A Review of Basic Research and Clinical Studies
*Brain Research Unit
Institute of Biophysics
University of Freiburg
**Medical Research Council Group in Sensory-Motor Physiology
Department of Physiology
Queen's University, Kingston
Ontario K7L 3N6, Canada
Lesions in different brain structures and special diseases may - in addition to other symptoms - also result in deficits in eye movement control. Therefore the analysis of eye movements has been used - mostly in neurology and psychiatry - as an extra diagnostic tool. While optokinetic and vestibular nystagmus are widely in use, saccades have been used only recently. In particular, the question came up whether saccades could be made to locations that were not defined directly by visual stimuli but rather by certain instructions, by memory, or by previous experience. Under normal viewing conditions both reflexive and voluntary saccades are directed to a visual stimulus, i. e. the direction of both eye movement components are the same. One possibility to dissociate these components is to present a visual stimulus at one side and to ask the subject to make a saccade to the opposite side. This task has been originally introduced by Hallett in 1978 and is called the antisaccade task or - more briefly - the antitask. It requires that the subject successfully suppresss the reflex (for example by effective fixation) and the ability to generate a saccade to a position with no stimulus.
When using the antitask the first observation is that normal subjects can generally follow the instruction. The second observation is, however, that they make a certain number of erratic saccades to the stimulus. The analysis of these errors shows that many of them occur after extremely short reaction times in the order of 100 ms representing the mode of express saccades. Therefore, anti and express saccades are generated under the same condition in one session by the same subject in different numbers. Third, subjects do not correct all of their reflexive saccades. Finally, a great percentage of the reflexive saccades and their corrections remain unconscious.
The antitask has been used in basic research as well as in clinical studies and in the analysis of deficits related to circumscribed brain lesions. The express saccade (Fischer, Boch, 1983); (Fischer, Ramsperger, 1984)has been used to study basic aspects of fixation and attention control on the saccade system in normal adult subjects and in dyslexic subjects as well as in psychiatric patients.
This article summarizes the results of the studies on antisaccades since 1978 and discusses the neural mechanisms (tectal, frontal, parietal) underlying the control of antisaccade generation.
The fact that fixation can be maintained and saccades can be directed in a meaningful way despite large numbers of irrelevant visual events in the near and far periphery of the field of view is very important for many visual functions in everyday life. If a deficit occurs in the coordination between visual perception and eye movement generation a subject may be more or less severely impaired in certain functions.
On the other hand, lesions in different brain structures and special diseases may - in addition to other symptoms - also result in deficits in eye movement control. Therefore the analysis of eye movements has been used - mostly in neurology and psychiatry - as an extra diagnostic tool. While optokinetic and vestibular nystagmus are widely accepted and used in relation to cerebellar and brain stem disorders, the analysis of saccades is not established.
During the last 10 years after the neurophysiology and anatomy of the visual and oculomotor system had developed quite fast the investigation of saccades became more relevant. In particular the question came up whether saccades could be made to locations that were not defined directly by visual stimuli but rather by certain instructions, by memory, or by previous experience. One most easy way of setting the conditions for such a saccade is to present a visual stimulus at one side and to ask the subject to make a quick eye movement to the opposite side. This task has been originally introduced by Peter Hallett in 1978 as a "novel task" and is now called the antisaccade task or - more briefly - the antitask (Hallett, 1978); (Hallett, Adams, 1980).
The first important observation using the antitask is that subject can follow the instruction. The second observation is that they do make a small number of erratic prosaccades to the stimulus. The analysis of these errors shows that a proportion them occurs after extremely short reaction times in the order of 100 ms representing the mode of express saccades. Longer latency errors occur also as fast regular saccades. Therefore anti and express saccades are generated under the same condition in one session by the same subject in different numbers.
The antitask has been used in basic research as well as in clinical studies and in the analysis of deficits related to circumscribed brain lesions (Guitton et al. 1982); (Guitton et al. 1985). The express saccade has been used to study the basic aspects of fixation and attention control in saccade generation in normal adult subjects and in dyslexic subjects. Recently, one has also trained monkeys to perform the antitask (Funahashi et al. 1993); (Amador et al. 1995).
This article attempts to summarize the results of the studies on antisaccades in man and monkey, provides the reader with a quick look-up on what has been gained since 1978, and outlines the neural mechanisms (tectal, frontal, parietal structures) presumably underlying the control of voluntary saccades.
- the subjects were able to successfully look to the side opposite to the stimulus.
- in the beginning, however, they made quite a number of erratic saccades (30 - 80 %) toward the stimulus before they looked to the opposite side. Later they could reduce the error rate down to 5 - 7%.
- the mean reaction times of the antisaccades were prolonged as compared to prosaccades.
- antisaccade amplitude was quite variable both from subject to subject and within a subject.
- antisaccade velocity profiles were altered.
- secondary saccades followed primary antisaccades much faster than primary prosaccades.
The longer latencies of antisaccades versus prosaccades were confirmed and it was stated that there was no significant improvement with practice (Hallett, Adams, 1980). This results were later refined: when subjects were required to make antisaccades in a gap task they decreased both their error rate from an average of about 14 % to 11 % and their average latency from about 183 ms to 171 ms within 12 to 15 days of everyday practice (Fischer, Weber, 1992).
Characteristic parameters of the antisaccade: As for normal saccades the basic parameters of antisaccade are: latency, duration, velocity, size and accuracy, correction time in case of saccades undershooting or overshooting the required final position of the eye. In addition and specific for the antitask is the percent number of erratic prosaccades that are made against the subjects will inone or the other direction and the corresponding correction time. The latencies of the antisaccades depend on retinal factors like state of adaptation and rod-cone interaction. (Doma, Hallett, 1988) examined the influence of different luminance conditions on pro- and antisaccades. Photopic stimulus luminances led to longer latencies, larger angular error, less secondary saccades and more direction error in antisaccades compared with prosaccades. In scotopic stimulus luminances most differences between pro- and antisaccades disappeared. This was caused mainly by increased latencies, increased standard deviations of the angular errors and a decrease of the incidence of secondary saccades in prosaccades. Moreover, scotopic stimulus luminances increased the direction errors for prosaccades and antisaccades. For mesopic stimulus luminances, prosaccades showed a linear segment in the log latency-log luminance function which intersected at the peripheral cone threshold. In contrast, antisaccades showed a latency plateau which extended 0.7-1.0 log unit above foveal treshold. Moreover, antisaccades showed increased direction errors in this range. Additionally, antisaccadic latencies are variable for mesopic cues (Doma, Hallett, 1989). The peak velocity of antisaccades is decreased compared with prosaccades (345 deg/sec versus 512 deg/sec) and skewness of the velocity profile occurs more frequently for antisaccades than for prosaccades (Smit et al. 1987).
The role of the physical parameters on the performance of the antitask has been studied recently (Fischer and Weber, 1996 submitted). When a gap was used its duration was critical for the number of erratic prosaccades and for the latency of the correct antisaccades. For gap durations of 200-250 ms the mean error rate was maximal (15 %) and the latency minimal (175 ms) as compared with shorter and longer gap durations. The error rate increased and the latency decreased with increasing eccentricity of the stimulus from 1 deg to 12 deg. Stimulus size, on the other hand, had little or no effect.
Randomly interleaving of pro- and antitrials in a single block was of no importance when compared with blocks of only pro- or only anticommands (Hallett, Adams, 1980). These experiments were repeated using visual cues to indicate whether pro- or antisaccades were required at any given trial. It turned out that subjects made large numbers of errors eventhough the cue was given 100-200 ms ahead of time. The errors were of both kinds: erratic prosaccades on antitrials and - more surprisingly - erratic antisaccades on protrials. The analysis revealed that the subjects on many trials executed the command of the previous trial (Weber, 1995). This result clearly indicates that the generation of voluntary saccades even when they are prosaccades relies on non-visual functions, presumably of the frontal cortical system.
When provided with valid visual cues indicating correctly the side to which the antisaccade must be made 100 ms ahead of time trial by trial normal subjects produce more errors than without the cues (Fischer, Weber, 1996). The subjects reported that they were unable to suppress the unwanted prosaccades and moreover it turned out that on average 50% of the trials with erratic prosaccades escaped their conscious recognition (Fischer and Mokler, unpublished observation). Interestingly, almost all the erratic prosaccades were corrected immediately indicating that the subjects could generate antisaccades on every trial.
By contrast, subjects (mostly children), who also produce high error rates without the cues often do not correct their errors. They have difficulties generating saccades to the side opposite to the stimulus. They are really impaired on the antisaccade task not because a lack of fixation activity but because a lack of generating voluntary saccades. An impairment to generate an antisaccade after the execution of an erractic prosaccade has also been reported for patients with frontal lesions (Guitton et al. 1985).
Therefore, when high error rates are observed in the antisaccade task, it is important to see in addition whether a subject corrects them or not. This differentiation between the components of a successful performance of the antitask has been discussed in detail in the context of the significance and interpretation of the error frequency of schizophrenics and other patients (Huerta et al. 1987);(Levy, 1996).
Little is known about the correction time of the erratic prosaccades. If, in a protask a saccade fails to reach to the target at once by over- or undershooting it a corrective saccade occur not earlier than 130 to 150 ms afetr the end of the primary saccade. Extremely short correction times are observed only when the primary saccade is made in the wrong direction thus sleaving a large retinal error. These corrective saccade can be of the express type being triggered by the onset of the target stimulus not by the end of the primary saccade (Fischer et al. 1993). The erratic prosaccade produced in the antitask also leave a large error (by definition). Yet, only small proportion of them is corrected faster than 80 ms from the end of the erratic saccade. But with a mode around 100 ms the correction times are certainly faster than those following under- or overshoots in a protask (Mokler, in preparation).
On the other hand, the data obtained from the protask did not show much of developmental changes: the reaction times decreased from 210 to 180 ms and the percent number of express saccades decreased from about 15% to just below 10%. Comparing the data from the pro- and antitasks revealed that subjects with only a few express saccades and high error rates also failed to correct their errors on many trials indicating that they had difficulties in generating saccades to the side opposite to the stimulus (Fischer et al., submitted).
These results suggest that the fixation system preventing express saccades in the protask is pretty much developed at age 10 while the voluntary component of saccade generation develops over a much longer period. In fact, it has been reported that infants as young as 4 months can learn to inhibit automatic saccades to salient stimuli indicating the effectiveness of their fixation system (Johnson, 1995). Elderly memory-impaired people performed the antitask about as well as normal subjects of the same age exhibiting an error rate in the order of 30 - 40 % using a no-gap condition. The mean latency was almost 400 ms for both groups (Versino et al. 1993).
AMADOR N, SCHLAG-REY M, SCHLAG J, SANCHEZ H (1995) Supplementary eye field neuronal activity during monkey performance of antisaccade tasks. Society for Neuroscience Abstracts, 21, 1195, No.469.6(Abstract)
ANDERSON TJ, JENKINS IH, BROOKS DJ, HAWKEN MB, FRACKOWIAK RS, KENNARD C (1994) Cortical control of saccades and fixation in man. A PET study. Brain, 117, 1073-1084.
BECKER W, IWASE K, JÙRGENS R, KORNHUBER HH (1976) Bereitschaftspotential preceding voluntary slow and rapid hand movements. In: The Responsive Brain. Edited by WC McCallum, JR Knott. Bristol: Wright. 99-102.
BECKER W (1989) Metrics. In: The Neurobiology of Saccadic Eye Movements. Edited by RH Wurtz, ME Goldberg. Amsterdam: Elsevier. 13-67.
BISCALDI M, FISCHER B, AIPLE F (1994) Saccadic eye movements of dyslexic and normal reading children. Perception, 23, 45-64.
BISCALDI M, STUHR V, DÒRFLINGER K (1995) The performance of dyslexic and normally reading subjects in the antisaccade task. Perception, 24 Supplement, 27
BISCALDI M, FISCHER B, STUHR V (1996) Human express-saccade makers are impaired at suppressing visually-evoked saccades. J Neurophysiol, 76, 199
BISCALDI M, FISCHER B (1994) Saccadic eye movements of dyslexics in non-cognitive tasks. In: Eye Movements in Reading. Edited by Jan Ygge, Gunnar Lennerstrand. Pergamon. 245-259.
BRICKETT PA, WEINBERG H, DAVIS CM (1984) Cerebral potentials preceding visually triggered saccades. Ann N Y Acad Sci, 425, 429-433.
CAVEGN D, BISCALDI M (1996) Fixation and saccade control in an express-saccade maker. Exp Brain Res, 109, 101-116.
CLEMENTZ BA, SWEENEY JA, HIRT M, HAAS G (1990) Pursuit gain and saccadic intrusions in first-degree relatives of probands with schizophrenia. Journal of Abnormal Psychology, 99, 327-335.
CLEMENTZ BA, GROVE WM, IACONO WG, SWEENEY JA (1992) Smooth-pursuit eye movement dysfunction and liability for schizophrenia: Implications for genetic modeling. Journal of Abnormal Psychology, 101, 117-129.
CLEMENTZ BA, MCDOWELL JE, ZISOOK S (1994) Saccadic system functioning among schizophrenia patients and their first-degree biological relatives. Journal of Abnormal Psychology, 103, 277-287.
CRAWFORD TJ, HAEGER B, KENNARD C, REVELEY MA, HENDERSON L (1995) Saccadic abnormalities in psychotic patients. I. Neuroleptic-free psychotic patients. Psychological Medicine, 25, 461-471.
CURRIE J, BENSON E, RAMSDEN B, PERDICES M, COOPER D (1988) Eye movement abnormalities as a predictor of the acquired immunodeficiency syndrome dementia complex. Arch Neurol, 45, 949-953.
CURRIE J, RAMSDEN B, MCARTHUR C, MARUFF P (1991) Validation of a clinical antisaccadic eye movement test in the assessment of dementia. Archives of Neurology, 48, 644-648.
DOMA H, HALLETT PE (1988) Dependence of saccadic eye-movements on stimulus luminance, and an effect of task. Vision Research, 28, 915-924.
DOMA H, HALLETT PE (1989) Variable contributions of rods and cones to saccadic eye-movement latency in a non-foveating task. Vision Research, 29, 563-577.
EVDOKIMIDIS I, LIAKOPOULOS D, CONSTANTINIDIS TS, PAPAGEORGIOU C (1996) Cortical Potentials with antisaccades. Electroenceph.Clin.Neurophysiol. 98, 377-384.
FISCHER B, WEBER H, BISCALDI M (1993) The time of secondary saccades to primary targets. Experimental Brain Research, 97, 356-360.
FISCHER B, GEZECK S, HUBER W (1995) The three-loop-model: A neural network for the generation of saccadic reaction times. Biological Cybernetics, 72, 185-196.
FISCHER B, BOCH R (1983) Saccadic eye movements after extremely short reaction times in the monkey. Brain Research, 260, 21-26.
FISCHER B, RAMSPERGER E (1984) Human express saccades: extremely short reaction times of goal directed eye movements. Experimental Brain Research, 57, 191-195.
FISCHER B, WEBER H (1992) Characteristics of "anti" saccades in man. Experimental Brain Research, 89, 415-424.
FISCHER B, WEBER H (1993) Express Saccades and Visual Attention. Behav.& Brain Sciences, 16,3, 553-567.
FISCHER B, WEBER H (1996) Research note: effects of procues on error rate and reaction times of antisaccades in human subjects. Exp Brain Res, 109, 507-512.
FISCHER B, WEBER H (1997) Effects of precues on voluntary and reflexive saccade generation (I) Anticues for pro-saccades. (Abstract)
FLECHTNER WA, SHARPE JA (1986) Saccadic eye movement dysfunction in Alzheimer's disease. Ann Neurol, 10, 464-471.
FOX PT, FOX JM, RAICHLE ME, BURDE RM (1985) The role of cerebral cortex in the generation of voluntary saccades: a positron emission tomographic study. J-Neurophysiol, 54, 348-369.
FUKUSHIMA J, FUKUSHIMA K, CHIBA T, TANAKA S, YAMASHITA I, KATO M (1988) Disturbances of voluntary control of saccadic eye movements in schizophrenic patients. Biol Psychiatry, 23, 670-677.
FUKUSHIMA J, FUKUSHIMA K, MORITA N, YAMASHITA I (1990a) Disturbances in the control of saccadic eye movement and eye-head coordination in schizophrenics. Journal of Vestibular Research, 1, 171-180.
FUKUSHIMA J, FUKUSHIMA K, MORITA N, YAMASHITA I (1990b) Further analysis of the control of voluntary saccadic eye movements in schizophrenic patients. Biological Psychiatry, 28, 943-958.
FUKUSHIMA J, MORITA N, FUKUSHIMA K, CHIBA T, TANAKA S, YAMASHITA I (1990c) Voluntary control of saccadic eye movements in patients with schizophrenic and affective disorders. Journal of Psychiatric Research, 24, 9-24.
FUKUSHIMA J, FUKUSHIMA K, MIYASAKA K, YAMASHITA I (1994) Voluntary control of saccadic eye movement in patients with frontal cortical lesions and parkinsonian patients in comparison with that in schizophrenics. Biological Psychiatry, 36, 21-30.
FUNAHASHI S, CHAFEE MV, GOLDMAN RAKIC PS (1993) Prefrontal neuronal activity in rhesus monkeys performing a delayed anti-saccade task. Nature, 365, 753-756.
FUSTER JM (1991) The prefrontal cortex: anatomy, physiology, and neurophysiology of the frontal lobe. New York: Raven Press.
GAYMARD B, PIERROT-DESEILLIGNY C, RIVAUD S (1990) Impairment of sequences of memory-guided saccades after supplementary motor area lesions. Annals of Neurology, 28, 622-626.
GERFEN CR (1994) Relations between cortical and basal ganglia compartments. In: Motor and cognitive functions of the prefrontal cortex. Edited by AM Thierry, M Tovee, M Verin, L Wilkinson. Berlin: Springer. 789-793.
GEZECK S, FISCHER B, TIMMER J (1997) Saccadic Reaction Times: A Statistical Analysis of Multimodal Distributions. Vision Research,
GOLDBERG ME, SEGRAVES MA (1989) The Visual and Frontal Cortices. *BK # 92860, 3, 283-313.
GROVE WM, LEBOW BS, CLEMENTZ BA, CERRI A, ET (1991) Familial prevalence and coaggregation of schizotypy indicators: A multitrait family study. Journal of Abnormal Psychology, 100, 115-121.
GUITTON D, BUCHTEL HA, DOUGLAS RM (1982) Disturbances of voluntary saccadic eye movement mechanisms following discrete unilateral frontal lobe removals. In: Functional Basis of Ocular Motility Disorders. Edited by G Lennerstrand, DS Zee, EL Keller. Oxford: Pergamon Press. 497-500.
GUITTON D, BUCHTEL HA, DOUGLAS RM (1985) Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades. Experimental Brain Research, 58, 455-472.
GUITTON D (1992) Control of eye-head coordination during orienting gaze shifts. Trends Neurosci. 15, 174-179.
HALLETT P (1978) Primary and secondary saccades to goals defined by instructions. Vision Research, 18, 1279-1296.
HALLETT PE, ADAMS BD (1980) The predictability of saccadic latency in a novel voluntary oculomotor task. Vision Research, 20, 329-339.
HIKOSAKA O, SAKAMOTO M, MIYASHITA N (1993) Effects of caudate nucleus stimulation on substantia nigra cell activity in monkey. Experimental Brain Research, 95, 457-472.
HIKOSAKA O, WURTZ RH (1980) Discharge of substantia nigra neurons decreases before visually-guided saccades. Neurosci.Abstr. 6 Nr. 9.6, 15
HIKOSAKA O, WURTZ RH (1983) Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. J-Neurophysiol, 49, 1285-1301.
HOLZMAN PS, KRINGLEN E, MATTHYSSE S, FLANAGAN SD, ET (1988) A singledominant gene can account for eye tracking dysfunctions and schizophrenia in offspring of discordant twins. Archives of General Psychiatry, 45, 641-647.
HOLZMAN PS, MATTHYSSE S (1990) The genetics of schizophrenia: A review. Psychological Science, 1, 279-286.
HUERTA MF, KRUBITZER LA, KAAS JH (1987) Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys. II. Cortical connections. J comp Neurol, 265, 332-361.
JOHNSON MH (1995) The inhibition of automatic saccades in early infancy. Developmental Psychobiology, 28, 281-291.
JOHNSTON JL, MILLER JD, NATH A (1996) Ocular motor dysfunction in HIV-1-infected subjects- a quantitative oculographic analysis. Neurology, 46, 451-457.
KITAGAWA M, FUKUSHIMA J, TASHIRO K (1994) Relationship between antisaccades and the clinical symptoms in Parkinson's disease [published erratum appears in Neurology 1995 Apr;45(4):852]. Neurology, 44, 2285-2289.
KOPECZ K, SCHONER G (1995) Saccadic motor planning by integrating visual information and pre-information on neural dynamic fields. Biological Cybernetics, 73, 49-60.
KOPECZ K (1996) Saccadic Reaction Times in Gap/Overlap Paradigms: A Model Based on Intgration of Intentional and Visual Information on Neural, Dynamic Fields. Vision Research, 35(20), 2911-2925.
LASKER AG, ZEE DS, HAIN TC, FOLSTEIN SE, SINGER HS (1987) Saccades in Huntington's disease: initiation defects and distractibility. Neurology, 37, 364-370.
LEIGH JR, NEWMAN SA, FOLSTEIN SE, LASKER AG, JENSEN BA (1983) Abnormal ocular motor control in Huntington's disease. Neurology, 33, 1268-1275.
LEVY DL (1996) Location, location, location: The pathway from behavior to brain locus in schizophrenia. In: Psychopathology: The Evolving Science of Mental Disorder. Edited by SW Matthysse, DL Levy. Cambridge: Cambridge University Press. 100-126.
LUECK CJ, TANYERI S, CRAWFORD TJ, HENDERSON L, KENNARD C (1990) Antisaccades and remembered saccades in Parkinson's disease. Journal of Neurology, Neurosurgery & Psychiatry, 53, 284-288.
MARUFF P, HAY D, MALONE V, CURRIE J (1995) Asymmetries in the covert orienting of visual spatial attention in schizophrenia. Neuropsychologia, 33, 1205-1223.
MATSUE Y, OSAKABE K, SAITO H, GOTO Y, UENO T, MATSUOKA H, et al (1994a) Smooth pursuit eye movements and express saccades in schizophrenic patients. Schizophrenia Research, 12, 121-130.
MATSUE Y, SAITO H, OSAKABE K, AWATA S, UENO T, MATSUOKA H, et al (1994b) Smooth pursuit eye movements and voluntary control of saccades in the antisaccade task in schizophrenic patients. Japanese Journal of Psychiatry & Neurology, 48, 13-22.
MELAMED E, LARSEN B (1979) Cortical activation pattern during saccadic eye movement in humans: localization byy focal cerebral blood flow increases. Annals of Neurology, 5, 79-88.
MERRILL PT, PAIGE GD, ABRAMS RA, JACOBY RG, CLIFFORD DB (1991) Ocular motor abnormalities in human immunodeficiency virus infection. Ann Neurol, 30, 130-138.
MILNER B, PETRIDES M (1996) Behavioural effects of frontal-lobe lesions in man. Trends in Neurosciences, 11, 403-407.
MUNOZ DP, WURTZ RH (1992) Role of the rostral superior colliculus in active visual fixation and execution of express saccades. J-Neurophysiol, 67, 1000-1002.
MURI RM, HESS CW, MEIENBERG O (1991) Transcranial stimulation of the human frontal eye field by magnetic pulses. Experimental Brain Research, 86, 219-223.
NAKAYAMA K, MACKEBEN M (1989) Sustained and transient components of focal visual attention. Vision Research, 29, 1631-1647.
NOZAWA G, REUTER-LORENZ PA, HUGHES HC (1994) Parallel and serial processes in the human oculomotor system: bimodal integration and express saccades. Biological Cybernetics, 72, 19-34.
O'DRISCOLL GA, ALPERT NM, MATTHYSSE SW, LEVY DL, RAUCH SL, HOLZMAN PS (1995) Functional neuroanatomy of antisaccade eye movements investigated with positron emission tomography. Proceedings of the National Academy of Sciences of the United States of America, 92, 925-929.
OLSON RK, CONNERS FC, RACK JP (1991) Eye movements in dyslexic and normal readers. In: Vision and Visual Dysfunction, Vol 13, Vision and Vision Dyslexia. Edited by JF Stein. London: Macmillan. 243-250.
OPTICAN LM (1995) A Field Theory of Saccade Generation: Temporal-to-spatial Transform in the Superior Colliculus. Vision Research, 35, 3313-3320.
PAUS T, PETRIDES M, EVANS AC, MEYER E (1993) Role of the Human Anterior CingulateCortex in the Control of Oculomotor, Manual, and Speech Responses: A Positron Emission Tomography Study. J Neurophysiol, 70, 453-469.
PAUS T (1996) Review: Location and function of the human frontal eyefield: A selective review. Neuropsych. 34, 475-483.
PAVLIDIS GT (1981) Do eye movements hold the key to dyslexia? Neuropsychologia, 19, 57-64.
PETIT L, TZOURIO N, ORSSAUD C, PIETRZYK U, BERTHOZ A, MAZOYER B (1995) Functional neuroanatomy of the human visual fixation system. European Journal of Neuroscience, 7, 169-174.
PIERROT-DESEILLIGNY C (1989) Controle cortical des saccades. Rev Neurol (Paris), 145, 596-604.
PIERROT-DESEILLIGNY C, ROSA A, MASMOUDI K, RIVAUD S, GAYMARD B (1991) Saccade deficits after a unilateral lesion affecting the superior colliculus. Journal of Neurology, Neurosurgery & Psychiatry, 54, 1106-1109.
PIERROT-DESEILLIGNY C (1994) Saccade and smooth pursuit impairment after cerebral hemispheric lesions. European Neurologie, 34, 121-134.
PILLON B, BLIN J, VIDAILHET M, DEWEER B, SIRIGU A, DUBOIS B, et al (1995) The neuropsychological pattern of corticobasal degeneration: comparison with progressive supranuclear palsy and Alzheimer's disease. Neurology, 45, 1477-1483.
REUTER-LORENZ P, OONK H, BARNES L, HUGHES H (1995) Effects of warning signals and fixation point offsets on the latencies of pro- versus antisaccades: implications for an interpretation of the gap effect. Experimental Brain Research, 103, 287-293.
RIVAUD S, MURI RM, GAYMARD B, VERMERSCH AI, PIERROT-DESEILLIGNY C (1994) Eye movement disorders after frontal eye field lesions in humans. Experimental Brain Research, 102, 110-120.
ROSSE RB, SCHWARTZ BL, KIM SY, DEUTSCH SI (1993) Correlation between antisaccade and Wisconsin Card Sorting Test performance in schizophrenia. Am J Psychiatry, 150, 333-335.
ROSSE RB, MCCARTHY MF, ALIM TN, DEUTSCH SI (1994) Saccadic distractibility in cocaine dependent patients: a preliminary laboratory exploration of the cocaine-OCD hypothesis. Drug & Alcohol Dependence, 35, 25-30.
ROTHLIND JC, BRANDT J, ZEE D, CODORI AM, FOLSTEIN S (1993) Unimpaired verbalmemory and oculomotor control in asymptomatic adults with the genetic marker for Huntington's disease. Arch Neurol, 50, 799-802.
ROTHLIND JC, POSNER MI, SCHAUGHENCY EA (1995) lateralized control of eye movements in attention deficit hyperactivity disorders. J Cognitive Neurosci, 3,
ROY-BYRNE P, RADANT A, WINGERSON D, COWLEY DS (1995) Human oculomotor function: reliability and diurnal variation. Biological Psychiatry, 38, 92-97.
SCHLENKER R, COHEN R (1995) Smooth-pursuit eye-movement dysfunction and motor control in schizophrenia: a follow-up study. European Archives of Psychiatry & Clinical Neuroscience, 245, 125-126.
SELEMON LD, GOLDMAN-RAKIC PS (1988) Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior. J-Neurosci, 8, 4049-4068.
SERENO AB, HOLZMAN PS (1995) Antisaccades and Smooth Pursuit Eye Movements in Schizophrenia
. Society of Biol Psychiatry, 37, 394-401.
SERENO AB, HOLZMAN PS (1993) Express Saccades and Smooth Pursuit Eye Movement Function in Schizophrenic, Affective Disorder, and Normal Subjects. J Cognitive Neuroscience, 5(3), 303-316.
SHAUNAK S, ORRELL RW, O'SULLIVAN E, HAWKEN MB, LANE RJ, HENDERSON L, et al (1995) Oculomotor function in lateral sclerosis: evidence for frontal impairment. Ann-Neurol, 38, 38-44.
SMIT AC, VAN GISBERGEN JA, COOLS AR (1987) A parametric analysis of human saccades in different experimental paradigms. Vision Research, 27, 1745-1762.
SPARKS DL, BARTON EJ (1993) Neural control of saccadic eye movements. Curr Opin Neurobiol, 3, 966-972.
SWEENEY JA, MINTUN MA, KWEE S, WISEMAN MB, BROWN DL, ROSENBERG DR, et al (1996) Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. Journal of Neurophysiology, 75, 454-468.
THAKER G, KIRKPATRICK B, BUCHANAN RW, ELLSBERRY R, LAHTI A, TAMMINGA C (1989) Oculomotor abnormalities and their clinical correlates in schizophrenia. Psychopharmacology Bulletin, 25, 491-497.
THAKER GK, CASSADY S, ADAMI H, MORAN M, ROSS DE (1996) Eye movements in spectrum personality disorders: comparison of community subjects and relatives of schizophrenic patients. American Journal of Psychiatry, 153, 362-368.
TIEN AY, PEARLSON GD, MACHLIN SR, BYLSMA FW, HOEHN-SARIC R (1992) Oculomotor performance in obsessive-compulsive disorder. American Journal of Psychiatry, 149, 641-646.
VERMESCH AI, MÙRI RM, RIVAUD S, VIDAILHET M, GAYMARD B, AGID Y, et al (1996) Saccade disturbances after bilateral lentiform nucleus lesions in humans. Journal of Neurology,Neurosurgery,and Psychiatry, 60, 179-184.
VERSINO M, ROMANI A, BELTRAMI G, COSI V (1993) Saccadic and smooth pursuit eye movements in memory-impaired elderly. Acta Neurologica Scandinavica, 1, 39-43.
VIDAILHET M, RIVAUD S, GOUIDER-KHOUJA N, PILLON B, BONNET AM, GAYMARD B, et al (1994) Eye movements in parkinsonian syndromes [see comments]. Annals of Neurology, 35, 420-426.
WEBER H, AIPLE F, FISCHER B, LATANOV A (1992) Dead zone for express saccades. Experimental Brain Research, 89, 214-222.
WEBER H (1995) Presaccadic processes in the generation of pro and anti saccades in human subjects - a reaction time study. Perception, 24, 1265-1280.
WEBER H, FISCHER B (1995) Gap duration and location of attention focus modulate the occurrence of left/right asymmetries in the saccadic reaction times of human subjects. Vision Research, 35, 987-998.
WEBER H, FISCHER B (1996) Effects of procues on the execution of antisaccades. Neuroforum Supplement, 1, 194(Abstract)
WEINBERGER DR, BERMAN KF, DANIEL DG (1991) Prefrontal cortex dysfunction in schizophrenia. In: Frontal lobe function and dysfunction. Edited by HS Levin, HM Eisenberg, AL Benton. New York: Oxford University Press. 275-287.