Brain potentials during sentence verification: Late negativity and long-term memory strength

.Vntropsycholog,e, Vol. 22, No Prmled I” Great Br~tam

5, pp. 559-568.

1984 c

0028 3982 84 S3M+OOC 1984 Pergamon Press Ltd

BRAIN POTENTIALS DURING SENTENCE VERIFICATION: LATE NEGATIVITY AND LONG-TERM MEMORY STRENGTH IRA FISCHLER* and PAUL A. BLCIOM Department

of Psychology

DONALD G. CHILDERS and A. ANTONI~ ARROY~ Department

of Electrical

Engineering

and NATHAN W. PERRY, JR. Department

of Clinical

Psychology,

University

(Accepted

of Florida,

19 April

Gainesville,

FL 32611, USA

1984)

Abstract-Subjects decided whether self-referential statements were true or false. Event-related potentials (ERPs) associated with final words creating false statements displayed a late negativity (N340) relative to ERPs for true completions. The size of this difference between true and false statements was greater for highly familiar statements (e.g. “My name is Ira”) than for less familiar ones (e.g. “I go to bed late”) even after all the statements had been practised a number of times. The late negativity appears to be associated with a discrepancy between presented and remembered information, and its magnitude reflects the long-term familiarity or strength of the remembered information.

INTRODUCTION SINCELINGUISTIC communication is largely sequential, there has been great interest in how a sequence of words acts as a context to activate long-term memory and influence processing of subsequent words [6,28]. A number of recent studies have found differences in event-related brain potentials (ERPs) to words as a function of their relationship to a preceding context, suggesting that ERPs can serve as a real-time measure of language processing. For example, ERPs for individual words presented visually can be distinguished on the basis of whether preceding words were semantically related or unrelated [2, 3, 11, 21, 26) or, in at least one instance, phonologically related or unrelated [24]. The particular ERP feature distinguishing these classes of contexts has varied, but most commonly a greater negativity in the region of 250-450 msec has been observed for target words unrelated to the preceding context. In several of these studies, the context has been in the form of a sentence, with the critical words continuing or completing the sentence in particular ways. In the first of these studies, FRIEDMAN et al. [9] reported a larger late positive component for the final words than for the preceding words in repetitively shown sentences, suggesting to them a process of “syntactic

*To whom correspondence

should

be addressed. 559

560

IKA

FMHLER

(‘I ai.

closure”. In a series of experiments, BRO~.N and MARSH [e.g. 43 have found differences between homophones given noun and verb meanings by a sentence context (e.g. a pretty/roz/ vs the boatman/roz/). KUTAS and HILLYARD [12, 131 have described a late negativity (N400) in the ERPs associated with words that were semantically anomalous completions of sentences (e.g. “He spread the warm bread with socks”. The N400 for semantically incongruous words could be distinguished, on the basis of polarity. latency and scalp distribution, from ERP features for both phyically incongruous words [ 121 and for grammatical incongruities [14]. Semantic incongruity as such does not appear to be necessary for the late ERP negativit! to occur, since a similar negativity has been found for semantically acceptable but unlikely words in context (e.g. “He mailed the letter without a check”) by KL.TAS or 111.[15]. who suggested that the amplitude of the N400 is a function of the degree to which a presented word has not been activated by a preceding semantic context. Ifso. the N400 could serve as a tool ofsome generality in the study of how semantic information is represented and retrieved. We have been studying ERPs associated with a sentence-verification task, in which subjects decide if a statement is true or false. This task has been used extensively in behavioral studies of semantic memory [see 321, since it specifies the information that needs to be retrieved from memory in order for the statement to be evaluated. We have recently described an N400-like feature in the ERPs associated with words completing sentences falsely (e.g. “A robin is a vehicle”) [7]. The study included sentences of negative form. i.e. X is not a I’. and showed greater ERP negativity for the true sentences of this form (e.g. “A robin is not a plant”) implying that the late ERP negativity was not tied to the final decision about the falseness ofthe sentence or to the subsequent response, but to incongruity ofthe two nouns in semantic memory. A subsequent study testing statements that had been learned one day prior to the ERP session showed that the negativity was independent ofwhether subjects had to classify each statement as true or false, or merely attended to the presentation of the successive segments of each statement [8]. KUTAS et al. [ 15) found that the amplitude of the N400 varied inversely with the Cloze probability of their sentence completions; the less likely the completion (and therefore, in their view, the less facilitative priming of the completion by the context) the larger the N400. The statements we used for the verification of semantic information ranged from familiar ones such as “A rose is a flower” to more arbitrary and unfamiliar ones such as “A hammer is an object”. Information familiarity was not directly manipulated, however. and a systematic comparison of our N340 magnitude as a function of familiarity was not made. The present experiment was designed to provide such a comparison. Subjects were asked to verify statements regarding a variety of facts about themselves. Half of these self-referent statements concerned information that should be highly familiar, such as one’s first name. The other half concerned facts not likely to be as strongly represented in memory, such as one’s shoe size. It was hypothesized that the difference in ERPs for true and false statements would be greater for the more familiar statements. Self-referent information was chosen for several reasons. First. the false statements generated are not semantically anomalous, as is “A robin is a truck”. Second. it was felt that the manipulation of familiarity might be more salient for such self-referential information than for either the standard “semantic” materials of our first experiment, or for arbitrary information learned in the laboratory [8]. Also, there have been suggestions that the processing ofsuch information may be different than that of facts that are not self-referential [16]. We were therefore interested in whether the overall difference in true and false self-

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referential statements would resemble that found for statements concerning general semantic knowledge. The experiment was also designed to examine changes in the effects of truth value and familiarity with practice during the session. We suggested previously [7] that the smaller amplitude ofthe late negativity observed in our study compared with that reported by KCTTAS and HILLYARD[12] could be due to our repetition of each statement several times within the session. Any effects of statement familiarity might be expected to be particularly sensitive to short-term repetition during a sequence of trials, with the familiarity effect diminishing or disappearing across trial blocks. Similar changes can occur rapidly in studies of word familiarity and reaction time [27].

METHOD Subjecrs Twelve students at the University of Florida, ages ranging from 20 to 28 years. participated in the experiment. Of these, 10 were male and 11 were right-handed. Some had served previously m ERP studies. but none had experience with the present task. Materials

At the start of their session, each subject provided chosen to reflect well-learned or “strong” facts, such as shoe size or favorite author. These served as the described in Appendix 1. False completions of these that were false for each particular subject. Subjects Recording

the answers to 36 self-referential statements. Half of these were as first name or sex, and half. less famihar or “weak” facts. such true statements for each sub.iect. The set of statements used is sentences were selected that were semantically acceptable but reviewed all 72 sentences once prior to the verification task.

system and procedure

Subjects sat in a Faraday shielded screen room and observed a display monitor located about 80 cm away. A video momtor driven by a Hewlett-Packard terminal was used for the display. A white fixation box was displayed at all times near the centre of the screen and stimuli appeared black-on-white within the box. The fixation box subtended 0.8’ vertically and 3.5‘ horizontally. The words shown within the box were 0.6” high, and subtended 1.0 3.0” horizontally. A Data General Nova 4 computer controlled the display and monitored and recorded the EEG. An asterisk wasdisplayed between trials,and itsdisappearancesignaled thestart ofeach trial. A trial consisted ofa statement shown in three segments, with their onset 800 msec apart and their duration 17.5 msec. The third segment completed the statement, and subjects then indicated whether thestatement was true or f&e by lifting one finger of their rtght hand. For half the subjects, the index finger was used to indicate a true statement and the middle finger to Indicate a false statement. This was reversed for the remaining subjects. All subjects were instructed to read the segments of each statement and make their responses as soon as a decision had been reached. The mstructions stressed accuracy over speed, but subjects were told that reaction time was being recorded. There were four blocks of 72 trials each. Within each block, each of the 72 statements (36 true and 36 false) were presented once. Order of presentation within blocks was randomized. Each block required about 10 min and a few mmutes of rest was allowed between blocks. EEG activity was recorded from Cz, C3, C4, F3 and F4 localions in the lo!20 system. using nonpolarizmg cup electrodes (Beckman). each referred to the lmked mastoids. The choice ofelectrode placements was made durmg an initial series of studies using self-referential statements, prior to publication of KtIrAs ef al. [IS]. While therefore not Identical to that used by Kutas. they allowed for both lateral and midline comparison, includmg a central frontal comparrson that In both their work and ours has shown the greatest difierence in magnitude of late negative components. The EOG was also recorded between the supraorbital and canthal positions of the right eye. Trials with EOG deflections from baseline greater than 15% of the amplitude of a typical eyeblink for a given subject were rejected on-line and re-run at the end ofeach trial block. Across subjects, 7”,, of the trials were re-run due to EOG artifacts .20:, due to responses occuring more than 1.7 set after the final sentence segment appeared and I ‘>;,due to errors. EEG was digitized on-line at 125 samples/set/location and stored for later analysis. Amplifiers were essentially flat over the bandwidth of 1~50 Hz with a SO?,, attenuation at 1 and 50 Hz [5]. The high-pass filter characteristics have been used in our laboratory over the past 15 years. While it is true that this high-pass characteristic may attenuate certain ERP slow waves, a forward shifting in time of these slow components is caused by a nonlinear phase characteristic in the region of the cut-off frequency. A DC-coupled amplifier will solve the attenuation problem. but will not solve the forward shifting of ERP components unless the amplifier also has a linear phase

IRA FISCHLER er al

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characteristic down to DC. Many amplifiers presently used for EEG recordmg do not have such a characterlstlc. In the absence of a standard for these amplifier characlerlstlcs. we feel it is futile to speculate on the extent to which the ERP components are “dIstorted” m the present study by our filter settmgs. We can. of course, prowde a calibration result for various frequencies but such a result is exactly how the low frequency cut-off is determined m the first place. A 10 Hz, 50 JZVsignal was used to calibrate all channels at the start of each session. EEG recording began 400 msec prior to the onset of the first statement segment. and ended 2.1 set after the onset of the final (thud) segment.

RESULTS ERPs averaged across subjects for all true vs all false sentences are shown in Fig. 1A. for location Cz. The horizontal line indicates zero voltage referenced to ground output of the single-ended EEG amplifiers, which was used as a baseline for all amplitude measures below. Presentation of the first two terms of the sentence produced a sizeable P200 superimposed on a generally negative baseline that tended to drift more negative up to presentation of the third segment. A similar negative drift, resembling the CNV that appears prior to forewarned. task-relevant stimulation [30] has been previously observed [7. 121 during sentence presentation. ERPs for true and false statements were indistinguishable during this period. Following the third and final segment, a P200 is again elicited, followed by an irregular negative-going trend that is substantially more pronounced and prolonged for the false statements, with a peak latency of about 340 msec. The same data are combined by statement

A False _........

True -

B We a k.. .. . .. ..

Strang-

set

IO& 0.0 -

1st

Sentence

0.6

I

2nd

1.6

1

2.4

I

3rd Segment

FK;. I. Averaged ERPsforall trueandallfalsestatemencs(A),and forallstrongvsall weakstarements (B): all subJecIs, location Cz. Onset of the first, second and third segments of the statements are indlcaled; the truth value of a statement was determined by the third segment. The horizontal hne indicates zero voltage referenced lo ground.

563

BRAlN POTENTIALS AND MEMORY

strength in Fig. 1B. The ERPs to strong and weak statements are essentially identical (see below). ERPs to the final segment of the sentences for true and false sentences are shown separately for the strong and weak statements in Fig. 2. In each case, false statements are associated with a relatively more negative ERP than that for true statements in the region from about 250 to 450 msec. Overall, the true-false difference appears to be larger for the strong statements than for the weak statements. For both classes of statements, the difference appears larger over the central than frontal locations. TYPE

SENTENCE Strong

Weak

TrueFa 1se ...... ..... ...

F4

_h

IOpV 0

200

400

600

l---

0

200

400

600

msec

FIG. 2. Averaged ERPs for true vs false statements, all subjects, for each of five recording locations. The region shown begins 160 msec prior to the onset of the third and final segment of the statements. The horizontal line indicates zero voltage referenced to ground.

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The ERPs were analyzed by taking the average amplitude within each successive 160 msec epoch, beginning 160 msec prior to onset of the final segment. as the dependent measure in a repeated-measures analysis of variance. Truth value. statement strength, recording location and trial block were included as factors. ERP amplitude varied significantly (all P
1. Average

ERP amplllude over the region 320 480 msec following true and false sentence completions

cz “Srtmg”

Recording locauon c4 F?

F4

siaremenr

‘I rue False Difference “U euk” .sl~ltwuwl.* l-rue False Difference Standal-d 0.7x /IL’.

c3

-0.48 2.42

3.07 0.6 I 2.3b

1.94 1.77 3.17

3 Sb 2.21 1.35

4.39 2.7 1.b.l

0.4b - 0.76 1.22

x0 1.26 1.04

3.73 2.24 I .49

3.33 2.X0 0.53

3.x0 7.94 0.M

I .%I

errors within condttlons

(e.g. true. strong, Cz) ranged

from 0.47 10

The latency of the most negative peak within a region 300~ 600 msec after onset segment for false statements was identified for each subject on Cz. The mean strong and weak statements did not differ. Latency of peak negattvity of ERPs statements was 337 msec, SE. =24 msec; for weak statements. 343 msec. SE. t(l 1)=0.35, P>O.O20.

of the final latency for for strong = 19 msec:

For strong statements. response latency was 803 msec for true and 836 msec for false statements. For the weak statements. latency was 826 msec for true and 881 msec for false. Standard errors ranged from 16 to 20 msec. In an analysis of variance. there were significant effects of truth value. F (1, 11)=8.81, P-cO.05, and statement strength, F (1. 11)=5.94. PcO.05. The interaction of truth value and strength fell short of significance, however, F (1. 11 )=4.59. P ~0.10. indicating that the true-false difference in latency was similar for

BRAIN POTENTIALS AND MEMORY

565

strong and weak statements. Responses became faster across trial block, F (3,33) = 3.62, but this effect did not interact with the other factors.

DISCUSSION A late negativity (N340) was found in the ERPs for false completions of self-referential statements. Since the difference between true and false statements appears to occur during a negative-going phase of the ERP, it seems reasonable to describe the difference as an enhanced negativity for the ERPs associated with false completions, despite the fact that the ERP goes negative with respect to baseline only for Cz and C3 (see Fig. 2). The alternative, that the ERP for true completions is associated with an enhanced positivity in this region, cannot be rejected by the present data. We have elsewhere discussed other reasons for preferring our interpretation of the difference as an enhanced negativity for false completions, rather than either a positivity for true completions in the region or a delayed positivity for false completions [7, 406407; see also 83. The feature closely resembles that found previously for verification of general knowledge [7] in overall appearance of the ERP waveforms, in the size of the amplitude difference between true and false statements and in the tendency for a greater difference to be found in central and (to a lesser degree) right locations. The peak latency of the N340 appears to occur about 50 msec earlier in the present experiment, which could reflect a greater salience for self-referent information, or simply the use of a generally easier task (there were no statements of negative form in the present study, and response latencies were substantially shorter than before). The amplitude, but not the latency, of the N340 was found to be sensitive to the familiarity or strength of the tested information, with a greater amplitude for falsification of familiar statements. The interaction of truth value and statement strength was modest, but the effect was significant and was observed at each recording location. The direction of this difference is consistent with previous demonstrations that the N400 is larger for strongly anomalous completions than weak ones [12] and for less likely than more likely completions [ 151. The manipulation of long-term memory strength was done on a largely intuitive basis and the significant effects of statement strength on N340 amplitude and response latency provides some degrees of validation of our choices. The greater N340 for strong statements is unlikely to be due to the particular words or syntax involved, in view of the similarity of the ERPs to strong and weak statements when averaged over truth value (Fig. 1B). The absence of any difference between strong and weak statements prior to the presentation of the third and final segment also suggests that the effect of familiarity occurs only as the sentence completion is analyzed in context of the preceding information. The effect of statement strength on the amplitude ofthe N340 was maintained through the session; neither the main effect of trial block, nor any interaction involving trial block, approached significance. This finding is an important one, since it suggests that the ERP negativity is a more direct reflection of the long-term familiarity or strength of information in memory than of any changes in expectancies developed as long-term memory is accessed during the session. The familiarity effect occurred despite the preview of all statements before the EEG collection began, the repetition of all statements an equal number of times through the session and the equal probability of completion by a correct or incorrect word. It is possible that more repetitions would reduce or eliminate the difference between the N340 for

566

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strong and weak statements, but then a large number of repetitions would mean that the information is becoming better represented in long-term memory. The absence of changes in the familiarity effect over the “short run”, as defined in this study, contrasts with several studies of word recognition speed. wherein the effects of long-term familiarity or frequency have been reduced or eliminated by a small number of repetitions within a single session [37; cf. 11. KUTAS et al. [lS] showed that the late negativity for words varied inversely with the predictability of the words in context. Our results suggest that the basis of this effect lies more in the automatic activation of long-term knowledge than in subjects’ ability to predict possible target words given some context. We would anticipate, for example. that even if a particular sentence were repeated during a session with the same anomalous completion. as long as the task required comprehension of the words, a late negativity would be found despite the predictability of the anomalous word within the confines of the task. Relation

to other late negative ERPfeatures

The relation among the variety of late negative ERP features now being reported during information-processing tasks is a matter of some controversy [22,8]. The present enhanced negativity for false statements may be distinguished from a “mismatch negativity” or N2 that occurs to unexpected or deviant stimuli [18]. The N340 observed here is centrally rather than frontally maximal, and shows no subsequent enhanced P300 compared to the true statements, despite the task-relevant nature of the match between the final word and the preceding context. Also. in all our studies of verification to date, we have observed no correlation between the peak latency of the late negative feature, and response latency, at least across subjects for averaged data. In contrast, peak latency of N2 typically correlates positively with RT [23]. Finally, N2 is usually associated with infrequent stimuli, while the false statements in the present study were no less frequent, and presumably no less expected, than the true statements. It is also difficult to equate the N340 with the “processing negativity” [ 171 that is observed during selective attention tasks, where targets specified for further processing show enhanced negativity compared with nontargets. Both the true and false completions required a decision and response to be made. so the analogy to tasks involving selection of, or orienting to, a subset of stimuli is unclear. The N340 seems unlikely to be identified with resolution of the CNV that develops prior to the onset of the final segment of the sentence (see Fig. 1), sincewe have found the amplitude of the N340 to be unaffected by whether or not an overt decision is required. while the CNV is significantly influenced by this manipulation [8]. Also, KUTAS and HIILYARD [I41 have found an N400 to unlikely words in the early portions of sentences where no apparent CNV had developed. The false statements in the present study were not semantically anomalous, but simply not consistent with patterns previously learned by the subjects. The implication is that such negativity will be found whenever a verbal context activates one code and another is actually presented. In a subsequent experiment, we have found a very similar pattern for statements that were based on arbitrary information learned by the subjects one day prior to the ERP session [S]. This consistency in ERPs across semantic, self-referential and episodic types of information supports the recent claim that these superficially different kinds of information are represented and accessed in similar ways [l. 19, 311. Recent studies of ERPs during other tasks involving word processing suggests that a

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variety of situations may produce late negative ERP features associated with inappropriate or out-of-context words. This includes words presented in isolation [29,20] and words not rhyming with preceding prime words [24]. A suggestion that the process being indexed by the ERP may be prelexical was made by RUGG [24], who found a similar late negativity to nonrhyming nonwords. The relation among these tasks and ERP components has been discussed elsewhere [ 10,253. Working out the relations among this “family of negatives” and corresponding psychological events should help clarify the processes involved in perceiving and understanding verbal messages. Acknowledgements-The collectlon and analysis.

authors

thank

David Click&erg

and Teera Achariyapaopan

for their assistance

in da:a

REFERENCES distinction. J. exp. Psychol.: Hum. 1. ANDERSON, J. R. and Ross, B. H. Evidence against a semantic-episodic Learn. Mem. 6, 441-446, 1980. potentials during lexical access and antonym 2. BENTIN, S., MCCARTHY, G. and WOOD, C. Event-related processing. Electroenceph. c/in. Neurophysiol. (Proceedings of the Seventh International Congress on Evoked Potentials). in press. mechanisms and semantic categorization. Biol. 3. BODDY. J. and WEINBERG, H. Brain potentials, perceptual Psychol. 12, 43-61, 1981. 4. BROWN, W. S., LEHMANN, D. and MARSH, J. T. Linguistic meaning related to differences in evoked potential topography: English, Swiss-German, and imagined. Brain Lan,q. 11, 34Cb353, 1980. models, methodology, and wavefront reconstruction and 5. CHILDERS. D. G. Evoked responses: Electrogenesis, tracking analysis. Proc. IEEE 65, 611-626, 1977. 6. FISCHLER, 1. and BLOOM, P. A. Automatic and attentional processes in the effects of sentence contexts on word recognition. J. Verb. Learn. Verb. Behar. 18, I-20, 1979. 7. FISCHLER, I., BLOOM. P. A., CHILDERS, D. G., Roucos. S. E. and PERRY. N. W. JR. Brain potentials related to stages of sentence verification. Psychophysiolo,yy 20, 4#-409, 1983. 8. FISCHLER, I., CHILDERS, D. G., ACHARIYAPAOPAN. T. and PERRY, N. W. JR. Brain potentials during sentence verification: Il. Automatic aspects of comprehension. Submitted for publication. (P300) and information 9. FRIEDMAN. D.. SIMSON, R.. RITTER. W. and RAPIN, 1. The late positive component processmg in sentences. Electroenceph. din. Neurophysiol. 38, 255-262. 1975. ofcognitiveprocessing. Ann. Ret.. Psycho/. 34,33-61. 1983. 10. HILLYARD, S. A. and KUTAS, M. Electrophysiology P. ERP correlates of semantic facilitation. Electroenceph. din. Neurophysiol. (Proceedings of 11. HOLCOMB, Seventh International Congress on Evoked Potentials) in press. 12. KUTAS, M. and HILLYARD, S. A. Reading senseless sentences: Brain potentials reflect semantic incongruity. Science 207, 203 -204, 1980.

13. KL’TAS, M. and HILLYARD, S. A. The lateral distribution ofevent-related potentials during sentence processing. Neuropsychologia 20, 579-590, 1982. errors and semantic anomalies. Me,i~. 14. KUTAS. M. and HILLYARD, S. A. Event-related potentials to grammatical Cogn. 11, 539-550, 1983. 15. KUAS, M. LINDAMOOD,T. E. and HILLYARD. S. A. Word expectancy and event-related brain potentials during sentence processing. In Preparatory States and Processes, S. KORNRLUM and J. RFQ~IIN (Editors), pp. 271-237. Lawrence Erlbaum. Hillsdale, New Jersey, 1984. 16. MAKI. R. H. and MCCAUL, K. D. When does self-reference enhance memory’? Paper presented to the Psychonomic Society. Minneapolis, May 1982. reflection of selective attention. P.~ychol. Bull. 92, 17. NAATANEN R. Processing negativity: An evoked-potential 605-640. 198’. brain potentials. Biol. IX. NAATAXEN. R.. SIMPSON, M. and LOVELESS,N. E. Stimulus deviance and event-related Psychol. 14, 53 -98, 1982. 19. NEEL~, J. M. and PAYNE, D. G. A direct comparison of recognition failure rates for recallable names in episodic and semantic memory tests. Mem. Cogn. 11, 161-171, 1983. potential studies of cerebral specialization during 20. NEVILLE, H. J.. KUTAS. M. and SCHMIDT, A. Event-related readmg. J. Studies of normal adults. Brain Lang. 16, 300-315, 1982. 21. POLISH. J.. VANASSE,L. and DONTHIN. E. Category expectancy and the NZOO. Psychophwoh~,uy 18. 142. 19XI. 22. RITTER. W., FORD, J. M., GAILLARD, A. W. K., HARTER, M. R., KUTAS, M.. NAA~rmm. R.. POLISH. J., RENAULT,B. and ROHRBAIJGH,J. Cognition and event-related potentials: The relation of negative potentials and cognitive processes. In Annals of the New York Academy ojsciences, J. COHEN, R. KARREK and P. TEUTING (Editors), in press.

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APPENDIX

I

The facts used for the strong statements were: first name; mtddlename: last name: father’s name; mother’s name: college major: intended occupation; hair texture (straight. wavy. etc.): haircolour: eyecolour: sex: handedness; city and state of birth; city and state of residence; parents’ occupation(s). The facts used for the weak statements were: college class (freshman. etc); age bracket (over 20.30. etc): favourtte sport. food. author. colour and actor; least favoured food and sport; parents’ place of residence: ancestor’s country of origin; largest meal oftheday; timeofretiring(earlyorlate);current modeoftransportatton(bike. caretc.): most recent employment: nearness ofcurrent residence. For statements involving preferences where subject Indicated no Immediate preference they were asked to generate possibilittes (e.g. actors’ names) and select the most appropriate instance (most or least favoured) from that list.