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Corrective movements following refixation saccades: Type and control system analysis
Vfafon Res. Vol. 12, pp. 467-475. Porgamon Prom 1972. Printed in @‘oat Britain
CORRECTIVE MOVEMENTS FOLLOWING REFIXATION SACCADES: TYPE AND CONTROL SYSTEM ANALYSIS RONALDB. WEBERand ROBERTB. DAROFF Ocular
Motor NeurophysiologyLaboratory, Mii VeteransAdministrationHospital,and The Department of Neurology, Universityof Miami School of Medicine,Miami, Florida 33125,U.S.A. (Received 10 June 1971; in revised form 10 August 1971)
EARLYinvestigators recognized a variability in the accuracy of saccadic eye movements, noting in particular a tendency for the eyes to fall short of the target (D-RN, 1904; MCALLISTW, 1905 ; DODGE, 1907 ; MILES, 1929). The frequency of eye-target errors was proportional to the angular displacement of the fixation points. In a detailed presentation of the metric characteristics of saccadic movements in 25 human subjects (WEB= and DAROFF,1971), we reaffirmed that the major influence upon saccadic precision is amplitude of the refixation. Nearly 70 per cent of 10 deg saccades were normometric (required no correction). The remaining trials at this amplitude demonstrated conjugate undershoots (12.8 per cent), overshoots (9.3 per cent) or a brief dysconjugacy (9-S per cent). At 20 deg, fewer saccades were normometric (43 per cent), undershoots became more prevalent, overshoots decreased slightly, and dysconjugacies increased. The tendency towards inaccuracy (dysmetria) was more evident at refixations of 30 deg. Here, fewer than 20 per cent of trials were normometric, more than 50 per cent undershot conjugately, overshoots were rare, and 27 per cent terminated dysconjugately. This last situation was usually produced by monocular dysmetria- overshoot of the adducting eye or undershoot of the abducting eye. Considering all three amplitudes studied (10, 20 and 30 deg), 4.5~7per cent (of 4353 trials) were normometric, 37.5 per cent were conjugately dysmetric (conjugate undershooting: 30.9 per cent; conjugate overshooting: 6.6 per cent), and 16.7 per cent demonstrated dysconjugate dysmetria (monocular undershoot and/or overshoot). All dysmetric saccades are followed by a small corrective movement which ~omplishes alignment of the fovea with the new fixation target. Analysis of these corrective movements, for both conjugate and dysconjugate refixational errors, and a discussion of the possible feedback mechanisms involved in their generation, forms the basis of this report. METHOD The exact details of the methodology are describedelsewhere(WJWR and DAROFF,1971). Cameo-retinal potentials from each eye were d.c. coupled to a BeckmanType R 8 channel Dynograph. The fkst of each pair of osciliograph channels recorded amplitude and direction of ocular displacement. First stage preamplifiers contained a 60 Hz notch filter. The system band width was 25 Hz. An step auxiliary output signal from the eye position preamplifier was jumpered into a second cbel where it was di&rentiated to derive instantaneous velocity (Voom, 1969). All recordings were curvilinear and inkwritten at a chart speed of 250 mm/set. We seleaed electro-oculography (EOG) as the recording technique because it is a reliable monitor of eye movements greater than 15 deg and permits s~~t~eous binocular analysis. Frequent recalibration precludes SPUI+OUS alterations of pen deflection amplitudes secondary to fluctuations of the cameo-retinal 467
RONALD B. WEBERAND ROBHIT B. DAROFF
468
potential. EGG drift is minimized by careful skin preparation and electrode application. A filter reduces the upper roll-off (- 3 db) frequency to 25 Hz which provides a relatively noisefree output. This facilitates comparative analysis of the terminal portions of the slopes. The resultant damping of the trajectory trace is identical in all channels and acceptable for the purposes of our study. We recorded several subjects with an i.r. photoehztric technique (YOUNG, 19631, and obtained identical trace patterns as with EOG. This supports the app~~biIity of EGG for quantitative analysis of eye movements. Fixation targets were tungsten filament 1 cm dia. white bulbs, masked with white paint to eliminate glare. The lamps were mounted on a flat black background and subtended visual angles of 0, 10, 20 and 30 deg to the left and right of the subject’s “cycIopean eye” when the 0 deg light was 44” from the cornea. Twenty-five normals, mean age 30.1 yr, served as subjects (Ss). We eliminated volunteers with poor uncorrected vision or high diopter phorias. No subjects had taken sedatives, hypnotics, or anti-convulsants prior to testing. Each S performed a series of regular to-and-fro saccades between the fixation light of 0 deg and a selectively illuminated light at lo,20 and 30 deg to the left and right (e.g. from 0 to 10 deg right and back, O”-2O”R-O”, etc.). Several reversals were recorded at each amplitude and then the oscihograph was recalibrated. We examined 4353 individual eye movements and manually converted the analogs to digits for computer analysis (WEBER and DAROFF, 1971). RESULTS
The data concerning saccadic metrics appear elsewhere (WEBER and DAROFF, 197 I) and are summarized in the introduction to this report. We will herein be concerned with the corrective movements (CMs) which follow all dysmetric saccades. Two types of CMs occurred. One, designated saccadic CM, was fast, had a definite latency, and always foIlowed conjugate errors. The other was slow, drift-like, without a latency, and corrected dysconjugate retjxations. We utilized the term giissadic CM for this latter variety. Saccadic corrective movements
The saccadic correction was distinctive, easily recognized, equal in both eyes, and followed all binocular (conjugate) errors. Its rapid acceleration resulted in a conspicuous CONJUGATE UNDERSHOOT
100 msec Fm. 1. R&rational ~~~~~p~t a~
saceade from primary position to target 20 deg to the fight. The fhst and position of left (LE) and right eye (RR), respectively. The gccond and demon&ate the d%arentiated peak vem. Roth eyea i%%&CQt by 2 &g and, after 125 msec, binocular conjugate saccam corre&?e movements align the eyes with the target.
Corrective Movements following Refixation Saccades
469
step-like deflection of the EOG baseline (Figs. 1 and 2). A 3-deg movement was accomplished in less than 25 msec. The latencies from the termination of the initial movement until the onset of the corrective movements were approximately 125 msec (124-5 f 10.5 S.D.). This latency was the same with saccadic corrections for undershoots (positive CMs) and overshoots (negative CMs). CONJUGATE
OVERSHOOT
Lt
4ooq set-1
RE
100 Era. 2.
Conjugate overshoot corrected by saccadic CM. 2.0
t
CONJUGATE
10 3.
ERRORS
30
20 TARGET
FIG.
mei
DISTANCE
/degrees)
Relationship of interfixationai distance to mean size of binocular (conjugate) error.
The size of saccadic CMs increased monotonically with interGxationa1 distance (Fig. 3). The mean sizes of positive CMs for IO, 20 and 30 deg interfixational distances were l-3, 1.6 and l-8 deg respectively. For negative CMs the respective sizes were 1.2, l-3 and 1.5 deg.
470
RONALDB. WEBER AND ROBERT B. DAROFF
Glissadic corrective movements
This type of correction was of low velocity (approximately 20 deg/sec) and inseparable from the terminal portion of the saccade (Figs. 4 and 5). There was therefore no latency between the end of the initial saccade and the beginning of the correction. As previously stated, glissadic CMs exclusively followed dysconjugate errors. The glissadic CM size-interfixational distance relationship approximated those of saccadic CMs (Fig. 6). DYSCONJUGATE
UNDERSHOOT
I
-I
100 msec FIG. 4. Sac&e
from 20 deg left to primary position. Right eye (RE) undershoots target by
approximately2 deg
followed by a glissadic corrective less than 1 deg.
30”
movement.The left eye overshoots by
I
LE 4oo” I set -1
3o”
I
RE
100 msec FIO .
5. Uniocuku overshoot of LE followed by glissadic CM.
Corrective Movements following Refixation Saccades
DYSCONJUGATE
2.0
471
ERRORS r*
Ho
*/ f ?1 F
3
0’ d
1.5
4’
9
,’
/ 4’ 4’
5 0
z
30
4’
.-.
OVERSHOOT
o---o
UNDERSHOOT
20
10 TARGET
FIG. 6.
DISTANCE
(degrees)
Relationship of interfixaGona1 distance to mean size of dysconjugate unlocuhr error.
Saccadicprecision-amplituderelationships The results of our present and previous (WEBERand DAROFF,1971) studies indicate the following relationships of ocular response to increasing interfixational distance: (1) The incidence of dysmetria increases. (2) The incidence of positive CMs (fol undershoots) increases. (3) The incidence of negative CMs (for overshoots) decreases. (4) The size of all CMs increases. DISCUSSION Refixation
saccades
bring peripherally placed objects into central vision by sliding the
fovea under the object image. If the image is not captured on the fovea with the initial refixation saccade, the remaining error is resolved by an involuntary corrective movement (CM). This correction, we have determined, is always saccadic when the error is binocularly equal (conjugate) and slow (glissadic) following uniocular (dysconjugate) errors. With the aid of magnification, we were able to measure trace amplitudes accurately to approximately O-25 mm (30 arc min). In our tabulations, we regarded only eyes : target and eye:eye errors of 1 deg or greater, followed by a CM, as dysmetric (WEBEXand DAROFF, 1971). Smaller errors, indistinguishable from pre-terminal fusional vergence movements, were classified as normometric. In our target display, the angle of convergence in primary position (3” 4’) was 46 min greater than at 30 deg. We considered the possibility that the movements ultimately designated “glissadic CM” merely represented asymmetrical vergence (ZUBEX,1967). This we deemed unlikely for the following reasons: (1) there was considerable inter- and intra-subject variability of dysconjugate saccades (WEBFJR and DAROFF, 1971), despite the fixed difference in convergence angle between targets; (2) the magnitude of the errors (l-3 deg) exceeded the change in vergence angle; (3) since the greatest angle of convergence is in primary position, centering saccades were always to a target requiring increased convergence angle and, indeed, the greatest incidence of overconvergence (due to adductor overshoot or abductor undershoot) occurred with center-directed saccades. The
472
RONALD B. WEBER AND
ROBERT B. DAKOFF
corrective movement in these circumstances was therefore dicergent. Although it may t-x argued that the vergence angle change between targets was somehow responsible for the occurrence of the dysconjugate saccades, it does not follow that the subsequent corrective movements were fusional ; (4) the frequency and magnitude of convergerlt saccades (followed by glissadic CMs) did not decrease (actuaIly increased) when the subject : target distance was extended from 44” to 69” (WEBERand DAROFF,1971); and (5) we determined (unpublished experiments) that subjects making refixations with one eye occluded demonstrated dys~onjugate saccades followed by glissadic CMs. These occurred in both the seeing and occluded eyes. The reaction times (latency) of voluntary refixation and corrective saccades differ markedly. Corrective saccades of any size have nearly constant latencies of approximately 125 msec. In an unpublished experiment, we instructed subjects to make retiation saccades between objects separated by 20 deg followed by a second refixation to another object 2 deg away. The latter movements were performed in both positive and negative directions. The mean reaction time before the second saccade was 369 msec for positive steps and 468 msec for negative movements. These results confirm those of LEUSHINA(1965) who reported an inverse relationship between reaction time and intertixational distances for retIxation saccades. These saccades presumably require time-consuming discrimination of visual info~ation, whereas the short latency corrective saccades occur inde~ndent of visual feedback. BECKERand FUCHS (1969) determined that for 40 deg refixations, most subjects fell short of the target with the initial saccade and required a positive corrective saccade which had a mean latency of 127 msec. These same subjects performed almost identical 2-step saccades in darkness where visual feedback information was unavailable. Becker and Fuchs postulated that these large (40 deg) fixation changes may be preprogrammed as a package consisting of two movements: an initial large saccade which undershoots the targets, followed by a smaller corrective saccade. The “pre-packaged” concept would account for the short latency of the second saccade. Our study of saccadic metrics at IO,20 and 30 deg demonstrated an inter- and intra-subject spectrum of undershoots, overshoots, dysconjugate, as well as normometric movements (WEBERand DAROFF,1971). This variability and inconsistency renders “pre-packaging” an unlikely explanation, in our opinion, for the corrective movements following dysmetric smaller amplitude refixation saccades. We repeated Becker and Fuchs’ study of saccades in darkness but utilized 10-30 deg distances. The same pattern of dysmetria and consequent CMs observed with visible targets also occurred in darkness. This provides further evidence against any possible rofe of visual feedback in the generation of CMs. Mechanisms other than visual feedback and “pre-packaging” are therefore necessary to account for saccadic CMs with refixarions less than 40 deg. An obvious alternative is feedback from stretch receptors in extraocular muscles (proprioceptive loop, Fig. 7). Experimental (VOSSIUS,1960; FUCHSand KORNHUBER,1969) and clinical (HIGGINSand DAROFF, 1966) studies support the significance of this loop. Despite the physiologic and cybernetic appeal of such a mechanism (Brzzr and EVAKW, 1971), the func~on~ importance of stretch receptor feedback from eye muscles remains unproved (FILLENZ, 1955; STARK, 1968; PEXRYAUNand BR~RNIN,1971). “Response feedback” (pxoprioceptive or visual} cannot explain the no-delay ghssadic corrective movement which follow dysconjugate dysmetria. A reasonable hypothesis for gtissadic CMs involves prenuclear feedback (Fig. 7). Actual output is monitored at the brain
473
Corrective Movements following Refutation Saccades
Fro. 7. Simplified diagram proposed for ocular motor control system. The bolder lines indicate those aspects of the schema relevant to our study. (PPRF refers to pontine paramedian reticular formation.)
stem level and, if incompatible with the desired output, a corrective movement is generated by the pontine paramedian reticular formation (PPRF).l In this instance, where no latency is discernible, the correction is continuous with the saccade. Only an internal monitor could detect asymmetric outflow and rectify the condition “in flight”. JOHNSON (1963) postulated the existence of a similar loop which he designated “oculomotor monitoring”. EVARTS(1971) recently reviewed in detail the importance of this type of internal feedback in the regulation of all voluntary movements. Internal feedback seems the best explanation for the glissadic CMs following dysconjugate refixation saccades. A similar mechanism could account for saccadic CMs as well, particularly if further studies fail to establish the functional significance of proprioceptive feedback from eye muscles. authors extend their appreciation to Dr. ALVAN R. FEINSTEINand Mrs. ELIZABETH the Eastern Research Support Center, West Haven (Connecticut) Veterans Administration Hospital, for computer programming and analysis; to Dr. Lours Dx~~‘Osso for advice and constructive
Acknowledgements-The C. WRIGHT of
criticism; to RICHARDNAMON, biophysicist, technical assistance.
who refined our instrumentation;
and to Mr. MEL JOHNSINfor
REFERENCES BECKER,W.
and Fucrrs, A. F. (1969). Further properties of the human saccadic system: Eye movements and
correction saccades with and without visual fixation points. Vison Res. 9, 1247-1258. BIZZI, E. and EVAR~S,E. V. (1971). Translational mechanisms between input and output. In Central Control of Movement (edited by E. V. EVAIUS, et al.), Neurosciences Res. Prog. BUN. 9,31-59. DAROPF,R. B. and HOYT, W. F. (1971). Supranuclear disorders of ocular control systems in man: Clinical, anatomical and physiological correlations, 1969. In l?re Control of Eye Movements (edited by P. BACHY-RITAand C. C. COLLINS).Academic Press, New York. DEARBORN,W. F. (1904). Retinal local signs. Psychol. Rev. 11,297-307. DODGE, R. (1907). An experimental study of visual fixation. Psycho/. Monogr. 8, l-95.
r The PPRF is the final prenuclear anatomical substrate horizontal eye movements (DAROFFand HOYT, 1971).
for the generation
of saccadic and pursuit
RONALDB.
474
WEB~RANDROBERTB. DAROFF
EVARTS,E. V. (1971). Feedback and corollary discharge: A merging of the concepts. In Central Confro( u Movement (edited by E. V. EVARXet al.), Neurosciences Res. Prog. BUN.9, 86-l 12. RLLENZ, M. (1955). Responses in brainstem of the cat to stretch of extrinsic ocular mucks. J. Physic& Land. 128, 182-199. FUCHS,A. F. and KORNHUBER, H. H. (1969). Extraocular afferents to the cerebellum of the cat. J. Physiol.,
Land* 250,713-722. I&GGINS,D. C. and DAROFF,R. B. (1966). Overshoot and osciflation in ocular dysmetria. Archs Opht~l. 79, 742-745. JOHNSON, L. E., JR. (1963). Human eye tracking of aperiodic target functions. 37-B-63-8, Systems Reseamh
Center, Case Institute of Technology, Cleveland, Ohio. LEUSHINA,L. I. (1965). On estimation of position of photo stimulus and eye movements. Biofizika 10, 130-136. MCALLISTER, C. N. (1905). The fixation points in the visual field. Psycbol. Monogr. 7, 17-53. ti, W. R. (1929). Horizontal eye movements at the onset of sleep. PsychoL Rev. ‘36, 122-141. STARK,L. (1968). Neurological Control Systems; Studies in Bioeq#neering, p. 233. Plenum Press, New York. Voors, R. H. (1969). Computerless automatic data reduction for electronystagmography. Aerospace Med. 40,108~1086.
Vossrus, G. (1960). Das System der Along. 2. Bioi. 112,27-57. WEZ?IZR, R. B. and DARO~, R. B. (1971). The metrics of horizontal saccadic eye movements in normal humans. Vision Res. 11,921-928. YOUNQ,L. R. (1963). Measuring eye movements. Am. J. Med. EZectronics4,3od307. ZVIIER,B. L. (1967). Asymmetrical fusional vergenw Eye movements maul&g from target movement along the visual axis of one eye. Presbyterian-St. Luke’s Hosp. Med. Bull. 6, 15-20.
Ah&aet-Rational sacu&es frequently do not achieve the intandsd ampfihtde with the. initial displaoemsnt; the errors am binocular saa~dic (high-v8locity) after a 125 msee latency. Slow, dr#t-Bk8 original SBccBde,correct dysconjugate errors. We discuss the possiile rokrp and visual, proprioc8ptive and internal pmnuel8ar fGedback in the g8naration of CM% We conclude that a prenucl8ar intemal monitor be& accounts for gBwadl8 CMa wk8reas saaxdic CMs may be explained by either proprioceptive fsedttack or an internal monitor.
R&tm&--Les saccades de re-fixation ant frequemment une amplitude qui n’est pas celle qui convient au d6placement initial; les erruers sent soit conjugu&s (&al8s pour les deux yeux) soit dysconjugu8es. Un mouvement de correction (CM) binocuh&e, sac4ad8 st rapide, suit la position conjugu88 error&r ap&s 125 resee de latence. Les errems dygcQq*b sent corrigees par des CM de doriveslentes qui contiauent la tin de la saccade original8 Qn discute les r8Ies possibles des feedbacks visuek, proprioceptifa et pr6nucl&ires internes, darts ia g&&ration des CM. On conclut que les derives s’expliquent au mieux par un r8glage p&u&aire inteme,tandis que IesCMsaccad~ s’expliquent soit par un f~~~kprop~o~pt~,soit par un r&dage inteme.
intemen Monitor erklart werden kbnnen.
Corrective Movements
following Re6xation
Saccades
Pesmr+Ie - Pe@xaqomib~e CagKaAb~ YacTo He n=amT HaMegemo aMnrraTyAb& no CpaBHemiH) c Ha’IaTIbHbIMCMememieM: O~E~KE 6bIsaIoT JIE~O oJ@iriaxoabIbm B 06051~ maxix (conjugate), ~11x60He O~CIH~KOB~IMH (dysconjugate). %mo~y~~paoe car(g~ec~oe (BbICOKo-cKOpOCTHOe) KOpperEpyIoIsW wChfeTp&iet c naTeErTHbxh4 IIepHoAoM
KA, npo~onxcaxomaxx
,lWiXeIiEe oc4, COIIpOBOXQaeTCX KOWHJraJJEOHHOti B 125 MWK. Meanemax “~aBaH)~aR" rnaccapa
nocxe oKomaxna
nepsoaauaHoi3
caxxam1, EcnpasJureT OKIH~KH
,QECKOH%IOraQE&f.~6C~aeTCKBO3MOXCKaHpOJIbBB03HSiKIiOBeHEiE Kfl ‘?fpeJtJ'rOTOBaHHOii" a3p~eJIb~o~,~po~~o~em~~oZt~B~pe~eP~0~~eap~0tto6paT~o~c~~a~re~epauuIl KH.M~III~RIIIwKB~~BOW,¶TOII~~~~~~~~H~I~ BmpeHHHfi EH~J~KTO~ xopo111oo6~1c~~eT rmrccany KA, Torna KaK camamecme KA MOXCHO O~WICHEIX11x160nponpnouerrrnBHofi o6paTHog CBS'~~~IOHJ~~X~B~~~HF~HMHHAJ'KTO~OM.
475
CORRECTIVE MOVEMENTS FOLLOWING REFIXATION SACCADES: TYPE AND CONTROL SYSTEM ANALYSIS RONALDB. WEBERand ROBERTB. DAROFF Ocular
Motor NeurophysiologyLaboratory, Mii VeteransAdministrationHospital,and The Department of Neurology, Universityof Miami School of Medicine,Miami, Florida 33125,U.S.A. (Received 10 June 1971; in revised form 10 August 1971)
EARLYinvestigators recognized a variability in the accuracy of saccadic eye movements, noting in particular a tendency for the eyes to fall short of the target (D-RN, 1904; MCALLISTW, 1905 ; DODGE, 1907 ; MILES, 1929). The frequency of eye-target errors was proportional to the angular displacement of the fixation points. In a detailed presentation of the metric characteristics of saccadic movements in 25 human subjects (WEB= and DAROFF,1971), we reaffirmed that the major influence upon saccadic precision is amplitude of the refixation. Nearly 70 per cent of 10 deg saccades were normometric (required no correction). The remaining trials at this amplitude demonstrated conjugate undershoots (12.8 per cent), overshoots (9.3 per cent) or a brief dysconjugacy (9-S per cent). At 20 deg, fewer saccades were normometric (43 per cent), undershoots became more prevalent, overshoots decreased slightly, and dysconjugacies increased. The tendency towards inaccuracy (dysmetria) was more evident at refixations of 30 deg. Here, fewer than 20 per cent of trials were normometric, more than 50 per cent undershot conjugately, overshoots were rare, and 27 per cent terminated dysconjugately. This last situation was usually produced by monocular dysmetria- overshoot of the adducting eye or undershoot of the abducting eye. Considering all three amplitudes studied (10, 20 and 30 deg), 4.5~7per cent (of 4353 trials) were normometric, 37.5 per cent were conjugately dysmetric (conjugate undershooting: 30.9 per cent; conjugate overshooting: 6.6 per cent), and 16.7 per cent demonstrated dysconjugate dysmetria (monocular undershoot and/or overshoot). All dysmetric saccades are followed by a small corrective movement which ~omplishes alignment of the fovea with the new fixation target. Analysis of these corrective movements, for both conjugate and dysconjugate refixational errors, and a discussion of the possible feedback mechanisms involved in their generation, forms the basis of this report. METHOD The exact details of the methodology are describedelsewhere(WJWR and DAROFF,1971). Cameo-retinal potentials from each eye were d.c. coupled to a BeckmanType R 8 channel Dynograph. The fkst of each pair of osciliograph channels recorded amplitude and direction of ocular displacement. First stage preamplifiers contained a 60 Hz notch filter. The system band width was 25 Hz. An step auxiliary output signal from the eye position preamplifier was jumpered into a second cbel where it was di&rentiated to derive instantaneous velocity (Voom, 1969). All recordings were curvilinear and inkwritten at a chart speed of 250 mm/set. We seleaed electro-oculography (EOG) as the recording technique because it is a reliable monitor of eye movements greater than 15 deg and permits s~~t~eous binocular analysis. Frequent recalibration precludes SPUI+OUS alterations of pen deflection amplitudes secondary to fluctuations of the cameo-retinal 467
RONALD B. WEBERAND ROBHIT B. DAROFF
468
potential. EGG drift is minimized by careful skin preparation and electrode application. A filter reduces the upper roll-off (- 3 db) frequency to 25 Hz which provides a relatively noisefree output. This facilitates comparative analysis of the terminal portions of the slopes. The resultant damping of the trajectory trace is identical in all channels and acceptable for the purposes of our study. We recorded several subjects with an i.r. photoehztric technique (YOUNG, 19631, and obtained identical trace patterns as with EOG. This supports the app~~biIity of EGG for quantitative analysis of eye movements. Fixation targets were tungsten filament 1 cm dia. white bulbs, masked with white paint to eliminate glare. The lamps were mounted on a flat black background and subtended visual angles of 0, 10, 20 and 30 deg to the left and right of the subject’s “cycIopean eye” when the 0 deg light was 44” from the cornea. Twenty-five normals, mean age 30.1 yr, served as subjects (Ss). We eliminated volunteers with poor uncorrected vision or high diopter phorias. No subjects had taken sedatives, hypnotics, or anti-convulsants prior to testing. Each S performed a series of regular to-and-fro saccades between the fixation light of 0 deg and a selectively illuminated light at lo,20 and 30 deg to the left and right (e.g. from 0 to 10 deg right and back, O”-2O”R-O”, etc.). Several reversals were recorded at each amplitude and then the oscihograph was recalibrated. We examined 4353 individual eye movements and manually converted the analogs to digits for computer analysis (WEBER and DAROFF, 1971). RESULTS
The data concerning saccadic metrics appear elsewhere (WEBER and DAROFF, 197 I) and are summarized in the introduction to this report. We will herein be concerned with the corrective movements (CMs) which follow all dysmetric saccades. Two types of CMs occurred. One, designated saccadic CM, was fast, had a definite latency, and always foIlowed conjugate errors. The other was slow, drift-like, without a latency, and corrected dysconjugate retjxations. We utilized the term giissadic CM for this latter variety. Saccadic corrective movements
The saccadic correction was distinctive, easily recognized, equal in both eyes, and followed all binocular (conjugate) errors. Its rapid acceleration resulted in a conspicuous CONJUGATE UNDERSHOOT
100 msec Fm. 1. R&rational ~~~~~p~t a~
saceade from primary position to target 20 deg to the fight. The fhst and position of left (LE) and right eye (RR), respectively. The gccond and demon&ate the d%arentiated peak vem. Roth eyea i%%&CQt by 2 &g and, after 125 msec, binocular conjugate saccam corre&?e movements align the eyes with the target.
Corrective Movements following Refixation Saccades
469
step-like deflection of the EOG baseline (Figs. 1 and 2). A 3-deg movement was accomplished in less than 25 msec. The latencies from the termination of the initial movement until the onset of the corrective movements were approximately 125 msec (124-5 f 10.5 S.D.). This latency was the same with saccadic corrections for undershoots (positive CMs) and overshoots (negative CMs). CONJUGATE
OVERSHOOT
Lt
4ooq set-1
RE
100 Era. 2.
Conjugate overshoot corrected by saccadic CM. 2.0
t
CONJUGATE
10 3.
ERRORS
30
20 TARGET
FIG.
mei
DISTANCE
/degrees)
Relationship of interfixationai distance to mean size of binocular (conjugate) error.
The size of saccadic CMs increased monotonically with interGxationa1 distance (Fig. 3). The mean sizes of positive CMs for IO, 20 and 30 deg interfixational distances were l-3, 1.6 and l-8 deg respectively. For negative CMs the respective sizes were 1.2, l-3 and 1.5 deg.
470
RONALDB. WEBER AND ROBERT B. DAROFF
Glissadic corrective movements
This type of correction was of low velocity (approximately 20 deg/sec) and inseparable from the terminal portion of the saccade (Figs. 4 and 5). There was therefore no latency between the end of the initial saccade and the beginning of the correction. As previously stated, glissadic CMs exclusively followed dysconjugate errors. The glissadic CM size-interfixational distance relationship approximated those of saccadic CMs (Fig. 6). DYSCONJUGATE
UNDERSHOOT
I
-I
100 msec FIG. 4. Sac&e
from 20 deg left to primary position. Right eye (RE) undershoots target by
approximately2 deg
followed by a glissadic corrective less than 1 deg.
30”
movement.The left eye overshoots by
I
LE 4oo” I set -1
3o”
I
RE
100 msec FIO .
5. Uniocuku overshoot of LE followed by glissadic CM.
Corrective Movements following Refixation Saccades
DYSCONJUGATE
2.0
471
ERRORS r*
Ho
*/ f ?1 F
3
0’ d
1.5
4’
9
,’
/ 4’ 4’
5 0
z
30
4’
.-.
OVERSHOOT
o---o
UNDERSHOOT
20
10 TARGET
FIG. 6.
DISTANCE
(degrees)
Relationship of interfixaGona1 distance to mean size of dysconjugate unlocuhr error.
Saccadicprecision-amplituderelationships The results of our present and previous (WEBERand DAROFF,1971) studies indicate the following relationships of ocular response to increasing interfixational distance: (1) The incidence of dysmetria increases. (2) The incidence of positive CMs (fol undershoots) increases. (3) The incidence of negative CMs (for overshoots) decreases. (4) The size of all CMs increases. DISCUSSION Refixation
saccades
bring peripherally placed objects into central vision by sliding the
fovea under the object image. If the image is not captured on the fovea with the initial refixation saccade, the remaining error is resolved by an involuntary corrective movement (CM). This correction, we have determined, is always saccadic when the error is binocularly equal (conjugate) and slow (glissadic) following uniocular (dysconjugate) errors. With the aid of magnification, we were able to measure trace amplitudes accurately to approximately O-25 mm (30 arc min). In our tabulations, we regarded only eyes : target and eye:eye errors of 1 deg or greater, followed by a CM, as dysmetric (WEBEXand DAROFF, 1971). Smaller errors, indistinguishable from pre-terminal fusional vergence movements, were classified as normometric. In our target display, the angle of convergence in primary position (3” 4’) was 46 min greater than at 30 deg. We considered the possibility that the movements ultimately designated “glissadic CM” merely represented asymmetrical vergence (ZUBEX,1967). This we deemed unlikely for the following reasons: (1) there was considerable inter- and intra-subject variability of dysconjugate saccades (WEBFJR and DAROFF, 1971), despite the fixed difference in convergence angle between targets; (2) the magnitude of the errors (l-3 deg) exceeded the change in vergence angle; (3) since the greatest angle of convergence is in primary position, centering saccades were always to a target requiring increased convergence angle and, indeed, the greatest incidence of overconvergence (due to adductor overshoot or abductor undershoot) occurred with center-directed saccades. The
472
RONALD B. WEBER AND
ROBERT B. DAKOFF
corrective movement in these circumstances was therefore dicergent. Although it may t-x argued that the vergence angle change between targets was somehow responsible for the occurrence of the dysconjugate saccades, it does not follow that the subsequent corrective movements were fusional ; (4) the frequency and magnitude of convergerlt saccades (followed by glissadic CMs) did not decrease (actuaIly increased) when the subject : target distance was extended from 44” to 69” (WEBERand DAROFF,1971); and (5) we determined (unpublished experiments) that subjects making refixations with one eye occluded demonstrated dys~onjugate saccades followed by glissadic CMs. These occurred in both the seeing and occluded eyes. The reaction times (latency) of voluntary refixation and corrective saccades differ markedly. Corrective saccades of any size have nearly constant latencies of approximately 125 msec. In an unpublished experiment, we instructed subjects to make retiation saccades between objects separated by 20 deg followed by a second refixation to another object 2 deg away. The latter movements were performed in both positive and negative directions. The mean reaction time before the second saccade was 369 msec for positive steps and 468 msec for negative movements. These results confirm those of LEUSHINA(1965) who reported an inverse relationship between reaction time and intertixational distances for retIxation saccades. These saccades presumably require time-consuming discrimination of visual info~ation, whereas the short latency corrective saccades occur inde~ndent of visual feedback. BECKERand FUCHS (1969) determined that for 40 deg refixations, most subjects fell short of the target with the initial saccade and required a positive corrective saccade which had a mean latency of 127 msec. These same subjects performed almost identical 2-step saccades in darkness where visual feedback information was unavailable. Becker and Fuchs postulated that these large (40 deg) fixation changes may be preprogrammed as a package consisting of two movements: an initial large saccade which undershoots the targets, followed by a smaller corrective saccade. The “pre-packaged” concept would account for the short latency of the second saccade. Our study of saccadic metrics at IO,20 and 30 deg demonstrated an inter- and intra-subject spectrum of undershoots, overshoots, dysconjugate, as well as normometric movements (WEBERand DAROFF,1971). This variability and inconsistency renders “pre-packaging” an unlikely explanation, in our opinion, for the corrective movements following dysmetric smaller amplitude refixation saccades. We repeated Becker and Fuchs’ study of saccades in darkness but utilized 10-30 deg distances. The same pattern of dysmetria and consequent CMs observed with visible targets also occurred in darkness. This provides further evidence against any possible rofe of visual feedback in the generation of CMs. Mechanisms other than visual feedback and “pre-packaging” are therefore necessary to account for saccadic CMs with refixarions less than 40 deg. An obvious alternative is feedback from stretch receptors in extraocular muscles (proprioceptive loop, Fig. 7). Experimental (VOSSIUS,1960; FUCHSand KORNHUBER,1969) and clinical (HIGGINSand DAROFF, 1966) studies support the significance of this loop. Despite the physiologic and cybernetic appeal of such a mechanism (Brzzr and EVAKW, 1971), the func~on~ importance of stretch receptor feedback from eye muscles remains unproved (FILLENZ, 1955; STARK, 1968; PEXRYAUNand BR~RNIN,1971). “Response feedback” (pxoprioceptive or visual} cannot explain the no-delay ghssadic corrective movement which follow dysconjugate dysmetria. A reasonable hypothesis for gtissadic CMs involves prenuclear feedback (Fig. 7). Actual output is monitored at the brain
473
Corrective Movements following Refutation Saccades
Fro. 7. Simplified diagram proposed for ocular motor control system. The bolder lines indicate those aspects of the schema relevant to our study. (PPRF refers to pontine paramedian reticular formation.)
stem level and, if incompatible with the desired output, a corrective movement is generated by the pontine paramedian reticular formation (PPRF).l In this instance, where no latency is discernible, the correction is continuous with the saccade. Only an internal monitor could detect asymmetric outflow and rectify the condition “in flight”. JOHNSON (1963) postulated the existence of a similar loop which he designated “oculomotor monitoring”. EVARTS(1971) recently reviewed in detail the importance of this type of internal feedback in the regulation of all voluntary movements. Internal feedback seems the best explanation for the glissadic CMs following dysconjugate refixation saccades. A similar mechanism could account for saccadic CMs as well, particularly if further studies fail to establish the functional significance of proprioceptive feedback from eye muscles. authors extend their appreciation to Dr. ALVAN R. FEINSTEINand Mrs. ELIZABETH the Eastern Research Support Center, West Haven (Connecticut) Veterans Administration Hospital, for computer programming and analysis; to Dr. Lours Dx~~‘Osso for advice and constructive
Acknowledgements-The C. WRIGHT of
criticism; to RICHARDNAMON, biophysicist, technical assistance.
who refined our instrumentation;
and to Mr. MEL JOHNSINfor
REFERENCES BECKER,W.
and Fucrrs, A. F. (1969). Further properties of the human saccadic system: Eye movements and
correction saccades with and without visual fixation points. Vison Res. 9, 1247-1258. BIZZI, E. and EVAR~S,E. V. (1971). Translational mechanisms between input and output. In Central Control of Movement (edited by E. V. EVAIUS, et al.), Neurosciences Res. Prog. BUN. 9,31-59. DAROPF,R. B. and HOYT, W. F. (1971). Supranuclear disorders of ocular control systems in man: Clinical, anatomical and physiological correlations, 1969. In l?re Control of Eye Movements (edited by P. BACHY-RITAand C. C. COLLINS).Academic Press, New York. DEARBORN,W. F. (1904). Retinal local signs. Psychol. Rev. 11,297-307. DODGE, R. (1907). An experimental study of visual fixation. Psycho/. Monogr. 8, l-95.
r The PPRF is the final prenuclear anatomical substrate horizontal eye movements (DAROFFand HOYT, 1971).
for the generation
of saccadic and pursuit
RONALDB.
474
WEB~RANDROBERTB. DAROFF
EVARTS,E. V. (1971). Feedback and corollary discharge: A merging of the concepts. In Central Confro( u Movement (edited by E. V. EVARXet al.), Neurosciences Res. Prog. BUN.9, 86-l 12. RLLENZ, M. (1955). Responses in brainstem of the cat to stretch of extrinsic ocular mucks. J. Physic& Land. 128, 182-199. FUCHS,A. F. and KORNHUBER, H. H. (1969). Extraocular afferents to the cerebellum of the cat. J. Physiol.,
Land* 250,713-722. I&GGINS,D. C. and DAROFF,R. B. (1966). Overshoot and osciflation in ocular dysmetria. Archs Opht~l. 79, 742-745. JOHNSON, L. E., JR. (1963). Human eye tracking of aperiodic target functions. 37-B-63-8, Systems Reseamh
Center, Case Institute of Technology, Cleveland, Ohio. LEUSHINA,L. I. (1965). On estimation of position of photo stimulus and eye movements. Biofizika 10, 130-136. MCALLISTER, C. N. (1905). The fixation points in the visual field. Psycbol. Monogr. 7, 17-53. ti, W. R. (1929). Horizontal eye movements at the onset of sleep. PsychoL Rev. ‘36, 122-141. STARK,L. (1968). Neurological Control Systems; Studies in Bioeq#neering, p. 233. Plenum Press, New York. Voors, R. H. (1969). Computerless automatic data reduction for electronystagmography. Aerospace Med. 40,108~1086.
Vossrus, G. (1960). Das System der Along. 2. Bioi. 112,27-57. WEZ?IZR, R. B. and DARO~, R. B. (1971). The metrics of horizontal saccadic eye movements in normal humans. Vision Res. 11,921-928. YOUNQ,L. R. (1963). Measuring eye movements. Am. J. Med. EZectronics4,3od307. ZVIIER,B. L. (1967). Asymmetrical fusional vergenw Eye movements maul&g from target movement along the visual axis of one eye. Presbyterian-St. Luke’s Hosp. Med. Bull. 6, 15-20.
Ah&aet-Rational sacu&es frequently do not achieve the intandsd ampfihtde with the. initial displaoemsnt; the errors am binocular saa~dic (high-v8locity) after a 125 msee latency. Slow, dr#t-Bk8 original SBccBde,correct dysconjugate errors. We discuss the possiile rokrp and visual, proprioc8ptive and internal pmnuel8ar fGedback in the g8naration of CM% We conclude that a prenucl8ar intemal monitor be& accounts for gBwadl8 CMa wk8reas saaxdic CMs may be explained by either proprioceptive fsedttack or an internal monitor.
R&tm&--Les saccades de re-fixation ant frequemment une amplitude qui n’est pas celle qui convient au d6placement initial; les erruers sent soit conjugu&s (&al8s pour les deux yeux) soit dysconjugu8es. Un mouvement de correction (CM) binocuh&e, sac4ad8 st rapide, suit la position conjugu88 error&r ap&s 125 resee de latence. Les errems dygcQq*b sent corrigees par des CM de doriveslentes qui contiauent la tin de la saccade original8 Qn discute les r8Ies possibles des feedbacks visuek, proprioceptifa et pr6nucl&ires internes, darts ia g&&ration des CM. On conclut que les derives s’expliquent au mieux par un r8glage p&u&aire inteme,tandis que IesCMsaccad~ s’expliquent soit par un f~~~kprop~o~pt~,soit par un r&dage inteme.
intemen Monitor erklart werden kbnnen.
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following Re6xation
Saccades
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475