Journal ofNeurology, Neurosurgery, and Psychiatry, 1978, 41, 1024-1030

Disturbances of ocular movements andblinking in schizophreniaJANICE R. STEVENS

From the Departments of Neurology and Psychiatry, University of Oregon Health Sciences Center,Portland, Oregon, USA

S U MM A R Y Neurological examination and electroencephalograms and electro-oculograms,recorded by telemetry, from unmedicated patients with acute and chronic schizophreniademonstrate a number of abnormalities of extraocular movement including staring, abnormaiblink rate, absent glabellar reflex, and increase in horizontal eye movements. As potential cluesto the pathophysiology of schizophrenia, these disturbances are analysed in relation toanatomical substrate and dopamine modulation of ocular movement, rapid eye movementsleep, and the neurological disorders in which similar disturbances of ocular movement occur.

In distinguishing dementia praecox from otherforms of mental illness, Kraepelin (1913) calledattention to a number of ocular signs of the dis-order, including pupillary abnormalities, staring,nystagmus, abnormal blinking, and blepharospasm.Widespread use of neuroleptic medications hasnow induced a variety of neurological side effectsand sequelae which obscure the incidence of thesesigns and their relevance to the pathology of theschizophrenias. Because these ocular signs mayprovide clues to the pathology of the schizophreniasyndrome, it seemed worth while to documentthem carefully in medication-free patients.

Subjects and methods

Complete neurological examinations have beenperformed on 45 patients who were free frommedication for periods of one month to four years,and 10 patients who had never received drugs orother physical treatment. Nine patients were seenwithin a year of diagnosis, 14 had been diagnosedbetween one and five years, and the remaining 29patients, longer than five years. The youngestpatient was 17 years of age, the oldest, 49 years.Thirty-one were men, 24 were women.The diagnosis was made by senior staff con-

sensus and required the following five of the sevencriteria stipulated by Taylor and Abrams (1975):illness duration greater than six monrths; clearSupported by National Institutes of Health Grant 18055.Address for reprint requests: Department of Psychiatry, University ofOregon Health Sciences Center, Portland, Oregon 97201, USA.Accepted 23 June 1978

consciousness; delusions, hallucinations, or formalthought disorder; restricted affect; absence of signsand symptoms sufficient to make a diagnosis ofaffective illness or coarse brain disease. In ad-dition to the neurological examination, 36 of the55 medication-free patients and 12 normal controlsubjects have had 2-24 hour electroencephalo-grams (EEG) and electro-oculograms (EOG)recorded by radiotelemetry during which spontane-ous behaviour was recorded continuously by atrained observer. Bipolar EEGs were recordedfrom tin or gold disc electrodes attached to thescalp with collodion at central-parietal (C3-P3;C4-P4) and temporal (T3-T5; T4-T6) positionsbilaterally. Lateral eye movement was recordedbetween electrodes placed at the outer canthus ofeach eye. Vertical movements and blinks wererecorded between electrodes placed immediatelyabove and below one eye. Subjects wore a smallmultiplexed 8-channel transmitter (weight 90 g,Benton Instrument Company) held firmly to thehead by a special cap.During the recording period, patients were in

their rooms or the dayroom within a radius of 40-50 yards of the receiver antenna. They slept in theirown beds, and carried on their usual hospitalroutine. Electroencephalographic and EOG signalswere recorded on a 7-channel FM tape recordermonitored by an ink-writing polygraph. Receivingand recording devices were centrally placed in ahallway near the ward dayroom. The polygraphwas run at a speed of 15 mm per second andcould be correlated continuously with ongoingbehaviour and accelerated to 30 mm per second for

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more detailed examination during periods ofunusual behaviour. Frequency modulated tape wasrecorded at 17 inches per second, and portions ofthe taped record were played back during be-havioural events of particular interest and forsubsequent analysis. Behavioural observationswere recorded by a trained observer on a writtenlog and were coded by number at the moment ofoccurrence on a time code placed on one channelof the tape recorder and polygraph, assuring exactcorrelation between EEG-EOG recording andbehavioural events.

Results

Neurological examination of this group of patientsdemonstrated that, apart from the characteristicabnormalities of mental state and skeletal motoractivity (stereotyped behaviours, rocking, bizarrepostures), the most common signs were dis-turbances of ocular contact and movement. Theseincluded staring, abnormal blinking, saccades, andocular pursuit. Prolonged telemetered EEG-EOGconfirmed the clinical evidence of abnormal ocularmovements. Although slow or sharp activity ap-

peared over the left or right temporal region ofone-third of these patients, these abnormalitiescould not be associated with the clinical changesnor with the appearance of abnormal ocularactivity. In contrast, the oculomotor changes were

frequently correlated with abnormalities ofperception and attention.

ABNORMALITIES OF EYE CONTACT

A fixed penetrating stare directed into theexaminer's eyes, at a distant point, or avoidanceand failure of eye contact were noted in 34patients. These signs were equally common inacutely and chronically ill individuals, and usuallyresponded promptly to neuroleptic treatment inpatients with acute psychosis. Interrogation of thepatient rarely provided a clear explanation forstaring or diversion of gaze. A few individualsindicated that staring or avoidance of eye contactwas a response to perceptual change as indicatedby the following examples:

A 21 year old man with chronic paranoid schizo-phrenia, who stared fixedly at the examiner,explained "your face is turning into an animal."The mother of a 20 year old schizophrenic girl

reported: "when I go to the hairdresser I tell herI'll be right back. When I come back an hourlater and walk in she just stares at me like I'm a

new person to her. At other times she stares ather father like a stranger and shouts 'Get him outof here, he's doing things to me. Who is he? Gethim out!'"

A 17 year old boy avoided eye contact because"I'm afraid you'll read my thoughts."No change in simultaneous EEG accompanied

these clinical events.

ALTERED BLINK RATE

Although both Kraepelin (1913) and Bleuler (1950)remarked upon increased blinking in dementiapraecox, quantitative studies of blinking in thisillness are lacking. Abnormalities of blinking inthis group of unmedicated schizophrenic patientsfell into three categories: (1) decreased blinking,staring, and absent eye contact, most commonlyseen in acute exacerbations of the disorder; (2)steady increase in blinking at rest in patients withchronic schizophrenia; (3) episodic paroxysms ofrapid rhythmical blinking associated withhallucinations, sudden impulsive acts, or deludedspeech.

Sixteen patients demonstrated episodes ofrhythmic or paroxysmal blinking at rates up to2.5-3 per second, and seven patients, four of whomhad never received neuroleptic treatment, dis-played absent or decreased blinking (0-1 perminute).

Eight patients showed abrupt change in blinkrate during delusional excitement, while speakingin response to hallucinated voices, or duringautistic reveries.

A 26 year old former college student, in hospitalfor nine years with an unrelenting dementiapraecox, sat indolently in the dayroom of thehospital blinking steadily two and a half times persecond. He reported that he was in a "wakingnightmare" of frightening sexual experiences(Fig. 1).A patient with acute catatonia who was studied

before all treatment blinked only two to threetimes per minute during the day, but exhibited2-10 second epochs of rhythmic blinking two anda half to three times per second associated with aposture of supplication or deep sighing respirationat intervals during a sleepless night (Fig. 2).

ABNORMAL BLINK (GLABELLAR) REFLEXIn response to gentle taps of the glabella repeatedat one second intervals, most normal adultsrespond by single blinks to the first two to five taps,then stop blinking unless stimulation is discon-tinued for 10-20 seconds, after which the responsereturns and again habituates after repetition(Overend, 1896). Twelve of the 50 patients in thisstudy had no response to glabellar tap, six failedto habituate the reflex after 10 or more taps, and14 patients displayed paroxysmal bursts of rapidblinking to each tap on repetition. Absent blinkreflex was most common in patients with acuteexacerbation of psychosis, while persistent or

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Janice R. Stevens

A.D. 26 YEAR OLD 0' CHRONIC UNDIFFERENTIATED SCHIZOPHRENIA 4/26/76 No Med Mo

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C4-P *.,- s>---5s> '>- 9\¢;-x--\->-\w<>-\V-\'->h>o >M N 5 5 S T > t +

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eye

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50 jV 5/7/76 No Meds 6 Wks

.A.MM.M,i2r- ,-. ---- I v -1- . - .

4/26 3:14 pm "I keep feeling Im going to bed witha womon.

*.w ., _ ..... .JAe,,.-.%k, As,

j 2'4:02 pm Dozing No clinical sign

1.6 43 pm Eyes closed "My problem is think I'm not born. It's

like a woking nightmare.

Fig. 1 EEG-EOG by radiotelemetry in a 26 year old man shows steady rhythmic blinking which almostobliterates EEG on the top two panels. Note brief "spike" discharge at 4:02 pm from right parieto-occipitalregion while patient is dozing. No clinical signs detected. EEG shows asymmetrical temporal function withtheta activity on the left, high voltage alpha spindles on the right as patient lies quietly with eyelidsfluttering in a "waking nightmare."

paroxysmal response was more characteristic ofchronic or less florid psychoses in patients with-drawn from neuroleptics. Six of the 10 patientswho had received no previous treatment had noblink reflex to glabellar tap. Return and per-sistence of the glabellar reflex was one of theearliest effects of neuroleptic drug treatment inthese patients.

LATERAL EYE MOVEMENTSAbnormalities of three types were recorded: (1)rapid, irregular, searching movements; (2) spon-taneous, rhythmic, horizontal saccades; (3) single,sustained, lateral glances.

Darting, rapid, irregular searching movementswere exhibited by 12 patients, and were observedmost commonly during acute exacerbations of theillness or before all treatment. During such be-haviour, patients appeared to be hypervigilant

and looking in all directions for the source ofauditory or visual stimuli imperceptible to theobserver. Characteristically this was accompaniedby speech arrest or drivelling. In contrast topsychomotor seizures, which such ocular auto-matisms may resemble, the darting eye movementsof the psychosis usually can be readily, if briefly,interrupted by speaking to or touching the patient.Although the patient can thus be made aware ofthe activity, an explanation is rarely forthcoming(Fig. 2).Seven patients, including three without previous

treatment, displayed episodes of sustained hori-zontal lateral oscillations of the eyes at rates of oneto two per second lasting for 10-20 seconds. Theserhythmic ocular movements resembled nystagmusin amplitude of excursion and return of eyes tomidposition after each lateral movement. Rarelyobserved during conventional neurological ex-

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Disturbances of ocular movements and blinking in schizophrenia

Acute catatonic, 21 year old a 12/30/76Lights out, searching with eyes

C3-P3

T3 - Ts

C4 P4 --*_

T4 - T6

Lat. eye .', .- > ,- , w , <

Vert eye-* -

Stood up, darting loterol glonces j50 uYs

e, u le respon 11

Mute, unoble to respond

Fig. 2 Telemetered EEG-EOGfrom a 21 year old man withacute catatonia for three dayswith no previous treatment.Top: EEG is unremarkable indark room at night. Blinkingoccurs in showers accompaniedby lateral eye movements.Middle: 11 am, lighted room.Patient is mute, statuesque,appears frightened. There arerapid, darting, searching,horizontal eye movements.Bottom: midnight in lightedroom. Patient is unable to sleepor respond, and is blinkingrhythmically and rapidly. EEGshows only low voltage fastactivity.

amination, spontaneous horizontal oscillationsusually occurred during autistic reveries or psycho-motor blocking. These episodes usually lasted forless than 10 seconds, and continued for 30-60seconds in severely disturbed patients, particularlythose with intense delusory and hallucinatoryexperiences (Fig. 3).

Unexplained single sustained lateral glances in-terrupted the speech or attention of 14 patients,and, in their most extreme form, constituted acontinuous stereotyped automatism in two patientswith far advanced schizophrenia.

A 37 year old man in hospital for nearly 20years after adolescent onset of schizophrenia stoodby the hour against the wall in the hospital day-room repeatedly turning his eyes from side to sideas though following a tennis match. Meanwhile hetwisted his hands together steadily, flicking hisfingers, making signs to himself, smiling andlaughing vacuously. On reclining at bedtime his

head remained flexed on the neck several inchesabove the mattress ("psychological pillow"), andlateral eye movements continued for several hoursuntil sleep supervened.

IRREGULAR OCULAR PURSUITUsing simple bedside examination of extraocularmuscle function in which the patient was asked tofix his eyes on the examiner's moving finger, flash-light, or the movement of his own finger, 24patients demonstrated one or more abrupt arrestsor coarse saccades during each trajectory ofhorizontal ocular movement. Four patients, allwith severe chronic schizophrenia, were entirelyunable to follow the moving object with the eyes,and two patients with previously untreated acuteschizophrenia repeatedly lost ocular contact withthe moving object as their eyes returned frompursuit to staring at the examiner's face.

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Janice R. Stevens

ED. 22 YEAR OLD a CHRONIC

I5

I-T4-T6

UNDIFFERENTIATED SCHIZOPHRENiA 6/2 /76 No Med 2 Mos,:s _F*b~

_V& WY

\>A

Vert 2n eyes s n g l "M l -t A. Dr.,

Lot eye ;A ,_

2:14 pm Rubbing eyes, squeezing genitals "My legs hurt."Atnotlae. Dco enters.

Masturbation contmninuc I;tnncv.J..Qft.

6/3 9:34 pm Quiet, staring Muttering to sefFig. 3 EEG-EOG recorded by telemetry from a 22 year old man demonstrates rhythmic I cps lateralsaccades associated with spindled alpha activity during autistic reverie.

Discussion

SPONTANEOUS BLINKING: CLINICAL ANDEXPERIMENTAL STUDIESIn contrast to normal control subjects, whoseblink rates varied from 8-22 per minute (Zametkinet al., 1978), 17 patients in this series had restingblink rates in excess of 60 per minute. Sustainedhigh blink rates were more common in patientswith previously treated chronic schizophrenia,while blink rates of less than five per minute werefound in five of six patients with catatonic schizo-phrenia. There are many studies of reflex blinkingand the glabellar reflex in the literature, but veryfew address the clinical significance of spontaneousblinking. Ponder and Kennedy (1928), in one ofthe few published studies of quantitative blink ratein man, noted that the rate of blinking tends to beremarkably constant in a given individual, and re-mains essentially unchanged by darkness, tempera-ture, humidity, anaesthesia of the cornea, ordeafferentation of the fifth cranial nerve. Observ-ing that one of the earliest features of postence-phalitic Parkinsonism was the almost completeabsence of blinking, Ponder and Kennedy proposedthat normal blinking depends on the integrity ofthe basal ganglia.

The centres responsible for initiation andmodulation of spontaneous blinking are poorlydefined. Van Buren (1963) reported rapid burstsof blinking after stimulation of the caudatenucleus in man. Nashold (1969, 1970) elicited eyeclosure and rhythmic lid flutter in response tostimulation ventral to the superior colliculus andcentral grey matter, a region from which sensa-tions of burning chest pain and intense emotionalreactions were also elicited.

LATERAL SACCADES AND GLANCESThe darting glances displayed by these patientsare strikingly similar to the ocular searching move-ments termed "checking" displayed by cats andmonkeys in strange environments, when intenselyfrightened, or after administration of amphetamineand cocaine (Ellinwood, 1974). Sato (1977)described visual searching movements afterstimulation in the nucleus accumbens in cats.Similar movements are reported in encephalitis,alcoholic encephalopathy, pretectal lesions, andtemporal lobe seizures (Mayanagi and Walker,1974; Escueta et al., 1977). Shimazano et al. (1965)noted that, in contrast to normal subjects whocharacteristically increase horizontal saccades inresponse to external stimuli, patients with schizo-

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Disturbances of ocular movements and blinking in schizophrenia

phrenia decrease or arrest rapid horizontal eyemovements in response to the same stimuli. Theseinvestigators proposed that the increased horizontaleye movements of schizophrenia, which theytermed "waking REM," do not simply reflectarousal but represent a mechanism closely relatedto the psychotic state.We observed similar ocular movements after

stimulation of the mesolimbic dopaminergic path-way in cats and in response to apomorphine andother dopaminergic agents (Stevens et al., 1974;Stevens and Livermore, 1978). These stereotypedresponses were abolished by neuroleptic agents orby elimination of visual stimuli, suggesting thatthe ocular movements represent dopamine-mediated automatisms elicited by visual stimuli(Stevens et al., 1977).Wallach and Wallach (1964) described episodic

rapid regular horizontal oscillations of the eyes atrates of 60-100 per minute in children and adultswith severe forms of schizophrenia. Regularlyassociated with severe thought disturbance, pre-occupation with endogenous percepts, and a senseof personal dissolution, rhythmic lateral saccadesin their patients were also abolished by fixation ofattention and by remission of the illness. Recur-rence of rhythmic saccades coincided withdeterioration or recurrence of psychosis.

OCULAR PURSUITFirst described and illustrated graphically inpatients with dementia praecox by Diefendorf andDodge in 1908, interruption of smooth ocularpursuit movements has more recently beenrecorded again in a high percentage of patientswith schizophrenia and mania (Holzman et al.,1973, 1976; Shagass et al., 1976). Savitsky andWinkelman (1947) described similar cogwheelmotion on deviation of the eyes in patients withdisease of the corpus striatum, and Luria et al.(1966) reported similar saccades in patients withfrontal lobe lesions and severe cognitive disorders.Interruption in smooth pursuit can be overcomepartially by increasing the patient's attention tothe task (Shagass et al., 1976).

SCHIZOPHRENIA, DOPAMINE BLOCKADE, AND THELIMBIC SYSTEMEvidence that the effectiveness of neurolepticagents against the symptoms of schizophrenia isrelated directly to the capacity of these agents toblock dopamine receptors in the brain has impli-cated central dopaminergic systems in the patho-physiology of schizophrenia (Carlsson andLindquist, 1963). Striking similarities between thesubjective disturbances and stereotypes of

schizophrenia, and the auras and automatisms ofpsychomotor epilepsy suggest that schizophrenia,like psychomotor epilepsy, is associated with ab-normal function in the limbic system (Stevens,1973). The dopamine innervation of the limbicsystem derives principally from the most medialunits of the pars compacta of the substantia nigra(SN), and from the ventral tegmental area (VTA,A10), located just medial and rostral to SN. FromVTA, axons of the dopaminergic neurones of themesolimbic system ascend to the nucleus accum-bens, olfactory tubercle, nucleus of stria terminalis,diagonal band, lateral septum, and the centralnucleus of the amygdala (Ungerstedt, 1971). Ab-normal electrical activity has been reported fromthese regions in schizophrenic patients by Heath(1954), Hanley et al. (1970), and others. In keep-ing with a more medial position in the forebrain,the nucleus accumbens projects to more axialstructures of the diencephalon and mesencephalonthan the caudate nucleus, including the para-median pontine reticular formation and tectum(Domesick et al., 1976), regions closely associatedwith regulation of extraocular movement, arousaland attention.

Species specific stereotyped exploratory be-haviours released by dopaminergic agents, consist-ing of sniffing, licking, and chewing in rodents,depend on the integrity of the neostriatum(Randrup and Munkvad, 1967), while increasedexploratory activity induced by these agents isattributed to activation of the nucleus accumbensand other components of the limbic striatum(Iversen, 1977). The disturbances in eye movementdemonstrated by schizophrenic patients are usuallyattributed to the heightened state of fear orarousal associated with the acute psychosis. How-ever, the occurrence of these disturbances inpatients with longstanding psychosis, the modula-tion of these signs by agents which alter centraldopamine function, and the appearance of similarsigns after stimulation of the mesolimbic dopa-minergic system in experimental animals andduring temporal lobe seizures of man suggest thatthese ocular signs may represent abnormalfunction of the mesolimbic dopamine system.

I express my appreciation to Dr John Lipkin, USVeterans Administration Hospital, Portland,Oregon, to Dr Duane Denney, University ofOregon Health Sciences Center, Portland, Oregon,to Dr Richard Wyatt, National Institutes ofHealth, Washington, DC, to Dr Ernst Rodin,Lafayette Clinic, Detroit, Michigan, to Dr GeraldKlerman, Eric Lindemann Mental Health Center,Boston, Massachusetts, and to the staffs and

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patients of these hospitals. This study was sup-ported by National Institutes of Health Grant18055.

References

Bleuler, E. (1950). Dementia Praecox or the Group ofSchizophrenias, p. 22. Translated by J. Zinkin.International Universities Press: New York.

Carlsson, A., and Lindquist, M. (1963). Effect ofchlorpromazine or haloperidol on the formation of3-methoxytyramine and normetanephrine in mousebrain. A cta Pharmacologica et Toxicologica, 20,140-144.

Diefendorf, A. R., and Dodge, R. (1908). An experi-mental study of the ocular reactions of the insanefrom photographic records. Brain, 31, 451.

Domesick, V. B., Smith, G. P., and Nauta, W. J. H.(1976). Contrasting projections of the nucleusaccumbens and caudato-putamen in the rat.Procedures of the American Anatomy Society, Lex-ington, Kentucky.

Ellinwood, E. H. (1974). Behavioral and EEG changesin the amphetamine model of psychosis. In Neuro-psychopharmacology of Monoamines and TheirRegulatory Enzymes, pp. 281-295. Edited by E.Usdin. Raven Press: New York.

Escueta, A. V., Kunze, U., Waddell, G., Boxley, J.,and Nadel, A. (1977). Lapse of consciousness andautomatisms in temporal lobe epilepsy: a videotapeanalysis. Neurology (Minneapolis), 27, 144-155.

Hanley, J., Berkhout, J., Crandall, W. R., Rickles,W. R., and Walter, R. D. (1970). Spectral character-istics of EEG activity accompanying deep spindlingin a patient with schizophrenia. Electroencepha-lography and Clinical Neurophysiology, 28, 90.

Heath, R. G. (1954). Studies in Schizophrenia. HarvardUniversity Press: Cambridge.

Holzman, P. S., Proctor, L. R., and Hughes, D. W.(1973). Eye-tracking performance in psychiatricschizophrenia. Science, 181, 179-181.

Holzman, P. S., Levy, D. L., and Proctor, L. R.(1976). Smooth pursuit eye movements, attention,and schizophrenia. A rchives of General Psychiatry,33, 1415-1420.

Iversen, S. D. (1977). Striatal function and stereotypedbehavior. In Psychobiology of the Striatum, pp.99-118. Edited by A. R. Cools, A. H. M. Lohman,and J. H. L. van den Bercken. Elsevier/North-Holland Biomedical Press: Amsterdam.

Kraepelin, E. (1913). Lectures on Clinical Psychiatry,p. 24. William Wood and Company: New York.

Luria, A. R., Karpov, B. A., and Yarbuss, A. L.(1966). Disturbances of active visual perception withlesions of the frontal lobes. Cortex, 2, 202-212.

Mayanagi, Y., and Walker, A. E. (1974). Experimentaltemporal lobe epilepsy. Brain, 97, 423-446.

Nashold, B. S., Wilson, W. P., and Slaughter, D. G.(1969). Sensations evoked by stimulation in the mid-brain of man. Journal of Neurosurgery, 30, 14-24.

Janice R. Stevens

Nashold, B. S. (1970). Ocular reactions from brainstimulation in conscious man. Neuro-Ophthalmology,5, 92-103.

Overend, W. (1896). Preliminary note on a newcranial reflex. Lancet, 1, 619.

Ponder, E., and Kennedy, W. P. (1928). On the actof blinking. Quarterly Journal of ExperimentalPhysiology, 18, 89-1 10.

Randrup, A., and Munkvad, I. (1967). Stereotypedactivities produced by amphetamine in severalanimal species and man. Psychopharmacologia, 11,300.

Sato, Mitsumoto (1977). Functional changes in thecaudate and accumbens nuclei during amygdaloidand hippocampal seizure development in kindledcats. Folia Psychiatrica et Neurologica Japonica, 31,501-512.

Savitsky, N., and Winkelman, N. W. (1947). Cogwheelphenomenon of the eyes: its clinical significance.Archives of Neurology and Psychiatry (Chicago),57, 362-368.

Shagass, C., Amadeo, M., and Overton, D. A. (1976).Eye tracking performance and engagement ofattention. Archives of General Psychiatry, 33,121-125.

Shimazano, Y., Ando, K., Sakamoto, S., Tanaka, T.,Eguchi, T., and Nakamura, H. (1965). Eye move-ments of waking subjects with closed eyes. A com-parison between normals and chronic schizophrenics.Archives of General Psychiatry, 13, 537-543.

Stevens, J. R. (1973). An anatomy of schizophrenia?Archives of General Psychiatry, 29, 177-189.

Stevens, J. R., Wilson, K., and Foote, W. (1974).GABA blockade, dopamine and schizophrenia: ex-perimental studies in the cat. Psychopharmacologia,39, 105-119.

Stevens, J. R., Livermore, A., and Cronan, J. (1977).Effects of deafening and blindfolding on ampheta-mine induced stereotypy in the cat. Physiology andBehavior, 18, 809-812.

Stevens, J. R., and Livermore, A. (1978). Kindling ofthe mesolimbic dopamine system: animal model ofpsychosis. Neurology (Minneapolis), 28, 36-46.

Taylor, M. A., and Abrams, R. (1975). A critique ofthe St Louis psychiatric research criterion forschizophrenia. American Journal of Psychiatry, 132,1276-1280.

Ungerstedt, U. (1971). Stereotaxic mapping of themonoamine pathways in the rat brain. Acta Physio-logica Scandinavica, Supplement 367, 1-48.

Van Buren, J. M. (1963). Confusion and disturbanceof speech from stimulation in vicinity of the head ofthe caudate nucleus. Journal of Neurosurgery, 20,148-157.

Wallach, M. B., and Wallach, S. S. (1964). Involuntaryeye movement in certain schizophrenics. A rchivesof General Psychiatry, 11, 71-73.

Zametkin, A., Stevens, J. R., and Pittman, R. (1978).Ontogeny of spontaneous blinking and of habitu-ation of the blink reflex. Annals of Neurology. Inpress.

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