was exhibited bymost of the subjects and is illustrated in Figure 1.

Mean slow-phase velocity, which is closely linkedto intensity, has also been shown to vary during PAN,but not in a simple sinusoidal fashion. Instead, tempo-ral velocity profiles of those with congenital and ac-quired PAN have revealed that slow-phase velocitybuilds up more quickly than it declines in each halfcycle.7'21 Figure 2a illustrates the variation in intensityand mean slow-phase velocity over time during a com-plete PAN cycle, for a subject with TNOCA. The cycleis relatively symmetrical with mean slow-phase velocityincreasing rapidly at the start of each half cycle, reach-ing the peak value after approximately 40 seconds,and then declining gradually in the subsequent 80seconds. A slightly greater maximum velocity wasfound during the left-beating phase: 65°/second com-pared with 51°/second for the right-beating phase.The temporal variation in intensity paralleled that ofthe slow-phase velocity but was consistently lower invalue. Investigation of the velocity components of theslow phases revealed that the percentage of slow phasetime spent at low retinal slip velocities also varied dur-



ing each PAN cycle. Figure 2b shows that this particu-lar subject had longer "foveation" periods (definedas the percentage of the slow phase spent at velocities<10°/second) during her right-beating phase, as com-pared with her preceding left-beating phase. This dif-ference is clearly illustrated in the velocity histogramsthat were constructed from data recorded on a sepa-rate occasion (Fig. 3). Here it can be seen that duringthe right-beating phase, up to 7.4% of the cycle wasmade up of velocities ^10°/second, whereas this wasonly true of 0.6% of the left-beating phase. In addi-tion, the mean slow-phase velocity was less during theright-beating phase.

Eleven of the 12 subjects with albinism with PANdid not have completely motionless eyes during theirquiet phases but exhibited a variety of oscillations suchas triangular, bidirectional, and pendular waveforms(Fig. 4). The duration of the three phases of PAN werefound to be subject to the same external influences asa nonperiodic congenital nystagmus.12 For instance,when the subject felt tired or anxious, the intensity ofthe oscillations increased, and the length of the quietphase shortened. In contrast, if the subject was re-laxed, the quiet phase tended to lengthen, resultingin the eyes remaining virtually stationary for severalseconds.

Effect of Gaze Changes on Periodic AlternatingNystagmus

To test the hypothesis that PAN results from a tempo-ral shift in the null zone, eye movements were moni-

10'

10"

FIGURE 4. The waveforms recorded from the quiet phase offour subjects with albinism with PAN. One subject (a) hadvirtually motionless eyes during this quiet period, but theothers displayed pendular (b), triangular (c), and bidirec-tional (d) oscillations.

00

RE

Target.

-10

0'

(b)

RE

Target

0'

+10*

RE

Target

10

1S

FIGURE 5. Eye movement recordings from a TPOCA subjectthat support the hypothesis that PAN results from a tempo-ral shift in the null zone. In (a), a change in gaze positionfrom the center (0°) to the left ( — 10°) resulted in the reap-pearance of the quiet phase. In (b), a right-beating nystag-mus was evoked when gaze position was altered from thecenter (0°) to the right ( + 10°) at the start of a left-beatingphase. In (c), right gaze ( + 10°) elicited a right-beating oscil-lation when a quiet phase was present in central gaze (0°).

tored at different gaze positions, in an attempt to"track" the null zone. For example, if a subject hadgone into the quiet phase after a period of right-beat-ing nystagmus, then looking into right gaze (i.e., towhere the null should then move) ought to prolongthe quiet phase. Similarly, it should also be possibleeither to abolish completely or to alter significantlythe PAN cycle (such that one active phase is muchlonger than the other) by instructing the subject tomaintain fixation on a horizontally eccentric stimulus.Examination of the resulting eye movement traces re-vealed that it was indeed possible to interrupt the on-going PAN cycle and "chase" the null zone on someoccasions (Fig. 5).

To explore this effect further, the eye movementsof seven subjects with albinism and one with idiopathiccongenital PAN were recorded at three gaze positions(0°, +20°, and —20°). At each gaze, position fixationwas maintained until a complete PAN cycle had beenrecorded or until it became clear that the involuntaryoscillations were not going to change direction—usu-ally after a period of 6 minutes. The subjects weregiven a short rest after each period of fixation.



100-

8 0 -

6 0 -

4 0 -

2 0 -

0

CG CHa

llIll-20 0 +20

Gaze Position

-20 0 +20

Gaze Position

100-p8 0 -

6 0 -

4 0 -

2 0 -

0

CHo

-20 0 +20

Gaze Position

RE

tuI#

100-

8 0 -

6 0 -

4 0 -

2 0 -

IH111

-20 0 +20

Gaze Position

-20 0 +20

Gaze Position

100-1

80

6 0 -

4 0 -

2 0 -

0

SL

-20 0 +20

Gaze Position

100

8 0 -

6 0 -

4 0 -

2 0 -

0

TD

-20 0 +20

100-

8 0 -

6 0 -

4 0 -

2 0 -

0

SM

-20 0 +20

Left Beating

Quiet

Right Beating

Gaze Position Gaze Position

FIGURE 6. The effect of gaze position on the percentage of right-beating and left-beatingnystagmus per PAN cycle. Histograms for seven subjects with albinism and one with idiopathyare shown.

The percentages of time spent in the right-beat-ing, left-beating, and quiet phases were then calcu-lated for every PAN cycle. Figure 6 illustrates that, forall eight subjects who participated in this part of thestudy, gaze position influenced the proportions ofright-beating and left-beating nystagmus compared toprimary gaze. In four of the cases, there was an in-crease in the duration of the centrifugally beating nys-tagmus (i.e., right-beating on right gaze, left-beatingon left gaze) at the expense of the other phase,whereas in others, the PAN cycle disappeared. Twosubjects "lost" the periodicity of their nystagmus inboth directions of gaze, and two others exhibited anasymmetrical PAN in right gaze and a left-beating nys-tagmus in left gaze. As a general rule, holding aneccentric gaze position biased the directionality of thenystagmus beat for each complete cycle. Thus, duringright gaze, the time given to a right-beating nystagmuswas far greater than that seen during central gaze.This would suggest that it is predominantly the move-ment of the null zone that is responsible for the natureof the periodicity.

DISCUSSION

Our recent investigations have indicated that PANmay not be uncommon in humans with albinism.12"14

This study has established that this is indeed the case:37% of our subjects exhibited a PAN. Despite the smallsize of our sample (n = 32), it is unlikely that thiswas a chance finding because the relative number ofsubjects with albinism with PAN was large. In addition,those subjects with PAN did not have particularly pooracuity or other apparent visual problems that mighthave led to a greater level of referral to our laboratory.One possible explanation for such a high incidenceis that in our laboratory we routinely monitor fixa-tional eye movements over long continuous periods.In other published studies of people with albinism,any PAN may have been missed because recordingsessions were too short to reveal the spontaneouschanges in nystagmus beat direction.10'22 A larger sam-ple of people with albinism would need to be investi-gated to establish the real frequency of congenitalPAN in people with albinism.



TABLE i. Summary of the Eye Movement Behavior of the Original32 Subjects with Albinism

Number of subjectsAge rangeVA rangeStrabismus

Cn WaveformJef

PCJdvPPfeDJAPPC + PJef+DJPC + DJTorsion

PANSpatial null /oneConvergence nullAbnormal head postureHead nodding

TNOCA

1612-57 years0.52-1.00

16

4*5**

In—1211

——1*

—

443

104

TPOCA

913-52 years0.34-0.92

9

3*$**

———1

——1*

—1

42263

XOA

58-40 years0.70-1.12

5

2**1

—————2———21151

AROA

215-38 years0.80-0.86

2

1*1*

————————

20021

* Identifies 12 subjects with periodic alternating nystagmus (PAN). Visual acuity is given in logMAR.The dominant waveforms on primary gaze were either Jef (jerk with extended foveation), PC(pseudocycloid), Jdv (jerk with decreasing velocity), P (pendular), Pfs (pendular with fnvealingsaccades), DJ (dual jerk), or AP (asymmetric pendular). Sonic subjects exhibited a combination ofwaveforms, and one subject had a jerk with decreasing velocity slow phase (Jdv) waveform.

Although the variation in PAN timing with gazeposition has been mentioned in several other smallerstudies,3"7" this has often been in a qualitative man-ner. Our present research conclusively supports thehypothesis originally put forward by Daroff andDell'Osso6 that PAN results from a temporal shiftingof the null zone. It is also of interest that accuratefoveation during the minimum velocity period of theslow phase of each waveform can still be achieved evenwith this form of nystagmus periodicity.14 Theoreti-cally, a slow rotation of the head away from the direc-tion of the null zone should bring the null back tocenter again. This head-turning strategy is sometimesadopted by a PAN subject but was not evident in oursample. This is not surprising because the adoptionof an alternating head posture would require not onlythe precise control of the head posture, but also aregular periodicity in the shifting of the null zone.Moreover, even subjects with a congenital nystagmusand a static null zone may not adopt predictable headpostures.23

In a parallel study, we also examined subjects withidiopathic congenital PAN, and the spatial and tempo-ral nature of their involuntary oscillations appear tobe indistinguishable from those of the albino group.24

Thus, any attempt to elucidate the mechanisms be-hind PAN cannot rely on features that are unique toalbinism. For example, the suggestion that PAN or

nystagmus in general in albinism is a result of visualpathway misrouting seems improbable.10'"""

To date, there has been only one report of a PANin an albino animal. Guillery and his colleagues, whowere principally studying the aberrant visual pathwaysin a single albino green monkey, described a periodicnystagmus but gave no further details of the spatial ortemporal characteristics of the oscillations.25 Althoughit is tempting to suggest that this is further evidenceof the close relationship between congenital PAN andalbinism, the possibility of the PAN being secondary tocentral nervous system disease cannot be excluded.1"4

The etiology of PAN, both acquired and congeni-tal, has received some attention, but as yet no firmconclusions have been reached. Although the shiftingnull may represent a valid interpretation of these peri-odic oscillations and could account for the influenceof gaze position on the PAN cycle found in this andother studies, it does not explain how or why the peri-odicity develops. Some years ago, Leigh and col-leagues21 described a hypothetical model of PAN thatrelied on an instability in the neural mechanisms thatgenerate vestibular and optokinetic slow phases, com-bined with an inability to process retinal velocity errorsignals. Based on physiological data, this model gener-ated linear slow-phase oscillations with characteristicssimilar to acquired PAN and could predict a criticalrotational stimulus that temporarily stopped die PAN



of one individual. This model may not be fully appro-priate to explain a congenital PAN, because in thecongenital form, the slow phases are not linear butare almost always of an increasing velocity type.

More recently, Harris26 proposed that congenitalnystagmus was due to an excess gain in the internalefference copy, positive feedback loop of the smoothpursuit system. The efference copy is a velocity feed-back signal from the output of the common neuralintegrator of the ocular motor system (i.e., the posi-tion signal output of the neural integrator is differenti-ated and fed back). He further hypothesized the no-tion of two nulls, a velocity null and a positional null,to account for the null shifting found in PAN. Thenext stage of our work is to explore whether eithermodel can successfully mimic congenital PAN, includ-ing features such as the typical waveforms and thechanges in cycle with gaze angle, and also take intoaccount the fact that these subjects with congenitalnystagmus still have operational vestibular, optoki-netic, and pursuit systems, within the confines of eachfoveation period.

Key Words

albino, periodic alternating nystagmus, null zone

References

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6. Daroff RD, Dell'Osso LF. Periodic alternating nystag-mus and the shifting null. Can f Otolaryngol.1974;3:367-371.

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9. Cross SA, Smith JL, Norton EWD. Periodic alternating

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12. Abadi RV, Dickinson CM. Waveform characteristics incongenital nystagmus. Doc Ophthalmol. 1986; 64:153-167.

13. Abadi RV, Pascal E. The recognition and managementof albinism. Ophthalmic Physiol Opt. 1989;9:3-15.

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16. Worfolk R, Abadi RV. Quick phase programming andsaccadic re-orientation in congenital nystagmus. VisionRes. 1991;31:1819-1830.

17. Abadi RV, Cox MJ. The distribution of macular pig-ment in human albinos. Invest Ophthalmol Vis Sri.1992; 33:494-497.

18. Dell'Osso LF, Daroff RB. Congenital nystagmus wave-forms and foveation strategy. Doc Ophthalmol.1975;39:155-182.

19. Yee RD, Wong EK, Baloh RW, Honrubia V. A studyof congenital nystagmus: Waveforms. Neurology.1976; 26:326-333.

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21. Leigh RJ, Robinson DA, Zee DS. A hypothetical expla-nation for periodic alternating nystagmus: Instabilityin the optokinetic-vestibular system. Ann NY Acad Sri.1981;374:619-635.

22. St. John R, FiskJD, Timney B, Goodale MA. Eye move-ments of human albinos. Am ] Optom Physiol Opt.1984;61:377-385.

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25. Guillery RW, Hickey TL, Kass JH, Felleman DJ, DeBruyn EJ, Sparks DL. Abnormal central visual path-ways in the brain of an albino green monkey. / CompNeurol. 1984; 226:165-183.

26. Harris CM. Problems in modelling congenital nystag-mus. In: Findlay J, ed. Eye Movement Research: Processes,Mechanisms and Applications. Amsterdam: Elsevier;1993.


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