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Time perception dysfunction in psychometric schizotypy
Personality and Individual Differences 40 (2006) 1363–1373 www.elsevier.com/locate/paid
Time perception dysfunction in psychometric schizotypy Kwang-Hyuk Lee *, Joanna K. Dixon, Sean A. Spence, Peter W.R. Woodruff Sheffield Cognition and Neuroimaging Laboratory (SCANLab), Academic Clinical Psychiatry, University of Sheffield, The Longley Centre, Norwood Grange Drive, Sheffield S5 7JT, United Kingdom Received 4 April 2005; received in revised form 11 October 2005; accepted 17 October 2005 Available online 18 January 2006
Abstract Time perception dysfunction has been demonstrated in patients with schizophrenia. The aim of this study was to investigate whether judgements about brief durations of time (62 s) were disturbed in nonclinical high-schizotypal individuals. A total of 101 non-clinical university students completed the Schizotypal Personality Questionnaire (SPQ: Raine, 1991) and a temporal bisection task. In the latter, subjects were required to categorise a probe duration as short or long, based upon the similarity with two referents. All participants completed two temporal bisection conditions, a 400/800 ms condition and a 1000/2000 ms condition. Temporal bisection performance was compared in individuals with total SPQ score below and above one standard deviation from the mean. In addition, the whole sample was used to examine the correlation between bisection performance and schizotypal dimensions (cognitive/perceptual, interpersonal, and disorganisation). Compared to low SPQ scorers, high SPQ scorers judged durations significantly shorter in the 1000/2000 ms condition. Within schizotypy dimensions, both cognitive/perceptual and interpersonal dimensions were significantly associated with the shorter duration judgement. These findings provide evidence for time perception dysfunction among people with schizotypal traits and, therefore, for a continuum between subjects within the general population and clinically defined cases of schizophrenia. 2005 Elsevier Ltd. All rights reserved. Keywords: Time perception; Temporal bisection; Schizophrenia; Schizotypy; Attention; SPQ
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Corresponding author. Tel.: +44 114 226 1501; fax: +44 114 226 1522. E-mail address: k.h.lee@sheffield.ac.uk (K.-H. Lee).
0191-8869/$ - see front matter 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.paid.2005.10.021
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1. Introduction Disordered time sense in people with schizophrenia was described in early phenomenological and psychodynamic literatures (Lewis, 1932; Scott & Clifford, 1948). Experimental studies have found that patients with schizophrenia estimate more time has elapsed than has actually passed (‘overestimation’), although not all studies have demonstrated this association. Intervals that have been used include milliseconds (Rammsayer, 1990), 1 s (Weinstein, Goldstone, & Boardman, 1959), 5–30 s (Pearl & Berg, 1963) and minutes and hours (Rabin, 1957). When administered time estimation tasks repeatedly, patients are consistent in either under- or overestimating intervals (Tysk, 1984). It should be noted, however, that the traditional time perception methods (verbal estimation, production, or reproduction of a given duration) used in the above mentioned studies involve various confounding effects due to estimation strategies (tapping or counting), difference in perceived versus declared estimations, and response delays, along with inconsistencies in terminology applied (Orme, 1969; Zakay, 1990). The temporal bisection task has been used in experimental animals and recently, in humans to investigate temporal judgements (Allan & Gibbon, 1991; Wearden, 1991). The task has also been used in a study of schizophrenia (Elveva˚g et al., 2003) and in a study of individuals at high risk for the disorder (Penney, Meck, Roberts, Gibbon, & Erlenmeyer-Kimling, 2005). In the task, subjects are asked to categorise temporal durations as long or short, with reference to previously learned durations. The mean proportion of ‘‘long’’ responses is plotted against stimulus duration, yielding a ‘‘psychophysical function’’ from which the bisection point (indicating left- or rightward shift of the function) and difference limen (representing the gradient of the function) are determined. Elveva˚g and colleagues used 200 ms and 800 ms as referents in their temporal bisection task. Patients with schizophrenia showed an increase in bisection point value (a rightward shift of psychophysical function) and an increase in difference limen (flattened psychophysical function) (Elveva˚g et al., 2003). Penney and colleagues used relatively long referents (3–6 s) to study individuals who had one parent diagnosed with schizophrenia (Penney et al., 2005). They employed auditory and visual versions of the temporal bisection task, with or without distracters. While there were no group differences in either auditory or visual conditions, the high-risk group showed an increase in difference limen only in the distracter conditions. Phenomenological, cognitive, and psychophysiological studies of non-clinical subjects with schizotypal personality traits have indicated a continuum between subjects from the general population and clinically defined cases of schizophrenia (Claridge, 1997). While the clinical disorder of schizotypal personality is diagnosed on the basis of clinical interview, schizotypal personality traits among the non-clinical population is assessed using self-report scales, hence it is being termed ‘psychometric schizotypy’ (Mason, Claridge, & Jackson, 1995; Raine, 1991). Multivariate analyses of these scales suggest that the symptomatic heterogeneity of schizotypy is akin to that of schizophrenia, namely, cognitive–perceptual, interpersonal, and disorganised features of schizotypy (corresponding to positive, negative, and disorganisation syndromes, respectively) (Rossi & Daneluzzo, 2002). Associations between dimensions of schizotypy and neurocognitive measures suggest that distinct cognitive dysfunctions may underlie each dimension. Both the interpersonal and disorganisation dimensions have been associated with dysfunction in neurocognitive frontal lobe tests such as continuous performance and trail making (Chen, Hsiao, & Lin, 1997; Dinn, Harris, Aycicegi, Greene, & Andover, 2002). The positive features of schizotypy have been related
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to increased and divergent verbal responses (Green & Williams, 1999; Tsakanikos & Claridge, 2005). There are few relevant studies on time perception in schizotypy. Rammsayer (2002) examined the relationship between Eysenck’s personality dimensions (extraversion, neuroticism, and psychoticism) and time perception threshold in the range of 50 ms and 1 s. He found that only psychoticism exhibited greater sensitivity in estimating different intervals of duration around 1 s. On the other hand, Sarkin and colleagues used the Schizotypal Personality Questionnaire (SPQ; Raine, 1991) to assess the schizotypal personality trait (top 10% scorers on the SPQ) (Sarkin, Hillix, Granholm, & Dionisio, 2002). They asked subjects to reproduce various intervals (1, 2, 4, 8, 16, and 25 s) but they did not find any statistical difference between high and low SPQ scorers. Hence, we were interested in investigating whether high scorers on the SPQ show dysfunction in the temporal bisection task and whether different dimensions of schizotypy (assessed on the basis of three underlying SPQ factors) display dysfunction in temporal bisection performance. We focused on judgements of brief durations of time (62 s). Within this time range, some studies have suggested that subcortical and motor functions may be involved in the perception of sub-second durations in an automatic manner, whereas processing of longer durations requires further cognitive processing resources (Lewis & Miall, 2003). In this study, we therefore employed two temporal bisection conditions, a 400/800 ms condition and a 1000/2000 ms condition. It was hypothesised that people with high scores in the SPQ would show dysfunction in the temporal bisection task. Within schizotypal personality dimensions, the cognitive/perceptual and disorganisation factors (equivalent to positive syndrome schizophrenia) would be associated with an early bisection point, whereas the interpersonal factor (akin to negative syndrome schizophrenia) would be related to an increased bisection point.
2. Methods 2.1. Subjects A total of 101 non-clinical students from the University of Sheffield took part in this study. The sample comprised 37 males and 64 females (mean age = 23.5 years; SD = 5.7; range = 18–47 years). All participants reported that they had normal hearing. Written informed consent was obtained from all participants. 2.2. Materials and apparatus All subjects completed the Schizotypal Personality Questionnaire (SPQ; Raine, 1991). The SPQ consists of 74 self-report questions, based upon the features the DSM-III-R schizotypal personality disorder. Higher scores indicate an increased tendency toward schizotypy. Each subject underwent the auditory temporal bisection task. They were tested individually. A power McIntosh computer controlled experimental events and recorded data with Psyscope (Cohen, MacWhinney, Flatt, & Provost, 1993). Responses were made on the right and left buttons of a Psyscope response box. The stimuli used in the bisection tasks were 700-Hz tones produced by the computer speaker.
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2.3. Temporal bisection task All subjects participated in two experimental conditions, a 400/800 ms condition and a 1000/ 2000 ms condition. In the 400/800 ms condition, the referent stimulus was 400 ms for ‘short’ and 800 ms for ‘long’, and stimuli presented during the testing phase were 400, 467, 533, 600, 667, 733, and 800 ms. In the 1000/2000 ms condition, referent ‘short’ and ‘long’ stimuli, each lasted for 1000 ms and 2000 ms, and test stimuli were of 1000, 1170, 1340, 1500, 1660, 1830 and 2000 ms durations. Subjects were trained and tested for each condition separately. In the training phase, subjects heard two referent tones, each being repeated five times. Subsequently, they were trained to press one button on the response box in response to the referent ‘short’ and ‘long’ tones, each of which were presented 10 times. The subject received feedback for incorrect responses. Training was completed if the subject made 100% correct responses for a block of ten trials. In the testing phase, the short and long tones were presented concurrently with five intermediate tones in a randomised order. Subjects completed 4 blocks of 35 trials for each condition. They initiated each block by pressing one of the response buttons. The two conditions were tested separately in a counterbalanced order across subjects, and there was an approximately 5-min break between conditions to avoid interference by the former condition. The total testing lasted approximately 20 min. 2.4. Data analysis 2.4.1. Temporal bisection Data from the last ten of seven tones in each condition were included in the analysis as with other studies in temporal bisection (Wearden & Bray, 2001). In order to examine the bisection point and difference limen, we produced a psychophysical function for each individual. To this end, proportions of ‘long’ responses were calculated for each tone duration for each individual. These psychophysical functions showed a logistic growth (sigmoidal) pattern that increased gradually at first, more rapidly in the middle growth period, and slowly toward the end. Then, sigmoidal curve-fitting analysis was applied using a curve-fitting software (CurveExpert 1.3), to determine the bisection point and difference limen. The bisection point indicates the stimulus duration at which the subject will provide 50% ‘long’ responses. The difference limen is calculated as half the difference between the duration providing 75% and 25% ‘long’ responses. 2.4.2. Relationship between bisection performance and SPQ scores Individuals with total SPQ score below and above 1 standard deviation from the group mean were categorised into low and high scorers, respectively. Between- and within-group differences in the proportion of ‘long’ responses across two conditions were examined a 2 (group) · 2 (condition) mixed design analysis of variance. Between-group differences in bisection point and difference limen in each condition were examined using independent t-tests. To explore the associations between bisection performance and the three SPQ factors, we calculated nine separate sub-scale scores and then added the sub-scale scores to derive the three dimensions: (1) cognitive/perceptual (ideas of reference, odd beliefs/magical thinking, unusual perceptual experiences and paranoid ideation), (2) interpersonal (social anxiety, no close friends, constricted affect, paranoid ideation), and (3) disorganisation (odd behaviour and odd speech) (Raine et al., 1994). The
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association between three dimensions and temporal bisection performance was examined using Pearson correlation analysis, using the whole sample of subjects. To examine the possible confounding effects of age and sex, analysis of covariance (ANCOVA) and Spearman’s partial correlation were used.
3. Results 3.1. Schizotypy group analysis The overall SPQ score was obtained for all 101 subjects, and the total mean score was 17.2 (SD = 10.9, range 1–54). The means and standard deviations for the total SPQ scores of each group were 5.4 (n = 19; SD = 2.3) in low scorers and 34.9 (n = 19; SD = 8.6) in high scorers. The total SPQ scores between the two groups were significantly different (t36 = 13.98, p < 0.001). There were no statistically significant differences in age (25.8 ± 7.4 for the low group and 22.8 ± 4.7 for high group; t36 = 1.47, p < 0.15) or male/female ratio (10 females and 9 males in each group). Fig. 1 shows psychophysical functions for each group in which the proportion of ‘long’ responses was plotted against the stimulus duration for the different stimulus durations. The sigmoidal psychophysical function closely resembles that reported in previous studies (Lustig & Meck, 1
Mean proportion of "long" responses
0.9 0.8 0.7 0.6 0.5 0.4 0.3 Low schizotypy 0.2 High schizotypy 0.1 0 400
600
800
1000
1200
1400
1600
1800
2000
Stimulus duration (milliseconds)
Fig. 1. The mean proportion of long responses plotted against comparison stimuli durations averaged over subjects in each group. Data are shown separately for the 400/800 ms and the 1000/2000 ms conditions for each group. The high SPQ group showed a rightward shift of psychophysical function in the 1000/2000 ms condition, whereas there was no significant group difference in the 400/800 ms condition.
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Table 1 Means and standard deviations of temporal bisection variables for each group Bisection conditions
Low SPQ group (n = 19)
High SPQ group (n = 19)
400/800 condition % Long Bisection point Difference limen
0.50 (0.11) 587.5 (49.6) 92.4 (18.5)
0.54 (0.11) 569.9 (51.9) 85.8 (16.2)
1000/2000 condition % Long Bisection point Difference limen
0.58 (0.09) 1374.1 (97.8) 176.0 (56.7)
0.50 (0.11) 1468 (116.2) 215.0 (40.2)
2001). The mean proportion of ‘long’ response for each condition, shown in Table 1, was entered into a 2 · 2 mixed design analysis of variance, with a between-subject variable of group and a within-subject variable of condition. There was a significant interaction effect between group and condition [F(1,36) = 8.6, p < 0.01]. This interaction was explained by the high SPQ group’s lower proportion of ‘long’ response in the 1000/2000 ms condition [F(1,36) = 8.6, p < 0.05], hence a rightward shift of psychophysical function in high SPQ scorers in the 1000/2000 ms condition. On the other hand, there was no significant group difference in the 400/800 ms condition (see Fig. 1). There was no significant covariation between group differences in long responses and age. Table 1 shows the means and standard deviations of bisection point and difference limen for each condition for each group. An independent sample t-test for bisection point and difference limen showed significant group differences in the 1000/2000 ms condition. High SPQ scorers had increased bisection point value (t36 = 2.70, p < 0.05) and larger difference limen (t36 = 2.42, p < 0.05), compared with low SPQ scorers. When the effect of age was controlled for, the group difference in difference limen was significant at a trend level [F(1,35) = 3.4, p = 0.07]. 3.2. Schizotypy dimensions and temporal bisection To explore the associations between bisection performance and the three SPQ factors, correlation analyses were performed using the whole sample. Four subjects showed a substantial proportion of ‘short’ responses at the longer stimulus durations so that the bisection point obtained was not within the stimulus range. These subjects were excluded from this analysis, and the subjects were not included in the previous group analyses. The results are summarised in Table 2. Table 2 Pearson correlations (n = 97) for factor scores and temporal bisection performance Cognitive/perceptual Bisection 400/800 Difference limen 400/800 Bisection 1000/2000 Difference limen 1000/2000 *
p < 0.05.
*
0.20 0.05 0.22* 0.22*
Interpersonal 0.10 0.08 0.23* 0.14
Disorganisation 0.15 0.09 0.17 0.17
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In the 400/800 ms bisection condition, a significant negative correlation between cognitive/perceptual factor and bisection point was obtained, suggesting an earlier bisection point in this factor. But the association between cognitive/perceptual and 400/800 bisection point became a trend level (r = 0.18, p = 0.07), when age was controlled for using partial correlation analysis. In the 1000/2000 ms bisection condition, both cognitive/perceptual and interpersonal factors were associated with increased bisection point values. The cognitive/perceptual dimension was also related to increased difference limen in this condition, which was non-significant (r = 0.14, p = 0.18) when controlling for age.
4. Discussion The aim of this study was to investigate whether high scorers in the SPQ showed dysfunction in the temporal bisection task and whether different dimensions of schizotypy were correlated with specific dysfunctions of temporal bisection. We found that high SPQ scorers had a significantly increased bisection point (and hence rightward shift of the psychophysical function) in the 1000/2000 ms bisection condition, compared with low SPQ scorers. High SPQ scorers also exhibited a widened difference limen (at a trend level of significance when age was controlled for), compared with low SPQ scorers. Within dimensions of schizotypal personality, both cognitive/ perceptual and interpersonal SPQ dimensions were related to increased bisection point. A trend between the cognitive/perceptual and an earlier bisection point in the 400/800 bisection ms condition was also observed. The more schizotypal, as a group, showed a poor temporal sensitivity as reflected by an increased difference limen; they also exhibited a rightward shift of psychophysical function, in the 1000/2000 ms bisection condition. Decreased temporal sensitivity found in schizophrenia, as indicated by a flattened psychophysical function (Elveva˚g et al., 2003) and suggested by a significant increase in errors committed around the standard duration (Davalos, Kisley, & Ross, 2002), is consistent with our finding. We also observed the rightward shift of psychophysical function in schizotypy, as found in patients with schizophrenia (Elveva˚g et al., 2003). This can be explained by an attention allocation dysfunction (Lejeune, 1998). For example, if attentional resources are limited in temporal processing, a subjective duration becomes shorter; hence, the rightward shift of psychophysical function. It is also possible that the rightward shift is due to limited short-term memory function in this population. If short-term memory function becomes noisy and limited, referent intervals stored in the long-term memory appear to last relatively longer. It is difficult to determine why our findings are limited to the 1000/2000 ms condition. However, there is some evidence that sub-second duration perception is a relatively automatic process, whereas processing of longer durations requires further cognitive processing resources (Lewis & Miall, 2003). It is possible that schizotypy is particularly associated with an abnormality of cognitively controlled temporal processing. With regard to schizotypy dimensions and bisection performance in the 1000/2000 ms condition, both cognitive/perceptual and interpersonal factors were associated with an increased bisection point. Disorganisation also had a non-significant association toward an increased bisection point. Given the notion of a ‘subjective present’ lasting about 2 or 3 s, so that information within this range is automatically integrated into conscious awareness (Mates, Mu¨ller, Radil, & Po¨ppe,
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1994), our results suggest delayed information processing among individuals with any of these schizotypal dimensions of psychopathology. On the other hand, the cognitive/perceptual dimension was associated with an earlier bisection point in the 400/800 ms condition at the trend level. Faster timing performance in this time range has been associated with increased subcortical dopamine function (Meck, 1996). Hence, positive symptoms, in schizotypy, might be associated with elevated subcortical dopaminergic activity (Siever, 1995). Our results are in contrast with Rammsayer’s finding that Eysenck’s psychoticism is related to low time perception threshold (i.e., better performance) for 1 s (Rammsayer, 2002) and to accurate performance in reproducing time intervals ranging 5–40 s (Rammsayer, 1997). One might speculate that the difference in our findings is due to differences in the questionnaires used, in that the Eysenck’s psychoticism scale might be closely related to ‘‘impulsivity and novelty seeking’’ (Zuckerman, Kuhlman, & Camac, 1988), whereas the SPQ is based on the clinical features of schizotypal personality disorder. In view of the finding that high SPQ scorers did not show interval reproduction abnormalities (Sarkin et al., 2002), it would be of interest to test whether temporal bisection task employed in this study is more sensitive in detecting time perception dysfunction in schizotypy than traditional methods such as interval reproduction. Administering these two tasks to the same experimental sample would address this issue. The effect of age mainly altered temporal sensitivity findings in this study, as increased age was associated with decreased sensitivity. This finding is in accordance with previous studies showing decreased temporal sensitivity in older subjects in an attention demanding condition (Lustig & Meck, 2001), reduced accuracy in interval production (Tracy et al., 1998), and increased variability in estimating intervals (Espinosa-Fernandez, Miro, Cano, & Buela-Casal, 2003). There is also evidence that there is a significant age-related improvement in normal children (aged 3, 5, and 8 years) in temporal sensitivity (Droit-Volet & Wearden, 2001). These studies indicate that age is an important variable to consider when examining the possible trait marker status of time perception dysfunction. Neuroimaging studies have indicated that critical neural structures implicated in time perception include the frontal and parietal cortices (lateralised to the right), thalamus, basal ganglia and cerebellum (Lewis & Miall, 2003). The same brain areas have been described as crucial components of the brain network mediating sustained attention (Sarter, Givens, & Bruno, 2001). Poorer performance on sustained attention tasks in schizotypy (Chen et al., 1997) and in schizophrenia (Liu et al., 2002) has frequently been reported. Time perception dysfunction in schizotypy observed in this study and in schizophrenia (Elveva˚g et al., 2003) suggests a possibility that the two processes are closely related to each other in schizophrenia-related psychopathology. One might further speculate the mechanism underlying the association between time perception dysfunction and schizophrenia-related psychopathology. Given that multiple cortical–subcortical brain areas are involved in time perception, it is highly likely that each area of the brain acts as an oscillator. The interaction between these oscillators may provide the means by which the brain stores and recalls time intervals, for instance, via a phase synchronisation mechanism (Miall, 1989; Matell & Meck, 2004). Both first-episode (Symond, Harris, Gordon, & Williams, 2005) and patients with chronic schizophrenia (Lee, Williams, Breakspear, & Gordon, 2003) exhibit dysfunction in the phase synchronisation of brain oscillatory activities. It is possible therefore that time perception dysfunction in schizophrenia may arise from the failure of this phase synchronisation.
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There are some issues to consider in interpreting the results of this study. In our study, we did not collect information about psychoactive drug use (e.g., cannabis), although cannabis could increase time sense and perception (Hicks, Gualtieri, Mayo, & Perez-Reyes, 1984), which was the opposite effect of schizotypy observed in this study. We also could not rule out the possibility that time perception dysfunction observed in this study could partially be attributed to low IQ in some schizotypal individuals, as we did not assess IQ in our study sample. Given that we used a relatively homogeneous university student sample, and that schizotypy is not correlated with IQ (Tsakanikos & Reed, 2003), it is unlikely that IQ was a significant confounding variable in this study. However, it will be of interest in future studies to investigate whether compromised attention or executive functioning is associated with time perception dysfunction in schizotypy. In conclusion, the results of this study indicate that judgements of brief durations of time (62 s) are disturbed in individuals with schizotypal personality traits. Elucidation of the exact nature of time perception dysfunction in schizotypal personality and schizophrenia, however, will require a substantial amount of further research. Investigating time perception in patients with schizophrenia would be required to discover whether they have a specific deficit in the components of the scalar timing model (an internal clock, and memory and decision making processes; Allan, 1998), relative to diverse psychiatric groups. Studies on temporal bisection with neuroimaging tools and neuropsychological assessments could also be beneficial in confirming the underlying neural basis of time perception and identifying the neural pathology involved in schizophrenia. References Allan, L. G. (1998). The influence of the scalar timing model on human timing research. Behavioural Processes, 44, 101–117. Allan, L. G., & Gibbon, J. (1991). Human bisection at the geometric mean. Learning and Motivation, 22, 39–58. Chen, W. J., Hsiao, C. K., & Lin, C. C. (1997). Schizotypy in community samples: the three-factor structure and correlation with sustained attention. Journal of Abnormal Psychology, 106, 649–654. Claridge, G. (1997). Schizotypy: Implications for illness and health. Oxford: Oxford University Press. Cohen, J. D., MacWhinney, B., Flatt, M., & Provost, J. (1993). PsyScope: a new graphic interactive environment for designing psychology experiments. Behavioral Research Methods, Instruments, and Computers, 25, 257–271. Davalos, D. B., Kisley, M. A., & Ross, R. G. (2002). Deficits in auditory and visual temporal perception in schizophrenia. Cognitive Neuropsychiatry, 7, 273–282. Dinn, W. M., Harris, C. L., Aycicegi, A., Greene, P., & Andover, M. S. (2002). Positive and negative schizotypy in a student sample: neurocognitive and clinical correlates. Schizophrenia Research, 56, 171–185. Droit-Volet, S., & Wearden, J. H. (2001). Temporal bisection in children. Journal of Experimental Child Psychology, 80, 142–159. Elveva˚g, B., McCormack, T., Gilbert, A., Brown, G. D., Weinberger, D. R., & Goldberg, T. E. (2003). Duration judgements in patients with schizophrenia. Psychological Medicine, 33, 1249–1261. Espinosa-Fernandez, L., Miro, E., Cano, M., & Buela-Casal, G. (2003). Age-related changes and gender differences in time estimation. Acta Psychologica, 112, 221–232. Green, M. J., & Williams, L. M. (1999). Schizotypy and creativity as effects of reduced cognitive inhibition. Personality and Individual Differences, 27, 263–276. Hicks, R. E., Gualtieri, C. T., Mayo, J. P., Jr., & Perez-Reyes, M. (1984). Cannabis, atropine, and temporal information processing. Neuropsychobiology, 12, 229–237. Lee, K. H., Williams, L. M., Breakspear, M., & Gordon, E. (2003). Synchronous gamma activity: a review and contribution to an integrative neuroscience model of schizophrenia. Brain Research Reviews, 41, 57–78.
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Tsakanikos, E., & Reed, P. (2003). Visuo-spatial processing and dimensions of schizotypy: figure-ground segregation as a function of psychotic-like features. Personality and Individual Differences, 35, 703–712. Tysk, L. (1984). A longitudinal study of time estimation in psychotic disorders. Perceptual and Motor Skills, 59, 779–789. Wearden, J. H. (1991). Human performance on an analogue of an interval bisection task. The Quarterly Journal of Experimental Psychology. B, Comparative and Physiological Psychology, 43, 59–81. Wearden, J. H., & Bray, S. (2001). Scalar timing without reference memory? Episodic temporal generalization and bisection in humans. The Quarterly Journal of Experimental Psychology. B, Comparative and Physiological Psychology, 54, 289–309. Weinstein, A. D., Goldstone, S., & Boardman, W. K. (1959). The effect of recent and remote frames of reference on temporal judgments of schizophrenic patients. Journal of Abnormal and Social Psychology, 57, 241–244. Zakay, D. (1990). The evasive art of subjective time measurement: some methodological dilemmas. In R. A. Block (Ed.), Cognitive models of psychological time (pp. 59–84). Hillsdale: Lawrence Erlbaum Associates. Zuckerman, M., Kuhlman, D. M., & Camac, C. (1988). What lies beyond E and N? Factor analyses of scales believed to measure basic dimensions of personality. Journal of Personality and Social Psychology, 54, 96–107.
Time perception dysfunction in psychometric schizotypy Kwang-Hyuk Lee *, Joanna K. Dixon, Sean A. Spence, Peter W.R. Woodruff Sheffield Cognition and Neuroimaging Laboratory (SCANLab), Academic Clinical Psychiatry, University of Sheffield, The Longley Centre, Norwood Grange Drive, Sheffield S5 7JT, United Kingdom Received 4 April 2005; received in revised form 11 October 2005; accepted 17 October 2005 Available online 18 January 2006
Abstract Time perception dysfunction has been demonstrated in patients with schizophrenia. The aim of this study was to investigate whether judgements about brief durations of time (62 s) were disturbed in nonclinical high-schizotypal individuals. A total of 101 non-clinical university students completed the Schizotypal Personality Questionnaire (SPQ: Raine, 1991) and a temporal bisection task. In the latter, subjects were required to categorise a probe duration as short or long, based upon the similarity with two referents. All participants completed two temporal bisection conditions, a 400/800 ms condition and a 1000/2000 ms condition. Temporal bisection performance was compared in individuals with total SPQ score below and above one standard deviation from the mean. In addition, the whole sample was used to examine the correlation between bisection performance and schizotypal dimensions (cognitive/perceptual, interpersonal, and disorganisation). Compared to low SPQ scorers, high SPQ scorers judged durations significantly shorter in the 1000/2000 ms condition. Within schizotypy dimensions, both cognitive/perceptual and interpersonal dimensions were significantly associated with the shorter duration judgement. These findings provide evidence for time perception dysfunction among people with schizotypal traits and, therefore, for a continuum between subjects within the general population and clinically defined cases of schizophrenia. 2005 Elsevier Ltd. All rights reserved. Keywords: Time perception; Temporal bisection; Schizophrenia; Schizotypy; Attention; SPQ
*
Corresponding author. Tel.: +44 114 226 1501; fax: +44 114 226 1522. E-mail address: k.h.lee@sheffield.ac.uk (K.-H. Lee).
0191-8869/$ - see front matter 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.paid.2005.10.021
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1. Introduction Disordered time sense in people with schizophrenia was described in early phenomenological and psychodynamic literatures (Lewis, 1932; Scott & Clifford, 1948). Experimental studies have found that patients with schizophrenia estimate more time has elapsed than has actually passed (‘overestimation’), although not all studies have demonstrated this association. Intervals that have been used include milliseconds (Rammsayer, 1990), 1 s (Weinstein, Goldstone, & Boardman, 1959), 5–30 s (Pearl & Berg, 1963) and minutes and hours (Rabin, 1957). When administered time estimation tasks repeatedly, patients are consistent in either under- or overestimating intervals (Tysk, 1984). It should be noted, however, that the traditional time perception methods (verbal estimation, production, or reproduction of a given duration) used in the above mentioned studies involve various confounding effects due to estimation strategies (tapping or counting), difference in perceived versus declared estimations, and response delays, along with inconsistencies in terminology applied (Orme, 1969; Zakay, 1990). The temporal bisection task has been used in experimental animals and recently, in humans to investigate temporal judgements (Allan & Gibbon, 1991; Wearden, 1991). The task has also been used in a study of schizophrenia (Elveva˚g et al., 2003) and in a study of individuals at high risk for the disorder (Penney, Meck, Roberts, Gibbon, & Erlenmeyer-Kimling, 2005). In the task, subjects are asked to categorise temporal durations as long or short, with reference to previously learned durations. The mean proportion of ‘‘long’’ responses is plotted against stimulus duration, yielding a ‘‘psychophysical function’’ from which the bisection point (indicating left- or rightward shift of the function) and difference limen (representing the gradient of the function) are determined. Elveva˚g and colleagues used 200 ms and 800 ms as referents in their temporal bisection task. Patients with schizophrenia showed an increase in bisection point value (a rightward shift of psychophysical function) and an increase in difference limen (flattened psychophysical function) (Elveva˚g et al., 2003). Penney and colleagues used relatively long referents (3–6 s) to study individuals who had one parent diagnosed with schizophrenia (Penney et al., 2005). They employed auditory and visual versions of the temporal bisection task, with or without distracters. While there were no group differences in either auditory or visual conditions, the high-risk group showed an increase in difference limen only in the distracter conditions. Phenomenological, cognitive, and psychophysiological studies of non-clinical subjects with schizotypal personality traits have indicated a continuum between subjects from the general population and clinically defined cases of schizophrenia (Claridge, 1997). While the clinical disorder of schizotypal personality is diagnosed on the basis of clinical interview, schizotypal personality traits among the non-clinical population is assessed using self-report scales, hence it is being termed ‘psychometric schizotypy’ (Mason, Claridge, & Jackson, 1995; Raine, 1991). Multivariate analyses of these scales suggest that the symptomatic heterogeneity of schizotypy is akin to that of schizophrenia, namely, cognitive–perceptual, interpersonal, and disorganised features of schizotypy (corresponding to positive, negative, and disorganisation syndromes, respectively) (Rossi & Daneluzzo, 2002). Associations between dimensions of schizotypy and neurocognitive measures suggest that distinct cognitive dysfunctions may underlie each dimension. Both the interpersonal and disorganisation dimensions have been associated with dysfunction in neurocognitive frontal lobe tests such as continuous performance and trail making (Chen, Hsiao, & Lin, 1997; Dinn, Harris, Aycicegi, Greene, & Andover, 2002). The positive features of schizotypy have been related
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to increased and divergent verbal responses (Green & Williams, 1999; Tsakanikos & Claridge, 2005). There are few relevant studies on time perception in schizotypy. Rammsayer (2002) examined the relationship between Eysenck’s personality dimensions (extraversion, neuroticism, and psychoticism) and time perception threshold in the range of 50 ms and 1 s. He found that only psychoticism exhibited greater sensitivity in estimating different intervals of duration around 1 s. On the other hand, Sarkin and colleagues used the Schizotypal Personality Questionnaire (SPQ; Raine, 1991) to assess the schizotypal personality trait (top 10% scorers on the SPQ) (Sarkin, Hillix, Granholm, & Dionisio, 2002). They asked subjects to reproduce various intervals (1, 2, 4, 8, 16, and 25 s) but they did not find any statistical difference between high and low SPQ scorers. Hence, we were interested in investigating whether high scorers on the SPQ show dysfunction in the temporal bisection task and whether different dimensions of schizotypy (assessed on the basis of three underlying SPQ factors) display dysfunction in temporal bisection performance. We focused on judgements of brief durations of time (62 s). Within this time range, some studies have suggested that subcortical and motor functions may be involved in the perception of sub-second durations in an automatic manner, whereas processing of longer durations requires further cognitive processing resources (Lewis & Miall, 2003). In this study, we therefore employed two temporal bisection conditions, a 400/800 ms condition and a 1000/2000 ms condition. It was hypothesised that people with high scores in the SPQ would show dysfunction in the temporal bisection task. Within schizotypal personality dimensions, the cognitive/perceptual and disorganisation factors (equivalent to positive syndrome schizophrenia) would be associated with an early bisection point, whereas the interpersonal factor (akin to negative syndrome schizophrenia) would be related to an increased bisection point.
2. Methods 2.1. Subjects A total of 101 non-clinical students from the University of Sheffield took part in this study. The sample comprised 37 males and 64 females (mean age = 23.5 years; SD = 5.7; range = 18–47 years). All participants reported that they had normal hearing. Written informed consent was obtained from all participants. 2.2. Materials and apparatus All subjects completed the Schizotypal Personality Questionnaire (SPQ; Raine, 1991). The SPQ consists of 74 self-report questions, based upon the features the DSM-III-R schizotypal personality disorder. Higher scores indicate an increased tendency toward schizotypy. Each subject underwent the auditory temporal bisection task. They were tested individually. A power McIntosh computer controlled experimental events and recorded data with Psyscope (Cohen, MacWhinney, Flatt, & Provost, 1993). Responses were made on the right and left buttons of a Psyscope response box. The stimuli used in the bisection tasks were 700-Hz tones produced by the computer speaker.
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2.3. Temporal bisection task All subjects participated in two experimental conditions, a 400/800 ms condition and a 1000/ 2000 ms condition. In the 400/800 ms condition, the referent stimulus was 400 ms for ‘short’ and 800 ms for ‘long’, and stimuli presented during the testing phase were 400, 467, 533, 600, 667, 733, and 800 ms. In the 1000/2000 ms condition, referent ‘short’ and ‘long’ stimuli, each lasted for 1000 ms and 2000 ms, and test stimuli were of 1000, 1170, 1340, 1500, 1660, 1830 and 2000 ms durations. Subjects were trained and tested for each condition separately. In the training phase, subjects heard two referent tones, each being repeated five times. Subsequently, they were trained to press one button on the response box in response to the referent ‘short’ and ‘long’ tones, each of which were presented 10 times. The subject received feedback for incorrect responses. Training was completed if the subject made 100% correct responses for a block of ten trials. In the testing phase, the short and long tones were presented concurrently with five intermediate tones in a randomised order. Subjects completed 4 blocks of 35 trials for each condition. They initiated each block by pressing one of the response buttons. The two conditions were tested separately in a counterbalanced order across subjects, and there was an approximately 5-min break between conditions to avoid interference by the former condition. The total testing lasted approximately 20 min. 2.4. Data analysis 2.4.1. Temporal bisection Data from the last ten of seven tones in each condition were included in the analysis as with other studies in temporal bisection (Wearden & Bray, 2001). In order to examine the bisection point and difference limen, we produced a psychophysical function for each individual. To this end, proportions of ‘long’ responses were calculated for each tone duration for each individual. These psychophysical functions showed a logistic growth (sigmoidal) pattern that increased gradually at first, more rapidly in the middle growth period, and slowly toward the end. Then, sigmoidal curve-fitting analysis was applied using a curve-fitting software (CurveExpert 1.3), to determine the bisection point and difference limen. The bisection point indicates the stimulus duration at which the subject will provide 50% ‘long’ responses. The difference limen is calculated as half the difference between the duration providing 75% and 25% ‘long’ responses. 2.4.2. Relationship between bisection performance and SPQ scores Individuals with total SPQ score below and above 1 standard deviation from the group mean were categorised into low and high scorers, respectively. Between- and within-group differences in the proportion of ‘long’ responses across two conditions were examined a 2 (group) · 2 (condition) mixed design analysis of variance. Between-group differences in bisection point and difference limen in each condition were examined using independent t-tests. To explore the associations between bisection performance and the three SPQ factors, we calculated nine separate sub-scale scores and then added the sub-scale scores to derive the three dimensions: (1) cognitive/perceptual (ideas of reference, odd beliefs/magical thinking, unusual perceptual experiences and paranoid ideation), (2) interpersonal (social anxiety, no close friends, constricted affect, paranoid ideation), and (3) disorganisation (odd behaviour and odd speech) (Raine et al., 1994). The
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association between three dimensions and temporal bisection performance was examined using Pearson correlation analysis, using the whole sample of subjects. To examine the possible confounding effects of age and sex, analysis of covariance (ANCOVA) and Spearman’s partial correlation were used.
3. Results 3.1. Schizotypy group analysis The overall SPQ score was obtained for all 101 subjects, and the total mean score was 17.2 (SD = 10.9, range 1–54). The means and standard deviations for the total SPQ scores of each group were 5.4 (n = 19; SD = 2.3) in low scorers and 34.9 (n = 19; SD = 8.6) in high scorers. The total SPQ scores between the two groups were significantly different (t36 = 13.98, p < 0.001). There were no statistically significant differences in age (25.8 ± 7.4 for the low group and 22.8 ± 4.7 for high group; t36 = 1.47, p < 0.15) or male/female ratio (10 females and 9 males in each group). Fig. 1 shows psychophysical functions for each group in which the proportion of ‘long’ responses was plotted against the stimulus duration for the different stimulus durations. The sigmoidal psychophysical function closely resembles that reported in previous studies (Lustig & Meck, 1
Mean proportion of "long" responses
0.9 0.8 0.7 0.6 0.5 0.4 0.3 Low schizotypy 0.2 High schizotypy 0.1 0 400
600
800
1000
1200
1400
1600
1800
2000
Stimulus duration (milliseconds)
Fig. 1. The mean proportion of long responses plotted against comparison stimuli durations averaged over subjects in each group. Data are shown separately for the 400/800 ms and the 1000/2000 ms conditions for each group. The high SPQ group showed a rightward shift of psychophysical function in the 1000/2000 ms condition, whereas there was no significant group difference in the 400/800 ms condition.
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Table 1 Means and standard deviations of temporal bisection variables for each group Bisection conditions
Low SPQ group (n = 19)
High SPQ group (n = 19)
400/800 condition % Long Bisection point Difference limen
0.50 (0.11) 587.5 (49.6) 92.4 (18.5)
0.54 (0.11) 569.9 (51.9) 85.8 (16.2)
1000/2000 condition % Long Bisection point Difference limen
0.58 (0.09) 1374.1 (97.8) 176.0 (56.7)
0.50 (0.11) 1468 (116.2) 215.0 (40.2)
2001). The mean proportion of ‘long’ response for each condition, shown in Table 1, was entered into a 2 · 2 mixed design analysis of variance, with a between-subject variable of group and a within-subject variable of condition. There was a significant interaction effect between group and condition [F(1,36) = 8.6, p < 0.01]. This interaction was explained by the high SPQ group’s lower proportion of ‘long’ response in the 1000/2000 ms condition [F(1,36) = 8.6, p < 0.05], hence a rightward shift of psychophysical function in high SPQ scorers in the 1000/2000 ms condition. On the other hand, there was no significant group difference in the 400/800 ms condition (see Fig. 1). There was no significant covariation between group differences in long responses and age. Table 1 shows the means and standard deviations of bisection point and difference limen for each condition for each group. An independent sample t-test for bisection point and difference limen showed significant group differences in the 1000/2000 ms condition. High SPQ scorers had increased bisection point value (t36 = 2.70, p < 0.05) and larger difference limen (t36 = 2.42, p < 0.05), compared with low SPQ scorers. When the effect of age was controlled for, the group difference in difference limen was significant at a trend level [F(1,35) = 3.4, p = 0.07]. 3.2. Schizotypy dimensions and temporal bisection To explore the associations between bisection performance and the three SPQ factors, correlation analyses were performed using the whole sample. Four subjects showed a substantial proportion of ‘short’ responses at the longer stimulus durations so that the bisection point obtained was not within the stimulus range. These subjects were excluded from this analysis, and the subjects were not included in the previous group analyses. The results are summarised in Table 2. Table 2 Pearson correlations (n = 97) for factor scores and temporal bisection performance Cognitive/perceptual Bisection 400/800 Difference limen 400/800 Bisection 1000/2000 Difference limen 1000/2000 *
p < 0.05.
*
0.20 0.05 0.22* 0.22*
Interpersonal 0.10 0.08 0.23* 0.14
Disorganisation 0.15 0.09 0.17 0.17
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In the 400/800 ms bisection condition, a significant negative correlation between cognitive/perceptual factor and bisection point was obtained, suggesting an earlier bisection point in this factor. But the association between cognitive/perceptual and 400/800 bisection point became a trend level (r = 0.18, p = 0.07), when age was controlled for using partial correlation analysis. In the 1000/2000 ms bisection condition, both cognitive/perceptual and interpersonal factors were associated with increased bisection point values. The cognitive/perceptual dimension was also related to increased difference limen in this condition, which was non-significant (r = 0.14, p = 0.18) when controlling for age.
4. Discussion The aim of this study was to investigate whether high scorers in the SPQ showed dysfunction in the temporal bisection task and whether different dimensions of schizotypy were correlated with specific dysfunctions of temporal bisection. We found that high SPQ scorers had a significantly increased bisection point (and hence rightward shift of the psychophysical function) in the 1000/2000 ms bisection condition, compared with low SPQ scorers. High SPQ scorers also exhibited a widened difference limen (at a trend level of significance when age was controlled for), compared with low SPQ scorers. Within dimensions of schizotypal personality, both cognitive/ perceptual and interpersonal SPQ dimensions were related to increased bisection point. A trend between the cognitive/perceptual and an earlier bisection point in the 400/800 bisection ms condition was also observed. The more schizotypal, as a group, showed a poor temporal sensitivity as reflected by an increased difference limen; they also exhibited a rightward shift of psychophysical function, in the 1000/2000 ms bisection condition. Decreased temporal sensitivity found in schizophrenia, as indicated by a flattened psychophysical function (Elveva˚g et al., 2003) and suggested by a significant increase in errors committed around the standard duration (Davalos, Kisley, & Ross, 2002), is consistent with our finding. We also observed the rightward shift of psychophysical function in schizotypy, as found in patients with schizophrenia (Elveva˚g et al., 2003). This can be explained by an attention allocation dysfunction (Lejeune, 1998). For example, if attentional resources are limited in temporal processing, a subjective duration becomes shorter; hence, the rightward shift of psychophysical function. It is also possible that the rightward shift is due to limited short-term memory function in this population. If short-term memory function becomes noisy and limited, referent intervals stored in the long-term memory appear to last relatively longer. It is difficult to determine why our findings are limited to the 1000/2000 ms condition. However, there is some evidence that sub-second duration perception is a relatively automatic process, whereas processing of longer durations requires further cognitive processing resources (Lewis & Miall, 2003). It is possible that schizotypy is particularly associated with an abnormality of cognitively controlled temporal processing. With regard to schizotypy dimensions and bisection performance in the 1000/2000 ms condition, both cognitive/perceptual and interpersonal factors were associated with an increased bisection point. Disorganisation also had a non-significant association toward an increased bisection point. Given the notion of a ‘subjective present’ lasting about 2 or 3 s, so that information within this range is automatically integrated into conscious awareness (Mates, Mu¨ller, Radil, & Po¨ppe,
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1994), our results suggest delayed information processing among individuals with any of these schizotypal dimensions of psychopathology. On the other hand, the cognitive/perceptual dimension was associated with an earlier bisection point in the 400/800 ms condition at the trend level. Faster timing performance in this time range has been associated with increased subcortical dopamine function (Meck, 1996). Hence, positive symptoms, in schizotypy, might be associated with elevated subcortical dopaminergic activity (Siever, 1995). Our results are in contrast with Rammsayer’s finding that Eysenck’s psychoticism is related to low time perception threshold (i.e., better performance) for 1 s (Rammsayer, 2002) and to accurate performance in reproducing time intervals ranging 5–40 s (Rammsayer, 1997). One might speculate that the difference in our findings is due to differences in the questionnaires used, in that the Eysenck’s psychoticism scale might be closely related to ‘‘impulsivity and novelty seeking’’ (Zuckerman, Kuhlman, & Camac, 1988), whereas the SPQ is based on the clinical features of schizotypal personality disorder. In view of the finding that high SPQ scorers did not show interval reproduction abnormalities (Sarkin et al., 2002), it would be of interest to test whether temporal bisection task employed in this study is more sensitive in detecting time perception dysfunction in schizotypy than traditional methods such as interval reproduction. Administering these two tasks to the same experimental sample would address this issue. The effect of age mainly altered temporal sensitivity findings in this study, as increased age was associated with decreased sensitivity. This finding is in accordance with previous studies showing decreased temporal sensitivity in older subjects in an attention demanding condition (Lustig & Meck, 2001), reduced accuracy in interval production (Tracy et al., 1998), and increased variability in estimating intervals (Espinosa-Fernandez, Miro, Cano, & Buela-Casal, 2003). There is also evidence that there is a significant age-related improvement in normal children (aged 3, 5, and 8 years) in temporal sensitivity (Droit-Volet & Wearden, 2001). These studies indicate that age is an important variable to consider when examining the possible trait marker status of time perception dysfunction. Neuroimaging studies have indicated that critical neural structures implicated in time perception include the frontal and parietal cortices (lateralised to the right), thalamus, basal ganglia and cerebellum (Lewis & Miall, 2003). The same brain areas have been described as crucial components of the brain network mediating sustained attention (Sarter, Givens, & Bruno, 2001). Poorer performance on sustained attention tasks in schizotypy (Chen et al., 1997) and in schizophrenia (Liu et al., 2002) has frequently been reported. Time perception dysfunction in schizotypy observed in this study and in schizophrenia (Elveva˚g et al., 2003) suggests a possibility that the two processes are closely related to each other in schizophrenia-related psychopathology. One might further speculate the mechanism underlying the association between time perception dysfunction and schizophrenia-related psychopathology. Given that multiple cortical–subcortical brain areas are involved in time perception, it is highly likely that each area of the brain acts as an oscillator. The interaction between these oscillators may provide the means by which the brain stores and recalls time intervals, for instance, via a phase synchronisation mechanism (Miall, 1989; Matell & Meck, 2004). Both first-episode (Symond, Harris, Gordon, & Williams, 2005) and patients with chronic schizophrenia (Lee, Williams, Breakspear, & Gordon, 2003) exhibit dysfunction in the phase synchronisation of brain oscillatory activities. It is possible therefore that time perception dysfunction in schizophrenia may arise from the failure of this phase synchronisation.
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There are some issues to consider in interpreting the results of this study. In our study, we did not collect information about psychoactive drug use (e.g., cannabis), although cannabis could increase time sense and perception (Hicks, Gualtieri, Mayo, & Perez-Reyes, 1984), which was the opposite effect of schizotypy observed in this study. We also could not rule out the possibility that time perception dysfunction observed in this study could partially be attributed to low IQ in some schizotypal individuals, as we did not assess IQ in our study sample. Given that we used a relatively homogeneous university student sample, and that schizotypy is not correlated with IQ (Tsakanikos & Reed, 2003), it is unlikely that IQ was a significant confounding variable in this study. However, it will be of interest in future studies to investigate whether compromised attention or executive functioning is associated with time perception dysfunction in schizotypy. In conclusion, the results of this study indicate that judgements of brief durations of time (62 s) are disturbed in individuals with schizotypal personality traits. Elucidation of the exact nature of time perception dysfunction in schizotypal personality and schizophrenia, however, will require a substantial amount of further research. Investigating time perception in patients with schizophrenia would be required to discover whether they have a specific deficit in the components of the scalar timing model (an internal clock, and memory and decision making processes; Allan, 1998), relative to diverse psychiatric groups. Studies on temporal bisection with neuroimaging tools and neuropsychological assessments could also be beneficial in confirming the underlying neural basis of time perception and identifying the neural pathology involved in schizophrenia. References Allan, L. G. (1998). The influence of the scalar timing model on human timing research. Behavioural Processes, 44, 101–117. Allan, L. G., & Gibbon, J. (1991). Human bisection at the geometric mean. Learning and Motivation, 22, 39–58. Chen, W. J., Hsiao, C. K., & Lin, C. C. (1997). Schizotypy in community samples: the three-factor structure and correlation with sustained attention. Journal of Abnormal Psychology, 106, 649–654. Claridge, G. (1997). Schizotypy: Implications for illness and health. Oxford: Oxford University Press. Cohen, J. D., MacWhinney, B., Flatt, M., & Provost, J. (1993). PsyScope: a new graphic interactive environment for designing psychology experiments. Behavioral Research Methods, Instruments, and Computers, 25, 257–271. Davalos, D. B., Kisley, M. A., & Ross, R. G. (2002). Deficits in auditory and visual temporal perception in schizophrenia. Cognitive Neuropsychiatry, 7, 273–282. Dinn, W. M., Harris, C. L., Aycicegi, A., Greene, P., & Andover, M. S. (2002). Positive and negative schizotypy in a student sample: neurocognitive and clinical correlates. Schizophrenia Research, 56, 171–185. Droit-Volet, S., & Wearden, J. H. (2001). Temporal bisection in children. Journal of Experimental Child Psychology, 80, 142–159. Elveva˚g, B., McCormack, T., Gilbert, A., Brown, G. D., Weinberger, D. R., & Goldberg, T. E. (2003). Duration judgements in patients with schizophrenia. Psychological Medicine, 33, 1249–1261. Espinosa-Fernandez, L., Miro, E., Cano, M., & Buela-Casal, G. (2003). Age-related changes and gender differences in time estimation. Acta Psychologica, 112, 221–232. Green, M. J., & Williams, L. M. (1999). Schizotypy and creativity as effects of reduced cognitive inhibition. Personality and Individual Differences, 27, 263–276. Hicks, R. E., Gualtieri, C. T., Mayo, J. P., Jr., & Perez-Reyes, M. (1984). Cannabis, atropine, and temporal information processing. Neuropsychobiology, 12, 229–237. Lee, K. H., Williams, L. M., Breakspear, M., & Gordon, E. (2003). Synchronous gamma activity: a review and contribution to an integrative neuroscience model of schizophrenia. Brain Research Reviews, 41, 57–78.
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