temporal perception, aphasia and dÉjÀ vu

403

TEMPORAL PERCEPTION, APHASIA AND DEJA VU

BY

ROBERT EFRONNeurophysiology-Biophysics Research Unit, Veterans Administration Hospital

Boston, Massachusetts

Moreover, something is or seemsThat touches me with mystic gleamsLike glimpses of forgotten dreams—Of something felt, like something here;Of something done, I know not where;Such as no language may declare.

{Tennyson)

"Yossarian shook his head and explained that deja vuwas just a momentary infinitesimal lag in the operationof two coactive sensory nerve centers that commonlyfunctioned simultaneously."

—Heller (196\)

IN order to deal appropriately with the events in its environment, ananimal must perform at least two essential actions. It must be able toidentify or characterize an event, and it must also be able to determinewhen the particular event occurred in relation to other events. Withoutthe capacity to accurately identify both the nature as well as the time ofoccurrence of an event, effective action would be impossible.

The capacity to perform these functions is necessary to all information-processing systems whether they are conscious or not. The necessity forthe identification of the event itself is obvious. An illustration of theneed to identify the time of occurrence is, perhaps, most familiarlyillustrated in a ship's log. This is a bound book in which is kept a chrono-logical account of the events which have occurred. Each event carrieswith it a "time-label." From such a log it is possible to reconstruct thecomplete history of the ship. If the record had been kept on loose sheetsof paper which were not filed in order, it would be more difficult toreconstruct the history. If the loose record had no time or date "labels,"

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404 ROBERT EFRON

it would be virtually impossible to reconstruct more than fragmentaryparts of the history, and finally, if each word were on a separate card andthey had been randomly mixed, reconstruction would be theoreticallyimpossible. "Meaning" requires that the unitary bits of information bekept in a proper sequence.

A word is a sequence of auditory events (phonemes). Each word of alanguage is a unique sequence (except for rare homonyms such as "here"—"hear") of the small number of phonemes which serve as the base of aparticular language. Let us suppose that an individual loses the capacityfor identifying the correct order of phonemes. The word "electrician""i lek' tris' an" might as easily be interpreted as "tris' lek' an i" or as"an i tris' lek." The unique coding having been lost, words will be eithermeaningless or incorrect (such as, "stop"—"pots" which happen to havethe same phonemes). An occasional word might be correctly identified bychance, but the vast majority would be erroneously identified.

As languages are highly redundant, and as certain phoneme-sequencesdo not occur in particular languages, the jumbled phonemes might onoccasion be sorted out by applying the rules of the language deductively.This would be a slow process analogous to cryptogram solving and wouldalmost certainly be insufficient to understand normal English speech whichcontains 120-150 words per minute and an average of 5 phonemes perword. This is a rate of roughly 80 milliseconds per phoneme. Anyreduction in the capacity to "time-label" or "sequence" phonemes from80 milliseconds to 100 or 200 milliseconds should, by our reasoning, havesome effect upon comprehension of speech. What is the importance ofthis function in aphasic disorders? A similar defect in the efficiency ofproducing a proper phoneme or word sequence might result in jargon,neologisms and "word-salad"—more symptoms of aphasia. Lashley(1951) has discussed the logical necessity of proper sequence in verbaloutput but did not analyse the similar necessity of input sequencediscrimination. Brain (1950) has discussed the necessity for inputsequence analysis.

Previous studies (Efron, 1963a, b, c) have been concerned with thephysiological basis for the judgments of simultaneity and of sequence oftwo sensory events. The data of these experiments lent considerablesupport to the hypothesis that certain information (relative to the time ofoccurrence) is transferred from nondominant to dominant hemispherebefore temporal discrimination of simultaneity and order can be performed.It is in this sense only that we may say that the function of temporalperception of sequence is "located in" or "performed by" the hemispherewhich is dominant for speech. This hypothesis was tested quantitativelyin several experiments and was found to be consistent with the results.

The hypothesis did not specify which part(s) of the dominant hemisphere

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TEMPORAL PERCEPTION, APHASIA AND DEJA VU 405

was concerned with this function. However, if the hypothesis is correct,it should be possible to detect a defect in sequencing activities in patientswith lesions in the "dominant" hemisphere, and by analysis of the results, itmay be further possible to localize the region performing this activity evenmore precisely. Thus, the detection of any sequencing defect in dominanthemisphere lesions (as contrasted with nondominant hemisphere lesions)will strongly support the hypothesis previously formulated.

It is the purpose of this paper to present the evidence which suggeststhat the regions in the left hemisphere concerned with temporal discrimina-tion lie in the temporal lobe and extend posteriorly at least as far asWernicke's area and the angular gyrus. In addition, evidence will bepresented which indicates that some differentiation of various functions oftemporal analysis can be detected within this region.

The implications of these findings as they may apply to a general theoryof hemisphere dominance and to some of the specific symptoms of aphasia,and deja vu will be discussed.

METHODS

Visual stimuli consisted of 5 millisecond "square" pulses of light. Thecharacteristics of the light source and the means of controlling its durationwere described previously (Efron, 1963a). Two independent light sourceswere projected (by means of a half-silvered mirror) upon a Ramsden eyepiece. A red filter was placed before one light and a green filter was placedbefore the other light. The subject, looking into the eyepiece mono-cularly, perceived a round homogenous flash of light subtending approxi-mately 30 degrees. The subject was allowed to use either eye. Noattempt was made to correct for the difference of intensity of the twoflashes of different colour. The two coloured flashes were separated byvarious intervals of time from 0 to 600 milliseconds, and the pair of flasheswas repeated every four seconds. The subject was required to indicatewhether the red or green light appeared first.

Auditory stimuli consisted of tones of 10 milliseconds' duration. Thetones were produced by feeding a small earphone with a train of pulses froma gated Tektronix wave form generator, Type 162. Two pulse frequencieswere used—25OOpps and 250pps—thus giving rise to a high-pitched "bleep"and to a low-pitched, somewhat rasping "bop." There was no attempt tomake these sounds of equal energy, or of equal apparent loudness. Theywere both suprathreshold. Again, the subject merely had to reportwhich sound was first when the pair of sounds was repeated every fourseconds.

Subjects were selected from the in-patients on the neurology wards.Twelve subjects were obtained with unequivocal lesions of the left hemi-

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406 ROBERT EFRON

sphere of whom 11 had some degree of aphasia. Four subjects wereobtained who had unequivocal lesions of the right hemisphere in the samegeneral areas. The 5 subjects without aphasia constituted the controlgroup and were matched as closely as possible for age and general alert-ness. Patients with diffuse cerebral disease were excluded, as well as thosewith clinically obvious dementia. Patients with such a profound aphasiathat they could not be instructed in the task were regretfully excluded.Some of the aphasic patients gave their responses by hand signals. Theywere instructed to point upward for high-pitched sound first, downwardfor low-pitched sound first, and to slap their thighs when the stimuli wereconsidered "together" or "simultaneous" or "don't know." Similarly,they pointed to a red or green piece of filter to indicate which light flashedfirst. Considerable patience was necessary, and in a few subjects a largenumber of practice trials, before they understood the instructions.

EXPERIMENTAL PROTOCOL

The subjects were first introduced to one stimulus—the high tone, forexample, and this was identified and the appropriate expression evolved.Then the low tone was introduced alone and identified. Finally, the twosignals were introduced with a one-second interval between them, and theywere instructed to indicate by pointing (or by speech if this was possible)which tone or coloured light appeared first. A three-choice answer waspermitted—the third choice being "don't know" or "together."

The experiment consisted of 130 determinations of which 10 were madewhen the stimuli were simultaneous, 60 in which the high tone or red lightwas first and 60 in which the low tone or green light was earliest. Thirteenselected intervals (no interval counting as one) were given randomly butensuring that 10 determinations were made at each of the thirteen intervals.The subject was permitted to observe as many pairs of flashes as he wishedbefore he gave his reply. It was possible, during the instruction period todetermine the overall range which would be covered and select the thirteenintervals so that a 100 per cent correct response would be given on the firstand thirteenth intervals. Occasional errors were made in this selection sothat some subjects did not quite get a perfect score on the first and thir-teenth intervals and others had perfect scores for the first and last two orthree interval periods. It will be seen that these methodological errors donot lead to any confusion or to significant statistical problems. Theyoccurred only because of the necessity to keep the number of determina-tions to a small number to prevent fatigue.

Half the subjects were first instructed and tested with visual stimuli,the other half were first tested with auditory stimuli. Every subject wastested for both visual as well as auditory tasks. Only one subject (SU)failed to recognize that the two tests were essentially similar and he there-

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fore required equally detailed instructions for the second test. The othersimmediately recognized the similarity of the instructions as to signaUingtheir answer. There were obviously no such problems for the controlsubjects whose speech was normal.

RESULTS

The two most striking facts which emerge from the results are (1) thatthe lesions which produce disturbances in the discrimination of temporalsequence are all in the hemisphere which is dominant for speech functionsand (2) that every subject with a dominant hemisphere lesion who haddifficulty with temporal analysis also had some degree of aphasia.

The experimental subjects were divided into two major groups—thosewith or without aphasia. Table I lists the results of the performance in all

TABLE I.—100 PER CENT CORRECT THRESHOLD BY SUBJECT

SubjectNon-aphasic

CHBEMOZWCU

AphasicBUAN

A. MASGARELAR

CLB. GAL

MANHA

C. SU

BRE(LH)Word-blind

Age

3731644953

435543314461

55634451

51

45

VISUALGreenfirst

10015010015075

125125200200150250

300300250350

650

400

Redfirst

15010010015075

100150300200150150

300300300350

550

500

Mean

12512510015075

112-5138250200150200

300300275350

600

450

Lowtone first

15015075

150100

700600700700700150

350200200175

600

>700

AUDITORYHigh

tone first

15020050

175100

600500700600700400

250250300150

600

>700

Mean

15017562-5

162-5100

650550700650700275

300225250162-5

600

sixteen subjects for both auditory and visual tests. In this table, thenumerical value used is the interval (expressed in msec.) at which the subjectcorrectly identified the sequence in each often trials (100 per cent correct).As some difference frequently occurred in the two thresholds (red first vs.

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408 ROBERT EFRON

green first), each value is listed and the mean of these two figures has beencalculated. It is immediately apparent that the nonaphasic patients gave100 per cent correct discriminations at shorter intervals than the aphasicpatients. That this finding was true for all other criteria of performanceof less than 100 per cent is seen in figs. 1 and 2 for auditory and visual tasks.

AUDITORY SEQUENCE DISCRIMINATION

100

9O .

SO

| SO

3 0

20-

10-

\ * NON-APHASIC CONTROLS (S)

A O APHASIC SUBJECTS (II)

GOQ

" O G T

O6 0.5 0.4 O3 0.2 0.1 0 01 0-2 0.3 0.4 OS 06

LOW TONE FIRST (SECJ HIGH TONE FIRST (SECJ

FIG. 1.

In these figures, the "simultaneous" or "don't know" replies were equallydivided between the other two choices. These two figures also show thatthe auditory sequence analysis was more severely affected than the visualanalysis.

Examination of the results obtained on the control group reveals thatthe accuracy in the determination of correct sequence is similar for bothvisual and auditory stimuli. The 75 per cent threshold values (Table II)were 80 and 75 milliseconds respectively in the control group. This

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VISUAL SEQUENCE DISCRIMINATION

too

90

a 60uja

| SOL_

zUJ

S 40o*

30

10

o o oxO APHASIC SUBJECTS 00

Nx° \ * i NON-APHASIC CONTROLS (S3 A

07 0 6 05 04 Q3 02 01GREEN FIRST (SEO

01 02 03 04 Oi 06 07RED FIRST (SEC)

FIG. 2.

TABLE II.—75 PER CENT CORRECT RESPONSE THRESHOLD (MSEC.)*

Visual AuditoryControl subjects 80 75Expressive aphasics 100 400Receptive aphasics 160 140

•Interpolated value derived from figs. 3 and 4.

confirms the observations of Hirsh and Sherrick (1961) who found that theinterval required for 75 per cent correct discrimination of sequence was thesame for visual, auditory, and tactile stimuli. The value obtained byHirsh and Sherrick, using normal subjects, was 20 milliseconds which isappreciably smaller than that obtained by our hospitalized patients. Thepoor performance on tasks of sensory discrimination by hospitalized

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410 ROBERT EFRON

patients is well known and could account for the elevated threshold in ourcontrol group.

The aphasic subjects listed in Table I were further divided into twogroups. Group A consisted of those subjects who could be classified ashaving a predominantly "expressive" aphasia, by the criteria of markedlyreduced verbal output, disturbances of rhythm and modulation of speech,dysarthria, defective capacity to emit a meaningful sentence or propositionbut with relatively preserved comprehension of speech. Four of these 6patients had dense hemiplegias, and two had had hemiplegias during theacute phase of their illness.

Group B consisted of those patients whose aphasia was predominantly"receptive" in that their verbal outflow was of normal (or even increased)rate, propositions, sentences, and long expressions could be spontaneouslyemitted which had a normal rhythm and modulation. There was nodysarthria. They all had pronounced difficulty in understanding speech

One patient (SU) was so severely aphasic in both respects that he couldnot easily be classified in this way. He had had three operations on hisleft temporal lobe for a recurrent pyogenic abscess in the last of which theanterior tip was resected. The dissection for drainage of the abscess wasextended posteriorly to the occipital lobe. He was at the very limits oftestability by this technique and did as poorly on visual as on the auditorytask, requiring a 600 millisecond interval before he reached a 100 per centrate of correct responses in either modality. As classification was noteasily decided, the data from this subject are excluded from furtheranalysis.

TABLE III.—100 PER CENT CORRECT RESPONSE THRESHOLD (MSEC.) *

Visual AuditoryMsec.f S.D. Msec.-f S.D.

Control subjects(5) 115 ±28-5 130 ±47Expressive aphasics (6) 175 ±50-4 575 ±192Receptive aphasics (4) 306 ±31-5 235 ±57Unclassified aphasic (I) 600 600Word-blindness+aphasia(l) 450 >700

•Directly determined experimental point.

fEach numerical value derived from an average of the 100% points for "high tone first"and "low tone first." A similar average was obtained of the 100% points for "greenflash first" and "red flash first."

In Table 111 are found the mean values and standard deviation at the100 per cent correct point for these two groups of aphasics comparedwith the control subjects. Fig. 3 and Fig. 4 show the performance ofthese groups compared with the control subjects for all other time intervals.

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TABLE IV.—STATISTICAL COMPARISON*

Expressive aphasics vs. controlReceptive aphasics vs. controlExpressive vs. receptive

I

2-56729-55324-5845

Visuald.f.

1089

P<0-< 0<0-

0500101

/

501653 03893-3820

Auditoryd.f.1089

P<0-001<0 02<001

•Two-tailed test of significance.

Table IV lists the statistical analyses calculated at the 100 per centperformance level with a two-tailed t-test. The probability values inTable IV confirm the view that the performance of the expressive aphasicsis worse on the auditory sequence discrimination and that the receptiveaphasics do worse on the visual sequence discrimination.

AUDITORY SEQUENCE DISCRIMINATION

70

30-

4 0 -

3 0 •

20

OO-O--O-

*"*"*.

A---A . EXPRESSIVE APHASICS (6)

i O — 0 " RECEPTIVE APHASICS (4)

— •CONTROL SUBJECTS (3)

\ \

\ \

\

O.6 0.3 0.4 0.3 0.2 0.1 0 O.I 0.2 0.3 0.4 0.3 0.6

LOW TONE FIRST (SEO HIGH TONE FIRST (SEO

FIG. 3.

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412 ROBERT EFRON

VISUAL SEQUENCE DISCRIMINATION

80

\ ' I\ O ' \ 4—A EXPRESSIVE APHASICS (6)

O. , \ Q PRECEPTIVE APHA«CS K)

CONTROL SUBJECTS (5)

1o.6 OJ 04 0.3 a2 ai o ai 0.2 0.2 0,4 as o.s

GREEN FIRST (SEO RED FIRST (SEC)

FIG. 4.

INTERPRETATION OF RESULTS

There are several objections which might be raised concerning certainaspects of the performance of the control and aphasic subjects. In thefirst place, the control group contained a patient with a lesion in thedominant hemisphere—yet, this subject had normal temporal discrimina-tion of order. It is important to note, however, that this was the onlysubject with a dominant hemisphere lesion who had no aphasia althoughhe had a right hemiplegia. A clinical diagnosis of a capsular lesion hadbeen made. There was no evidence of temporal lobe damage. This casethus serves to demonstrate that it is not a dominant hemisphere lesionitself which is related to disorders of discrimination of sequence, but alesion in such a location which also produces aphasia.

It may be argued that these aphasic patients were merely demented andthat their poor performance was a consequence of general intellectual

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impairment. A cursory examination of the data will dispel this objectionas it can be seen that subjects BU, AN, and EL showed major defects forauditory temporal analysis but had an essentially normal response forvisual analysis. Conversely, subject HA had a normal response to audi-tory stimuli but had defective visual sequence discrimination. If theintellectual defect were of sufficient magnitude to produce a poor responsein one modality it is then inconsistent with the normal performance in theother modality.

It might be argued that the poor performance of the aphasic group inboth tasks was fundamentally due to a failure to understand the instruc-tions or the nature of the discrimination. The design of the protocol,however, excludes this possibility for every subject reached a 100 per centrate of correct identification of sequence at some finite interval. Thisresult proves that the subjects understood the task and could appropriatelysignal their reply. Furthermore, their performance levels at the shorterintervals showed a "normal" (Gaussian) distribution of correct replies{see figures 1, 2, 3, 4) indicating that the achievement of a 100 per centrate of correct replies was not just a matter of chance. This possibleobjection can also be rejected following analysis of the distribution of"simultaneous" or "don't know" replies. In figs. 5 and 6 are illustratedthe frequency of such replies as a function of the interval between stimuli.For both modalities of sensation, the aphasic distribution contains a higher

3In

10

G — © I I APHASIC SUBJECTS

SNON-APHASIC CONTROLS

0.6 QS cU d j 0L2 dl

LOW TONE FIRST (SEC)

~CJ dt2 cb 0 * 05 0 6

WGH TONE FIRST (SEO

Fio. 5.

27 BRAIN—VOL. LXXXV1

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414 ROBERT EFRON

O—O IIAPHASIC SUBJECTS

5 NON-APHASIC CONTROLS

0.6 CL5 04

6REEN FIRST (SECJ

FIG. 6.

percentage of such replies. The distribution of simultaneous replies is"normal" (i.e. Gaussian) in the aphasics as well as in the control subjects,and this is further indication that they understood the instructions. Thecurves also show that even at intervals of 400-600 msec, the aphasicsubjects were still somewhat uncertain as to the correct sequence and onoccasion called the stimuli "simultaneous."

A similar argument applies to the objection that the aphasics were tonedeaf—for if they were, a Gaussian distribution would be most improbable,and a 100 per cent correct reply rate would never be achieved. Similarly,colour blindness or difficulty in colour identification or in colour namingwould not account for these results. A hearing defect too can be excludedfor the same reasons.

The slowness of aphasic replies, again cannot be an explanation as thesubjects could receive as many pairs of flashes as they wished beforesignalling their reply. Their response time was not at issue.

It might be objected that the reason the aphasics made so many errorsis that they received a random distribution of intervals. Perseveration ofreplies might well produce errors even at intervals at which they really couldgive correct discriminations. This too can be discounted as the subjectsBU, AN, EL, and HA performed essentially normally on one of the twotests. Perseveration should play an equally great role in the two pro-cedures.

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TEMPORAL PERCEPTION, APHASIA AND DEJA VU 4 1 5

Finally, any imbalance of intensities of sounds and lights was identicalfor control as well as experimental subjects.

It is clear, therefore, that none of these objections, either singly or inconjunction are sufficient to "explain" the outcome of these experiments.The results of this experiment are consistent with the hypothesis that thefunction of temporal analysis is performed in the hemisphere which isdominant for speech. The disturbances of temporal analysis of sequencewhich occur as a consequence of a lesion in the dominant hemisphere weretheoretically anticipated. It was not possible, on the basis of the pre-viously reported experiments, to make any predictions as to either thelocation of the essential areas within the dominant hemisphere or themanner in which these areas function. Further analysis of the details ofthe performance of these subjects may provide some information on thesequestions.

Table IV shows that the "expressive" aphasics had more difficulty withthe auditory sequence analysis than with the visual and that the "receptive"aphasics showed the reverse. The group of expressive aphasics had severalsubjects (BU, MAS) whose defects were almost exclusively in producingspeech—comprehension being almost normal. The locus of lesions inthis group is likely to be in the region of distribution of the middle cerebralartery in the Sylvian fissure. Thrombosis (the aetiology in all 6 cases) hereusually produces damage to Broca's area as well as to the first temporalconvolution and very likely parts of Heschl's gyrus. The lesions are,therefore, closely related physically to the primary auditory cortex. Thesepatients had the more severe auditory sequencing defects in their perfor-mance in this experiment—although they had the mildest clinical defects in.understanding speech. The lesions of the Group B aphasics were moreposteriorly located (by clinical criteria) in the temporal lobe and thesesubjects had more severe visual sequencing difficulties. Two of thesesubjects (HA, GAL) had marked constructional apraxias. Although someauditory sequencing disturbance was clearly present in these subjects, itwas less severe than in the "expressive" aphasics yet these subjects had themost severe defects in understanding speech.

From the view-point of these experiments, it might appear reasonableto think that the area for temporal analysis shows internal differentiation—the most anterior region being more concerned with auditory sequence(and possibly more concerned with motor sequencing too), and the mostposterior being concerned with visual sequence analysis. If this view is-correct, it is very difficult to understand why the expressive aphasics havesuch mild difficulties in comprehension of speech. Similarly, it is difficultto understand why the "receptive" aphasics have a greater and not a lesserdisturbance.

It should be stressed at this point that the localization of lesions in this.

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416 ROBERT EFRON

group of aphasic subjects is on clinical grounds only and that anatomicalprecision cannot be expected. Yet, it seems most unlikely indeed that theclinical localization is inaccurate to such an extent that the dilemma canbe so simply resolved.

In an attempt to clarify this problem, a patient (BRE) was studied whoseprimary defect is word-blindness. This patient is unable to read words orlarge numbers but is able to identify any letter or numeral rapidly. Hiscomprehension of speech is essentially normal except that he will occasion-ally have difficulty if he is spoken to very quickly. He speaks fluentlyand has the barest trace of an occasional paraphasic difficulty. He has aconstructional apraxia and is dysgraphic for words but can write lettersand numbers. The performance of this subject (Table I) shows a majordefect for both auditory and visual sequencing tasks. His lesion is pro-bably located in the angular gyrus on the right side (he is strongly left-handed). His deficit, followed a severe head injury and for this reasonmultiple lesions cannot be ruled out.

It is thus not possible at the moment to correlate the relative defectsin visual and auditory sequence analysis with the severity of any particular•clinical manifestation with the possible exception of constructional apraxiaAvhich does occur in association with defects of visual sequencing ability.It is also not possible to find a correlation between the clinical severityof any particular defect and the magnitude of the 100 per cent correctresponse threshold. To resolve these questions will require extensiveneuropathological observations and much greater detailed knowledge ofthe anatomy of the dominant temporal lobe than is now available.

The performance of the expressive aphasic subjects on the auditorysequence task is so "poor" that one wonders how they can understandspeech at all. These subjects did not get a 100 per cent score until the twotones were separated by approximately 575 milliseconds. As phonemesoccur approximately every 80 milliseconds, it could be cogently argued thatcomprehension of normal speech should be impossible. This paradoxcan be partially avoided if we appreciate that the comprehension of speechis a matter of probability. It may well be that perfect sequencing is notnecessary for comprehension of speech but that a 75 per cent correct ratewill produce no detectable clinical disturbance of comprehension.Furthermore, the redundancy of the language serves as an additionalsafety margin. It is also known that more information is transmitted bythe consonants than the vowels (written Hebrew, for example, usuallyomits vowels entirely—they are implied by the context) and this gives anadded protection.

Finally, further information is received by word length, intensity,intonation, rhythm, etc. As the quantitative role of these factors isunknown, it is impossible to apply any correction to the 575 millisecond

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figure. These factors, however, may be sufficient to explain why com-prehension of speech is still relatively preserved in the expressive aphasics,despite their poor performance with tones which carry much less helpful"information."1

The performance of the "receptive" aphasics who had major difficultiesin comprehending speech showed a less severe disturbance of auditorysequence analysis than the expressive aphasics. It may well be the casethat the functional defect in the receptive aphasics occurs after thephonemes or words are already sequenced. Indeed, several of thesepatients could repeat words and short phrases although they clearly did notunderstand them. That some defect in auditory sequence analysis ispresent does not necessarily mean that this mild defect is the cause of theircomprehension failure. It must be recognized that after the phonemes ofa word are properly sequenced, logically the next step is to compare thisinput sequence with the memory of that particular sequence and with themeaning of it. (Thus, the reader's auditory sequencing mechanisms maybe intact but he will still not "comprehend" the words of an unfamiliarlanguage.) A discussion of the physiological nature of this comparisonwith a stored "schema" (Brain, 1950,1961) is beyond the scope of the paper.

The disturbances in speech which could occur at this later stage of inputanalysis may have nothing at all to do with temporal analysis. The"receptive" component of an expressive asphasic's difficulty may thus bequalitatively different (i.e. at an earlier stage of input data analysis) thanthe "receptive" component in Wernicke's aphasia.

DISCUSSIONA. Aphasia

It has been seen that the damage to certain areas of the brain disturbsthe function of temporal sequence discrimination. Damage to the same

'An additional complication which must be considered is the work of Liberman,Delattre and Cooper (1952) which shows that certain consonants are correctly identifiedonly when they are followed by particular vowels. These data can be taken to implyeither that the vowel sound has a retroactive effect on the capacity to identify apreceding event (consonant), or that the consonant-vowel complex is normally identifiedas a unit. In support of the first explanation is the work of Treisman and Howarth(1959) on perception of visual and auditory stimuli and of Halliday and Mingay (1961)on cutaneous stimuli. Both groups of workers have shown that a warning stimuluscan alter the threshold for perception of a stimulus which actually came before thewarning. There is evidence in support of the second view {see Brain, 1950, 1961) thata whole word may be identified as a sound unit. In this case, using an estimate of 150words per minute as an average figure for English speech, each word occupies approxi-mately 400 milliseconds. Some defect in comprehension might then be detected if asubject could correctly sequence words only at a rate of every 575 milliseconds. Theexperiments reported in this paper do not permit a decision on the question as towhether it is word sounds or phoneme sounds which are sequenced—they only showthat a defect in sequencing of simple visual and auditory elements exists in aphasics.

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418 ROBERT EFRON

areas is associated with aphasia—indeed, the defect in sequence discri-mination was found only when there was some degree of aphasia present.Is this merely coincidence or does it reflect an essential relationship betweenthe two observations ? Further study of this phenomenon will be requiredbefore a definitive answer can be provided. There are, however, otherobservations which, when coupled with the experiments described here,suggest that this relationship may be of significance physiologically.

It is an everyday clinical observation that communication with aphasicsis improved if they are spoken to slowly. Even with a reduced rate ofverbal inflow, significant difficulty is present but much greater opportunityis allowed for inferring, from the words which have been correctlysequenced, the next word. When the speech rate exceeds the capacity ofthe patient to properly sequence, complete failure of communication mightresult on the receptive side. If this view is correct we should not lookupon the aphasias as unique disorders of language but rather as aninevitable consequence of a primary defect in temporal analysis—in placinga "time-label" upon incoming data. Additional symptoms in the"receptive" aphasics may be due to defects at a later stage of analysis ofthe input pattern. Aphasia, thus considered, would be an epiphenomenon.

Similarly, one might reasonably expect a need for remarkably accurateprogramming of verbal output. In this case there is not only a precisesequence of innervation to a large number of respiratory, lingual, facial,and laryngeal muscles, but a preceding selection of the proper sequence ofwords. A disturbance of central nervous system motor timing mechanismswould be expected to have perhaps more devastating effects on speech thanon any other motor function. Thus, the aphasic dysarthria, facialapraxia, and other symptoms might be at least partially explained.

The area of the brain concerned with input sequence analysis of visualstimuli may be located somewhat more posteriorly than that for auditoryanalysis. If this is damaged and visual discrimination of order is dis-turbed, one might reasonably expect to see constructional apraxias andother "high level" visual disturbances. Indeed, 2 of the 5 patients withposterior lesions and receptive aphasias (HA, GAL) have clearly definedconstructional apraxias and these subjects had poor performance on thevisual task. The subject with word-blindness (BRE) who also had a severevisual sequencing difficulty also has constructional apraxia. The subjectSU similarly has constructional defects, but he is so severely disabled thatan accurate appraisal of any particular symptom is essentially impossible.

It may be objected that the list of special, "higher," or "cognitive"functions attributed to the dominant hemisphere is already so large thatto locate yet another function (temporal analysis of sequence) in thisoverburdened hemisphere is intolerable. The hypothesis that the basic

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TEMPORAL PERCEPTION, APHASIA AND DEjA VU 4 1 9

functions of temporal sequencing lie in the dominant temporal lobe maypossibly serve to resolve this difficulty. It may be precisely becausetemporal sequencing is performed in this area that the "higher" functionsappear to reside there.

In a series of papers, Walshe (1943, 1947) has logically demonstratedthe impropriety of statements to the effect that "speech is located in suchan area" or that "there is an area which performs constructional ewpraxia."The hypothesis that temporal sequencing mechanisms are located orheavily centered in an area does not, I think, merely substitute a new set ofwords for the same concepts to which Walshe objects. We are, in fact,not saying that the symptoms (aphasia, dysarthria, and apraxia) "reside"or are "located" in the major hemisphere. Similarly, we are not sayingthat the normal execution of certain activities (euphasia, euarthria, andeupraxia) is located anywhere at all. We do suggest that there is afundamental mechanism or process related to the requirements of "time-labelling" of input and output signals which is located in the dominanttemporal lobe and that damage to this area and its radiations may result insymptoms of disturbance to these "higher functions." The "higher"functions are not in themselves "located" in the temporal-parietal lobe.Symptoms of inadequate function are not the same thing as functions. Asymptom itself is not localizable—a function can be {see Walshe, 1947).A symptom, nevertheless, may be useful for localizing a lesion.

The fact that all the subjects who had defects in sequencing had notonly some degree of aphasia, but had lesions in the temporal area1 suggeststhat this area (and its connexions) is essentially concerned with time analysis.

B. Temporal Lobe DiseaseThis view is further supported by the notorious frequency of disturbances

of subjective time sense which occur during temporal lobe seizures. Theearliest papers on uncinate fits by Jackson (1888,1890) describes a disorderin perception of time ("dreamy state"). The symptoms of disturbedappreciation of time interval as a consequence of a temporal lobe seizurecan be exceedingly complex—subjective time being either accelerated orretarded or otherwise disturbed even during the course of one seizure(Efron, 1956, 1957). Seizures in these areas also produce speech arrestand word-blindness, and word-deafness is often seen in the post-ictal state.

Patients with damage to the temporal lobe also have memory distur-bances which are associated with disturbances of personal time sense.Symonds (1960) has analysed a group of such patients and concluded that'The concept of a physical basis for memory must allow for the assump-tion, to begin with, that every moment of personal time has its physiologicalidentity, and the further assumption that there are arrangements in the

1Used in this sense, the word temporal is to be taken to include the first frontal•convolution (Broca's area).

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brain for recording these units of time. These constitute the personalclock, which provides for continuity of experience, without which memoryin the ordinary sense could not exist." He then suggested that a "cinemafilm instead of being projected in the ordinary way were cut into shortstrips, and these strips were joined together in a random order instead ofthe proper chronological sequence, the result would have no meaning."Symonds' prediction can be confirmed by a viewing of the recent film"Last Year at Marienbad" directed by Alain Resnais. In this film theplot chronology was intentionally randomized for presumed "artistic"purposes and, as expected, the result had no meaning but conveyed adream-like mood.

C. Dija VuThere is yet another symptom of temporal lobe dysfunction which may

be attributed to a disturbance of the "time-labelling" mechanism—that isdeja vu. We have seen (Efron, 1963a, b) that information pertinent tothe time of occurrence of an event which is received by the nondominanthemisphere may be transferred to the dominant hemisphere. Undernormal conditions of life with the eyes freely moving, the head turning, andsounds being received bilaterally and from all directions, the two hemi-spheres receive essentially the same information about the events of theexternal world. The few milliseconds delay in the time of arrival of thedata from the right hemisphere is not, apparently, subjectively detected.Suppose, however, that the delay in transmission from right to lefthemisphere were, for a period of a minute, delayed by several hundredmilliseconds. Under such conditions, the left hemisphere would receiveinformation (and essentially the same information) twice—once directly,and the second time relayed after this delay from the right hemisphere.Normally an interpretation would be made that two different events haveoccurred. Yet, as has been pointed out, the data are essentially identical.It does not appear to be unreasonable to assume that under these conditionsa person might have the following rapid, but unconscious interpretation:"Everything which I am perceiving now has already occurred once before(because it has already been 'logged-in' by the left hemisphere via thedirect pathway). Yet, I cannot find any memory trace of that previousexperience." A delay in the incorporation of data into a durable memorysystem is well established. In this case, the few hundred millisecondsmight not be sufficient time for the memory (of the undelayed message) tobe filed and retrieved. This subjective interpretation is clearly preferableto the alternative that "Everything is happening twice." The secondinterpretation requires an additional universe of similar events running ona parallel time scale. This latter conclusion is unacceptable as it requiresthat the subject discard his metaphysical principles of identity and causa-lity. Thus, deja vu may be explained.

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After this state of delayed transmission has persisted for a few seconds,,the subject has more information. He can then say "I am aware that aseries of events are apparently occurring twice. As this is not acceptable(for the above reasons), the more likely alternative is that I am merelyanticipating what will occur"—thus, clairvoyance may be explained.

The close relationship between deja vu and clairvoyance, symptomswhich, in some patients (Efron, 1956) occur simultaneously, may beexplicable in this fashion. At any instant the two interpretations mayeven be equally valid. Dickens has most elegantly described the co-existence of deja vu and clairvoyance in David Copperfield, "We have allsome experience of a feeling which comes over us occasionally, of what weare saying and doing having been said or done before, in a remote time—of our having been surrounded, dim ages ago, by the same faces, objects,and circumstances—of our knowing perfectly what will be said next, as ifwe suddenly remembered it." Mullan and Penfield (1959) have calledattention to the fact that deja vu occurs primarily as a consequence oflesions in the nondominant hemisphere. It does not appear unreasonableto assume that a fit in this region may delay transmission of data to thedominant hemisphere—merely virtue of the fact that the interhemisphericpathways are overloaded with seizure discharges.

The preceding interpretations are based upon an implicit assumption—namely, that it is only after sensory data have reached the left hemispherethat one is "conscious" of the occurrence of an event. An "event" whichis not occurring at any particular time (in relation to the "personal clock")can hardly provide the landmarks necessary for the continuity of experienceand cannot be subsequently used to reconstruct reality. Even if theseuntimed events were stored in the memory, they would be of little practicalvalue except possibly for their transient, short-lived consequence. Onemight not be any more conscious of them than of fleeting changes inexcitatory states of spinal cord interneurones. To be conscious of some-thing is to be conscious of something now. It is the thesis of this paperthat the "now" is the moment of arrival of sensory data in the dominanttemporal lobe. It may be argued that this view leads one to the untenableposition that destruction of the left hemisphere should result in un-consciousness. This would be true only if no other region could performthe same function after the dominant hemisphere is destroyed or seriouslydamaged.1

JIt should be pointed out that the cardiac rhythm, normally determined by the rhyth-mic discharges of the sino-auricular node, is only momentarily stopped by destructioaof that region. The migration of the pacemaker to the auriculo-ventricular region-re-establishes the rhythm though at a slower rate. In this respect, it must be recalledthat the aphasic patients could still sequence stimuli (after damage to their dominanthemisphere) but again at a slower rate.

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The suggestion that deja vu represents a disturbance of transmissionof data from the non-dominant to dominant hemisphere is, at the moment,purely speculative. It is put forward, nevertheless, as it is consistent not•only with the clinical and experimental observations but also with thehypothesis that has been elaborated in this paper. The speculation hasadditional merit in that it might be tested during neurosurgical operation"by local ansesthesia of the corpus callosum.

In a previous paper (Efron, 1962c) on the Pulfrich effect, it was pointedout that at the point where the stereoscopic illusion fails (as a consequenceof the excessive time taken by the sensory data from one eye to reach thelevel of consciousness), the subject "sees" two spots. In this case, we aredealing with an artificially introduced delay in one message going to bothliemispheres. At any instant ("now"), the brain is presented with two""images" which are dissimilar. It reasonably concludes that there aretwo different events (spots) at one time.

It may be argued (see first paragraph) that temporal discrimination oforder or "time-labelling" is necessarily present to some extent in allanimals. Why should the function be so localized in man ? Where is itlocated in lower animals ? This question is only a concrete formulation ofthe more general question of cerebral dominance (encephalization). Thatthe time analysis functions of the nervous system of man are localizable inthe hemispheres is no more (or less) mysterious than that any otherfunctions are performed in the cerebral hemispheres. Similarly, the ideathat temporal analysis is performed in the dominant temporal lobe in theintact human is no more distasteful than the idea that the two hemispheresare different in their functions. Furthermore, it is not in conflict with thefact that unconscious temporal analysis takes place at every synapse.Implicit in Sherrington's concepts of the central excitatory and inhibitorystate is the importance of the timing of impulses over the afferent arcs.The subsequent electrical analysis of synaptic action by Eccles (1957) andothers has shown that the time-constant (RC) of the neural membranedetermines the time course of the potential changes induced by each sub-threshold stimulus. Thus, the membrane characteristics may be con-sidered to serve as the elementary building blocks for more elaboratetemporal analysis mechanism. The integration of spinal reflexes such asthe crossed extension reflex requires a sequencing of activity whichis ultimately dependent upon the time-constants of the individualneuronal membranes which in turn depends on their physico-chemical•structure.

The apparent differences in the functions performed by the two hemi-•spheres may be explicable on the basis of the genetic localization of themore complex temporal analysis mechanisms in the dominant hemisphere."Wyke and Ettlinger (1961) have shown that the efficiency of recognition is

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significantly greater when drawings are tachistoscopically exposed to theright visual field as compared to the left. Semmes, Weinstein, Ghent, andTeuber (1960) have shown that lesions in the dominant hemispherefrequently affect sensation bilaterally, whereas lesions in the nondominanthemisphere produce only contralateral sensory disturbances. They havecalled attention to the earlier observations of Foix (1922), Guillain,Alajouanine, and Garcin (1925) which demonstrated this phenomenon.Similarly, apraxias are frequently bilateral following dominant hemi-sphere lesions. Recent work by Goodglass and Kaplan (1962) on thegestural deficiencies in aphasics suggests that this deficiency is a con-sequence of an apraxia and not a defect of "communication." They alsoshowed that the severity of the gestural deficiency is not correlated with theseverity of the "aphasia."

Clinical as well as experimental observations thus strongly support thehypothesis which has been presented in this series of papers that temporalanalysis of sequence, interval and simultaneity is performed in the lefthemisphere in the right-handed subjects, as well as in the majority ofleft-handed ones. The localization of this particular function in the lefthemisphere may make it more efficient for other tasks (requiring accuratetemporal analysis of incoming or outgoing data) to be similarly "localized"in the same or nearby regions. Disorders of the central mechanism(s) forsequence analysis and control might thus account for certain essentialaspects of the symptoms of aphasias, apraxias, and possibly otherdisturbances of "higher" functions particularly memory and consciousness.It is obvious but not trivial to point out that to "think" is to order our ideassequentially and towards a purpose. Randomly occurring mental statesor mental states triggered by chance external events, while they may welloccur all too frequently, are neither purposeful nor can they be called"thinking."

Note added on proof: Prof. O. L. Zangwill has kindly called to my attention amonograph (The Duality of the Mind by A. L. Wigan, 1844, published by Longman,Brown and Green, London) in which the author suggests an explanation of deja vusuperficially resembling the one proposed in this paper. Wigan's thesis is that eachhemisphere has a "consciousness" of its own but that one is normally dominated orsuppressed by the other, Deja vu, according to this view, results from the momentaryloss of this suppression which in turn gives rise to a doubling or a duality of con-sciousness. This concept differs markedly from the speculation put forward in thispaper. The only element in common between the two positions is the view that inman the right and left hemispheres have different functions—a fact which wouldnot be denied by any neurologist.

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BIBLIOGRAPHYBRAIN, W. R. (1950) In: "Perspectives in Neuropsychiatry," edited by D. Richter.

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Jeffress. Chapman, N.Y., p. 112.LIBERMAN, A. M., DELATTRE, P., and COOPER, F. S. (1952) Amer. J. Psychol. 65,497.MULLAN, S., and PENFIELD, W. (1959) Arch. Neurol., 81,269.SEMMES, J., WEINSTEIN, S., GHENT, L., and TEUBER, H. L. (1960) "Somatosensory

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