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Schizophrenia patients are impaired in recognition task but more for intentionality than physical causality
Consciousness and Cognition 67 (2019) 98–107
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Consciousness and Cognition journal homepage: www.elsevier.com/locate/concog
Schizophrenia patients are impaired in recognition task but more for intentionality than physical causality
T
Ali Okera, , Sarah Del Goletod, Alice Vignesb, Christine Passerieuxb,c, Paul Rouxb,c, Eric-Brunet Gouetb,c ⁎
a
Laboratoire C2S (Cognition, Santé, Société), EA 6291, Department ESPE, Université de Reims Champagne-Ardenne, Reims, France Laboratoire HANDIReSP (EA4047), Université de Versailles Saint-Quentin-En-Yvelines, Versailles, France c Service de Psychiatrie de l’Adulte et d’Addictologie, Centre Hospitalier de Versailles, Le Chesnay, France d Laboratoire de Psychopathologie et Neuropsychologie (EA 2027), Université Paris Lumières, Paris 8, St. Denis, France b
ABSTRACT
It is now largely accepted that patients with schizophrenia have a deficit to attribute mental states to others, such as intentions, needs and motivations but also to perform memory tasks. According to one hypothesis, these impairments may be due to an early visual attention deficit during the encounter of social stimuli. Another hypothesis posits a robust correlation between intention attribution and autobiographical memory that results in impaired recollection of past events making it difficult to infer others’ intentions. In sum, the link between intention attribution and encoding process is yet to be explored in patients with schizophrenia. The objective of the present study is to contribute to this debate by investigating whether schizophrenic patients’ recollection can be boosted by an attentional cueing on relevant information and to determine the influence of two different situational contexts: attribution of intentions or physical causality scripts. By using a supraliminal attentional cue, we made relevant areas of our material more salient across two conditions: attribution of intentions (AI) and physical causality with human characters (PCCH). The results confirmed expected deficit of explicit memory in schizophrenia patients while attentional cueing on relevant areas for intentions attribution or physical causality had no effect on recollection in any group. However, it seems that the recollection performances are highly influenced by the nature of intentions attribution. Also, it is the first time that the material used for the assessment of theory of mind performances has been tested with a recognition test.
1. Introduction Social cognition represents a high priority area for the study of schizophrenia due to its strong association with the functional outcome (Couture, Penn, & Roberts, 2006; Fett, Viechtbauer, Penn, van Os, & Krabbendam, 2011; Lam, Raine, & Lee, 2014; MartínezDomínguez, Penadés, Segura, González-Rodríguez, & Catalán, 2015). Among the different social cognitive abilities, theory of mind (ToM) refers to the capacity to infer mental states (i.e. intentions, beliefs, needs…) in order to understand and predict others’ behavior (Premack & Woodruff, 1978). A consensus emerged during the past decades regarding ToM impairment in patients with schizophrenia (for reviews, see Brüne, 2005; Kronbichler, Tschernegg, Martin, Schurz, & Kronbichler, 2017; Sprong, Schothorst, Vos, Hox, & Van Engeland, 2007). In general, theory of mind in schizophrenia is tested using verbal (Corcoran & Frith, 2003; Janssen, Krabbendam, Jolles, & Van Os, 2003) or non-verbal tasks based on successive comic strips depicting sequences of actions (Sarfati & Hardy-Baylé, 1999; Langdon, Coltheart, & Ward, 2006; Vistoli, Brunet-Gouet, Lemoalle, Hardy-Baylé, & Passerieux, 2011) in which participants are generally asked to decide whether the last picture is congruent or not regarding the preceding three images. One of the comic strips paradigm available having a control condition is based on the work of Brunet, Sarfati, Hardy-Baylé, and Decety (2000). This material involves a condition with physical causality (reasoning about the weight, location, speed, and the physical
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Corresponding author. E-mail address: [email protected] (A. Oker).
https://doi.org/10.1016/j.concog.2018.11.007 Received 27 December 2017; Received in revised form 24 October 2018; Accepted 25 November 2018 1053-8100/ © 2018 Elsevier Inc. All rights reserved.
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properties of objects but in the presence of a person) and a condition with an attribution intention towards a person (reasoning about the need, belief or desire of a person). Studies using this material revealed an impaired theory of mind performance in patients with schizophrenia (Bara, Ciaramidaro, Walter, & Adenzato, 2011; Roux, Brunet-Gouet, Passerieux, & Ramus, 2016; Vistoli et al., 2011, 2015). It has also been reported that patients with schizophrenia have poor performance in several memory tasks (Reichenberg & Harvey, 2007) and particularly in episodic memory (Cirillo & Seidman, 2003; Rushe, Woodruff, Murray, & Morris, 1999). More precisely, patients seem to have difficulties in two critical aspects of episodic memory (i.e. conscious recollection and autobiographical memory, for a review see Danion, Huron, Vidailhet, & Berna, 2007). Concerning episodic memory, clusters of arguments tend to show an overlap between autobiographical memory and theory of mind (Corcoran & Frith, 2003; Dimaggio, Salvatore, Popolo, & Lysaker, 2012; Perner, 2000; Rabin & Rosenbaum, 2012; Rabin, Gilboa, Stuss, Mar, & Rosenbaum, 2010; Spreng & Grady, 2010; Spreng, Mar, & Kim, 2009; Suddendorf & Corballis, 1997). For example, Corcoran and Frith (2003) found a robust relationship1 between autobiographical memory and theory of mind performances (as measured with the hinting task2) in patients with schizophrenia. Moreover, the authors found out that participants with schizophrenia tended to recollect odd or negative events when they were asked to answer standard autobiographical memory questions. The authors suggested that patients’ poor recollection of events could mislead them when attributing other’s intentions (Corcoran & Frith, 2003). Recent neuroimaging studies concur with this overlap (Spreng & Grady, 2010). According to this fMRI study, autobiographical memory, prospection and theory of mind shared a common pattern of brain activity including midline structures in the frontal and parietal lobes operating within the default mode network (the DMN, for a review see Mothersill, Knee-Zaska, & Donohoe, 2016). In line with these results, in a large meta-analysis conducted on more than 30 neuroimaging studies, Spreng et al. (2009) concluded that even if autobiographical memory and theory of mind have been previously studied as distinct, these two cognitive processes exhibited extensive functional overlap. Indeed, this meta-analyse showed that there is a convergence between theory of mind and autobiographical memory in prefrontal area (rostral anterior cingulate gyrus), in medial temporal area (parahippocampal cortex and amygdala), in medial parietal lobe (precuneus and posterior cingulate cortex) and in lateral area (jonction temporo-parietal junction and superior temporal sulcus). However, according to another hypothesis, theory of mind impairments may also be due to an early visual attention deficit, which could alter the selection and the process of relevant social cues to attribute intentions to others (Bjorkquist & Herbener, 2013; Rassovsky, Green, Nuechterlein, Breitmeyer, & Mintz, 2004; Sergi, Rassovsky, Nuechterlein, & Green, 2006). Generally, these works focused on visual perception of emotionally charged images for less than 100 ms and suggested that impaired social perception appears to be influenced by abnormalities in early aspect of visual processing in individuals with schizophrenia. For instance, regarding social perception, Maher, Mashhoon, Ekstrom, Lukas, and Chen (2016) have shown that N1703 amplitudes didn’t differ between faces and non-socially relevant stimuli in patients with schizophrenia. Others studies also suggested a connection between early visual processes and social perceptual deficits in schizophrenia (Rassovsky, Horan, Lee, Sergi, & Green, 2011; Sergi & Green, 2003). According to Rassovsky et al. (2011) because social perception consists of fast visual identification of socially relevant cues (facial expressions, gaze directions etc…), “It is therefore possible that early visual perceptual deficits, … impose limits on the amount of visual information that can be processed at a given time, which in turn could reduce one’s ability to process socially relevant visual information and result in failures to identify briefly available social cues” (pg. 294). Moreover, Roux et al. (2016) shed light on the time course of social context processing during intention attribution in patients with schizophrenia. In their study, the authors evaluated ToM performances using comic strips (with intention attribution and physical reasoning conditions) while performing eye tracking recording in order to assess processing time dedicated to intention attribution. They stated that compared to control subjects, patients with schizophrenia were slower in intention attribution but not in physical reasoning. In conclusion, authors highlighted that schizophrenia was characterized by a delay in intention attribution related to a slowdown of social context processing. Based on their findings, Sergi and Green (2003) and Sergi et al. (2006) also suggested an association between early visual processes and social perceptual deficits in schizophrenia. In Sergi et al. (2006) authors conducted a study of structural equation modelling to correlate early visual processing (evaluated by visually masked stimulus of 12.5 ms), social perception and functional status of patients. Results showed that early visual processing was highly correlated (via multiple regression analysis) to social perception compared to functional status in patients with schizophrenia. It can be proposed that if theory of mind impairments are related to deficits of early visual attention, these combined disorders should also impact long-term memory. The idea of an intimate relationship between memory and attention has been widely defended by Cowan and Conway. According to the initial description of Cowan (1998), “there is an intricate relation between memory and attention in a model of processing” (pg. 27). In his model, a central executive module (similar to Baddeley’s model, 1986) directs attention to the stimulus involved in a cognitive task, and provides a processing ‘in’ (write) and ‘out’ (read) contents toward what’s called a ‘focus of attention’ module. This focus of attention works as a magnifying glass in the activated part of the short-term memory and thus, writes and reads contents of the short-term memory. According to Cowan, this process provides a long-term storage of some features automatically. However, attentional processing required by the task results in more elaborate encoding which is critical for voluntary retrieval later on (Cowan, 2011). Thus, the more intense the attention, the easier the retrieval. On the other hand, Conway (2001) has proposed a model based on a constructivist view of autobiographical memory (Piolino, Desgranges, Eustache, & Eustache, 2000). According to Conway (2001), when we are retrieving a memory, the retrieved information
1
By the means of Pearson’s r excluding logical memory and IQ. 10 short vignettes to read in which it’s presented an interaction between two characters. “All of these end with one of the characters dropping a very obvious hint. The subject is asked what the character really meant when he/she said this” (Corcoran, Mercer, & Frith, 1995). 3 The N170 ERP component is a right hemisphere lateralized negativity peaking around 170 ms after stimulus-onset, and a reliable marker of face detection. 2
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is not just the information itself; it is more likely a construct involving past experiences and a model of self-integrity and coherence. Thus, the retrieval process depends on the context, prior experiences, the relevance of the task for the subject and the personal involvement of the subject to the stimulus. 2. Present work The aim of this study is to contribute to the debate on whether the theory of mind impairment is due to a bottom-up cognitive process such as early visual attention deficit. In cognitive psychology, bottom-up processing (or data-driven processing) can be defined by a cognitive task which is triggered from the perception of the stimulus or the sensory-motor data itself. On the contrary, top-down processing is required for a cognitive task which need prior knowledge, contextual information and inferences already stored in the system. In 1970, this distinction has first appeared in the field of visual perception (Gregory, 1970) then it became a reference for other cognitive tasks and information processing involving central and peripheral nervous system. We propose an experiment in which early perceptual cues are used on comic strip series to evaluate theory of mind performance on schizophrenia patients’ recollection. The general idea is to verify whether by triggering experimentally a bottom-up process provided by a supraliminal cue on critical regions to perform the theory of mind task has an impact on the recollection. The regions of interest for eye movements on the comic strips (Vistoli et al., 2015) have been evaluated and determined in a previous eyetracking study (Roux et al., 2016). In the pilot study, 18 participants without any medical or past psychiatric illness were recruited. The authors recorded participants’ ocular fixations on the comic strips used for evaluating theory of mind and computed a heat map based on duration of fixations in order to define regions of interest (ROI) needed to accomplish the task (Appendix A, Roux et al., 2016). In the present work, a flashed red light was used to capture patients’ attention towards critical features of the comics (as defined by the ROI in Roux et al. (2016). We hypothesize that while patients with schizophrenia have an automatic inability to process bottom-up information, a visual cue which brings their attention to the ROI would result in better ToM task accuracy and recollection. 3. Methods 3.1. Subjects 42 individuals of two groups have been recruited as a control group and patients with schizophrenia. The demographic and clinical characteristics of participants are shown in Table 1. Schizophrenia, schizoaffective disorder or schizophreniform disorders were diagnosed based on the DSM-IV-R criteria. Patients were interviewed by senior psychiatrists. Patients were stable and were recruited from community mental health centers and outpatient clinics in the Versailles area. All of the participants were naturally French speaking. They had no current or past neurological pathology (as epilepsy, former coma or head trauma) neither drugs addiction or clinical alcoholism. Thus, participants with neurological or substance abuse comorbidities were excluded from the study. Senior psychiatrists have not found other comorbidities which could led to alter the subjects’ performance. All of them volunteered for the experiment and had eyesight normal or corrected-tonormal. Control group was constituted from individuals without any psychiatric or neurological pathology. All participants gave their written informed consent to participate in the study according to French regulations. 3.2. Procedure and experimental conditions Experimental procedure was authored and executed by the E-prime software 2.0. The subject was placed to 60 cm from the computer screen with a refresh rate of 85 Hz. The black and white thumbnails were presented successively on a white background. Table 1 Demographical and clinical characteristics of participants. Patients
Sex
Age (in years) Premorbid verbal IQ Education Level Lateralisation Cognitive Empathy Affective Empathy Total Empathy Schizophrenia duration (in years) Treatment (equivalent chlorpromazine) PANSS P PANSS N PANSS T PSP
Controls
Analysis
Female
Male
Female
Male
Chi2
df
3
18
8
13
p
3.08
1
0.079
Mean (SD)
Mean (SD)
t
df
p
38.4 (12.2) 27.5 (4.26) 11.2 (1.86) 47.6 (56.9) 50.9 (9.3) 32.4 (5.2) 83.3 (11.3) 15 (10.2) 497 (375) 14.3 (4.84) 19.1 (5.72) 69.2 (17.9) 58.1 (18.1)
37.3 29.7 13.9 68.6 56.2 32.5 88.7
0.295 −1.35 −4.56 −1.35 −2.09 −0.0990 −1.73
40 40 38 40 40 40 40
0.769 0.182 0.000 0.185 0.0430 0.921 0.091
100
(12.7) (5.85) (1.88) (50) (6.82) (4.06) (8.61)
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3.3. Intention attribution phase The Brunet et al.’s (2000) non-verbal intention attribution test was carried out on a microcomputer. This test was composed of four-pictures comic-strips. Participants had to look at first three pictures, presented one after another and then decide by using the keyboard whether the fourth picture is a logical end to the story or not (congruent versus incongruent). The type of causality involved in the comic strips varied according to two experimental conditions. In the intention attribution (IA) condition, the participants were presented with 24 scenarios depicting a character whose behavior was driven by a specific intention; participants had to infer the character’s intention to understand the scenario. In the physical causality with characters (PCCh) condition, the participants were presented another set of 24 scenarios depicting a character whose movement was determined by a physical causality; participants had to reason on the mechanical properties of human bodies (e.g., gravity) in order to understand the scenario. The task was implicit as the participants were not informed about the differences between AI and PCCh. Moreover, in order to see whether attentional cues on intention attribution would impact patients’ recollection, we introduced visual saliency reinforcement to stimuli: most relevant areas of the first three pictures were colored in red for a very short period of time. To determine these pertinent areas, maxima from fixation heat maps from Roux et al.’s work (2016) were extracted. In this work, Roux et collaborators recorded ocular movements with same comic strip material and attribution intention task on control subjects. Then they determined which regions were hit by participants’ ocular movement for every comic strip. We used this ROI in order to determine the localization of our attentional cues. Therefore, in our experiment we had 2 experimental conditions within 2 modalities
• Types of attribution: Intention Attribution (IA) and Physical causality with characters (PCCh). • Attentional Cuing: IA and PCCh without or with cuing (IA-C or PCCh-C). Thus, every subject was seeing 48 comic strips in three equal sessions just after a training session. Therefore, 16 comic strips were distributed (IA/IA-C/PCCh/PCCh-C) across three sessions while randomizing every presentation of those. The Fig. 1 depicts an example of this intention attribution task with IA-Cueing. Every thumbnail was presented for 2000 ms. The fourth thumbnail was presented until the subject’s response and for a maximum of 5000 ms. Thumbnails were separated from each other by a white background in which a fixation point was inserted for 1500 ms at the center. The apparition of attentional cueing started 100 ms after the presentation of the thumbnails in Attentional Cueing condition. These cues, in the shape of a transparent red flash on the pertinent regions of the strips was presented during 70 ms. While a stimulus above the threshold of sensation or of awareness is defined such as supraliminal, this stimulus onset asynchrony keeps our attentional cue at a supraliminal level. According to Posner and Cohen (1984), every prime should be under the 300 ms in order not to distract the subjects’ attention but to mobilize it. Therefore, we used 70 ms as the threshold between the subliminal and supraliminal level with this kind of stimulus according in-house pretests with our materials. While the current research question is to explore whether mobilizing bottom-up process can lead to better realization of the ToM task without distracting the subjects, an attentional cueing of 70 ms duration has been used.
Fig. 1. An example of this intention attribution task with IA-Cueing. The task is to see all first three thumbnails and decide whether the 4. Thumbnail is a congruous or not with the scenario. 101
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3.4. Recognition phase At the end of the intention attribution phase, we conducted a picture recognition task in order to assess the impact of the attentional cueing of the relevant regions. The task consisted in looking at thumbnails extracted from the comic strips and to indicate after each thumbnail whether this picture had been seen during the intention attribution task. 72 miniatures were presented to the subjects. Half of these items were unseen by the participants and other half has been seen during the first phase. Regarding already seen items, half of them had been proposed with attentional cues during the first phase while the other half had been seen without attentional cues. In the recognition task, these items were randomly presented without any cues. Every trial started with a fixation point presented for 1500 ms. Then, miniatures of comic strips were presented on the screen until the participant’s response. All items were separated with 200 ms intervals. In order to assure that the recognition task assessed the content of long-term memory, we gave a 15 min break between the intention attribution phase and the recognition phase of our experiment (this break was also needed for changing e-prime scripts and explaining the new instructions). Indeed, given the fact that this level of concentration for realizing two different tasks is hard to maintain for people with schizophrenia, we deliberately gave the opportunity to subjects to take a rest. 4. Results The mean response latencies and correct response rates presented here were calculated across subjects for each experimental condition (see Table 1). Latencies that under 100 ms and of incorrect responses were eliminated for the analysis. Separate repeatedmeasures analyses of variance (ANOVA) were performed on latencies and correct response rates as between-subject factor ‘ patients group’ and ‘control group’ and as within subject factor of item type ‘IA/IA-C/PCCh/PCCh-C’ for intention attribution task and ‘Past Seen items with cue, Past Seen items without cue and New Items’ for recognition task. For every Anova presented here we verified that the data is conform to normality, tested by the means of Kolmogorov–Smirnov test. 4.1. Intention attribution task The analysis of variance has revealed a main effect of Group (F = 16.09, p < 0.0005) on correct responses rates. The difference between two populations was the following: 69.15% for patients and 83% for control groups’ correct answers globally. Regarding latency; the analysis of variance has also revealed a main effect of Group (F = 10.5, p < 0.005) and item type (F = 57.47, p < 0.0000). Indeed, patients have a mean of correct answer of 2133 ms while the control subjects present 1840 ms globally. At the same time, within all subjects, intention attribution condition (AI) processing seems to be much longer (i.e. 2027 ms) than Physical causality with characters (PCCh) processing (i.e. 1852 ms). The analysis of variance did not reveal any interaction between type of attribution and attentional cueing across populations (see Graph 1). 4.2. Recognition task The analysis of variance has revealed a significant effect of Group on correct responses rates (F = 52.3, p < 0.000*). The accuracy of discrimination of new and old miniatures of comic strip was 71.5% for the patients with schizophrenia group and 80% for the control group. Regarding correct response latencies, we also observed a significant difference between the two populations (F = 6.76, p < 0.01). According to this result, for correct accuracy of recognition task, patients require 1660 ms while the control patients need a mean of 1414 ms. However, an interesting result is provided concerning already seen items. Finally, although there was no difference between previously miniatures of thumbnails seen with or without attentional cue, there was a difference in regard of the type of items presented. Indeed, the analysis has revealed a difference between AI condition (60%) and PCCh (69%) condition (F = 12.9, p < 0.001) for accuracy. Again, the same pattern occurred for the latency. AI condition processing was slower (1636 ms) than Pcch condition processing (1529 ms) (F = 7.3, p < 0.001) (see Graph 2).
Correct Answers for Intention Attribution Task 100% 80% 60% 40% 20% 0% AI
LP Patients
Control
Graph 1. Descriptive statistics of percentage of correct answers for intention attribution task. 102
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Correct Answers for Recognition Task 100% 80% 60% 40% 20% 0% AI
LP Patients
Controls
Graph 2. Descriptive statistics of percentage of correct answers for recognition task.
4.3. Signal Detection Theory (SDT) analysis We also conducted a signal detection theory (Green & Swets, 1966; Macmillan & Creelman, 1990) analysis regarding the global performances of recognition task. This methodology allows measurement of both attention-specific factors measured by the nonparametric index of perceptual sensitivity d′, and response bias, measured by B (Grier, 1971). For every subject, a d′ and B index has been calculated and submitted to Wilcoxon test. The results showed a significant difference between d′ of schizophrenia patients (average = 1.7) and control group (average = 1.11): Z = −1.902; p < 0.05 for global recognition task. 5. Discussion It is now largely accepted that patients with schizophrenia have a deficit to attribute mental states to others, such as intentions, needs and motivations (Brüne, 2005; Sprong et al., 2007) and to perform memory tasks (Reichenberg & Harvey, 2007). According to one hypothesis, these impairments may be due to a deficit of early visual attention, (Bjorkquist & Herbener, 2013). Another hypothesis posits a robust correlation between intention attribution and autobiographical memory that results in the fact that impaired recollection of past events makes it difficult to infer others’ intentions (Corcoran & Frith, 2003). In sum, when there are recollection impairments on intentionality in schizophrenia, according to Bjorkquist and Herbener (2013), this is because of a deficit of early visual attention (a bottom-up process). However, according to Corcoran and Frith (2003), intention attribution in schizophrenia impairments may be due to generalized autobiographical memory difficulties. In this paper, we present an experiment in which we triggered a bottom-up process by using a supraliminal attentional cue in order to explore (1) whether this cue would improve intention attribution of comic strip characters in patients with schizophrenia and (2) whether this cue would impact patient’s recollection performances. 5.1. For attribution intention task The results showed that our attentional cue had no impact on the performance of attribution intention in any group. However, it seems that we were able to replicate the results of Brüne (2005) and Sprong et al. (2007); patients with schizophrenia have poorer performance than the control group for performing attribution intention task although they’re taking their time more than the control group. Of great interest, in any group, correct answers of comic strips presenting Physical causality with characters (PCCh) seems to need lesser latencies than comic strips presenting Attribution Intention (AI). Thus, for each group, analysis of results on the correct answers show that attribution intention needs more cognitive process than physical causality for the coherent recognition of events. 5.2. For recollection task Results from the recollection task indicate that we replicated for the first time the recollection deficit of patients with schizophrenia with a material designed to assess theory of mind. One of the main contributions of our paper is to show that for the first time a comic strip based attribution intention stimuli has been tested in the long-term memory. According to the results, the presence of characters with attribution intention or physical causality does not itself improve recollection of schizophrenia patients since the overall memory performance as well as the latencies for the correct answer were lower than control subjects. Interesting enough, across any group, the physical causality with characters seems to be better remembered (69%) than characters with attribution intention (60%) according to the analysis of variance. However, the main latency for correct answers were higher for characters with attribution intention than physical causality. These results highlight that there are none statistical differences regarding the modality of attribution task between patients with schizophrenia and control patients. Thus, the main difficulties that patients encounter seem to be a generalized effect on long-term memory. However, patients with schizophrenia seem to be impaired in recognition task but more for memory traces coding intentions than physical causality. 103
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6. Conclusion Our results show that a supraliminal attentional cue under the form that we designed to trigger bottom-up cognitive processes does not improve neither intention attribution nor autobiographical memory. However, interesting enough, we find out that when providing the correct answer, the latencies needed for the cognitive task does not differ from schizophrenia patients than control patients. Again, while providing the correct answer, the latency difference needed in order to process stimuli with psychical causality and characters with an intention are not statistically different between patients with schizophrenia and control patients. Regarding the recollection, the visual attentional cue presented during 70 ms and placed on the pertinent parts of the comic strip in order to accomplish the intention attribution task did not result in any recollection improvement in any group. This result is not consistent with the hypothesis of Bjorkquist and Herbener (2013) regarding deficit of early visual attention. The use of 70 ms as a choice of supraliminal attentional cue can be seen as a limitation of our study. In fact, it can be argued that a 70 ms red flash was not sufficient to make pertinent areas of the comic strip more salient and to mobilize the participants’ attention, although according to Posner and Cohen (1984) it should have. However, given the fact that patients with schizophrenia have general neurocognitive impairments, the use of an attentional may not constitute a good candidate to mobilize attentional skills. Further study should increase gradually the duration of the attentional cue from 70 to 300 ms which is the limit in order to mobilize attention according to Posner and Cohen (1984). Finally, and most importantly, patients with schizophrenia exhibit better recollection performances with physical casualty than characters with intention. These results show that schizophrenia patients, when they remember seeing a comic strip, they remember much more strips involving physical causality than characters with intention. One could argue, given the fact that widely acknowledged overall long-term memory impairment exists in schizophrenia, recollection performance should not be different according the nature of the stimuli. Our results show that autobiographical deficits of schizophrenia patients tend to be different across the nature of the stimuli. To the best of our knowledge, this is the first demonstration that schizophrenia patients are impaired in recognition task but more for intentionality than physical causality, tested with comic strip based material (Vistoli et al., 2011). Deficits of long-term memory present differential profiles according the encoding conditions as intentional or incidental and according to retrieval strategies as free recall or recognition (for a review see Bonner-Jackson, Yodkovik, Csernansky, & Barch, 2008). For instance, according to Bonner-Jackson and collaborators, incidental encoding strategy improves overall recognition memory among individuals with schizophrenia. Normally, a supraliminal attentional cue or at least under the form that we that we used in our study should have triggered an incidental encoding which would establish an improvement of attribution intention and recollection of those items. Our results show that although incidental encoding would improve overall recognition performance in individuals with schizophrenia, this is not the case for stimuli in which characters are presenting an intention. In the field of episodic memory, the fact that intention attribution seems to be impaired for schizophrenia patients in every day, the recollection of intentions suffer more than physical causality. If early visual attention deficit theory of schizophrenia patients cannot be validated from our study, the best candidate to explain our results is Corcoran and Frith’s theory (2003). In their work, Corcoran and Frith (2003) found a robust relationship between the abilities to recollect events from the past and the ability to understand the mental states of others. These authors conclude that this result can be best explained by the fact that mentalizing is accomplished using inductive or analogical reasoning since to solve these social inference problems one can rely upon information gathered in the past, which is a complex topdown cognitive process. The fact that participants performed faster the task for physical causality than characters with intentions can also be explained by the nature and organization of the memory traces in human memory. In our everyday life, we are exposed to more diverse types of physical objects and the reasoning behind their use and attributes are much more different from people’s intentions, which tend to be similar toward us. Thus, memory traces for intentions are in nature more agglutinated and represent a higher cognitive cost than memory traces for physical objects whose are more distinct and easier to differentiate. This organization of long-term human memory (Oker & Versace, 2010) can explain why participants were faster to infer physical causality in our experiment. In sum, the results of our experiment seem to provide further arguments in favor of Corcoran and Frith (2003) view along with theories of a strong relationship between the autobiographical memory and theory of mind performances. Besides, as Conway (2001) states that although episodic memory is highly dependent to sensory-perceptual information, autobiographical memory is an integrated system of all prior experiences, sensorimotor or cognitive, including a sense of self. Thus, given the theory of mind deficits of patients with schizophrenia, in the light of current results, it is understandable that their recollection performance reflects their own attribution intention performances. Finally, our results provide arguments for physicians and other researchers whom are constantly developing new cognitive remediation or cognitive training programs for patients with schizophrenia. While the theory of mind impairments is generally the focus of those programs, the use of a supraliminal attentional cue as proposed in the present study cannot be recommended. These programs should be more focused on higher level cognitive process such as metacognition for instance. Acknowledgements This research was partially funded by a grant from the Agence Nationale de la Recherche: ANR-11-EMCO- 0007. We are very thankful to Dr. Graziella Zanatta, Dr. Erica Martins, Elisabeth Massé, and all the members of the Adult Psychiatric Service at Versailles Hospital for their support, and their help for the participant’s recruitment, along this work.
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Appendix A
Without cuing
Eye tracking Data
Condition within cuing
Without cuing
Eye tracking Data
Condition within cuing
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Appendix B. Supplementary material Supplementary data to this article can be found online at https://doi.org/10.1016/j.concog.2018.11.007.
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Oker, A., & Versace, R. (2010). Distinctiveness effect due to contextual information in a categorization task. Current Psychology Letters, Vol. 26(1). Perner, J. (2000). Memory and theory of mind. The Oxford handbook of memory (pp. 297–312). . Piolino, P., Desgranges, B., Eustache, F., & Eustache, F. (2000). La mémoire autobiographique: théorie et pratique. Marseille, France: Solal. Posner, M. I., & Cohen, Y. (1984). Components of visual orienting Attention and performance X. Control of Language Processes, 32, 531–556. Premack, D., & Woodruff, G. (1978). Does the chimpanzee have a theory of mind? Behavioral and Brain Sciences, 1(4), 515–526. Rabin, J. S., Gilboa, A., Stuss, D. T., Mar, R. A., & Rosenbaum, R. S. (2010). Common and unique neural correlates of autobiographical memory and theory of mind. Journal of Cognitive Neuroscience, 22(6), 1095–1111. Rabin, J. S., & Rosenbaum, R. S. (2012). Familiarity modulates the functional relationship between theory of mind and autobiographical memory. Neuroimage, 62(1), 520–529. Rassovsky, Y., Green, M. F., Nuechterlein, K. H., Breitmeyer, B., & Mintz, J. (2004). Paracontrast and metacontrast in schizophrenia: Clarifying the mechanism for visual masking deficits. Schizophrenia Research, 71(2), 485–492. Rassovsky, Y., Horan, W. P., Lee, J., Sergi, M. J., & Green, M. F. (2011). Pathways between early visual processing and functional outcome in schizophrenia. Psychological Medicine, 41(3), 487–497. Reichenberg, A., & Harvey, P. D. (2007). Neuropsychological impairments in schizophrenia: Integration of performance-based and brain imaging findings. Psychological Bulletin, 133(5), 833. Roux, P., Brunet-Gouet, E., Passerieux, C., & Ramus, F. (2016). Eye-tracking reveals a slowdown of social context processing during intention attribution in patients with schizophrenia. Journal of Psychiatry & Neuroscience: JPN, 41(2), E13. Rushe, T. M., Woodruff, P. W. R., Murray, R. M., & Morris, R. G. (1999). Episodic memory and learning in patients with chronic schizophrenia. Schizophrenia Research, 35(1), 85–96. Sarfati, Y., & Hardy-Baylé, M. C. (1999). How do people with schizophrenia explain the behaviour of others? A study of theory of mind and its relationship to thought and speech disorganization in schizophrenia. Psychological Medicine, 29(3), 613–620. Sergi, M. J., & Green, M. F. (2003). Social perception and early visual processing in schizophrenia. Schizophrenia Research, 59(2), 233–241. Sergi, M. J., Rassovsky, Y., Nuechterlein, K. H., & Green, M. F. (2006). Social perception as a mediator of the influence of early visual processing on functional status in schizophrenia. American Journal of Psychiatry, 163(3), 448–454. Spreng, R. N., & Grady, C. L. (2010). Patterns of brain activity supporting autobiographical memory, prospection, and theory of mind, and their relationship to the default mode network. 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Sprong, M., Schothorst, P., Vos, E., Hox, J., & Van Engeland, H. (2007). Theory of mind in schizophrenia. The British Journal of Psychiatry, 191(1), 5–13. Suddendorf, T., & Corballis, M. C. (1997). Mental time travel and the evolution of the human mind. Genetic, Social, and General Psychology Monographs, 123(2), 133–167. Vistoli, D., Brunet-Gouet, E., Lemoalle, A., Hardy-Baylé, M. C., & Passerieux, C. (2011). Abnormal temporal and parietal magnetic activations during the early stages of theory of mind in schizophrenic patients. Social Neuroscience, 6(3), 316–326. Vistoli, D., Passerieux, C., El Zein, M., Clumeck, C., Braun, S., & Brunet-Gouet, E. (2015). Characterizing an ERP correlate of intentions understanding using a sequential comic strips paradigm. Social Neuroscience, 10(4), 391–407.
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Consciousness and Cognition journal homepage: www.elsevier.com/locate/concog
Schizophrenia patients are impaired in recognition task but more for intentionality than physical causality
T
Ali Okera, , Sarah Del Goletod, Alice Vignesb, Christine Passerieuxb,c, Paul Rouxb,c, Eric-Brunet Gouetb,c ⁎
a
Laboratoire C2S (Cognition, Santé, Société), EA 6291, Department ESPE, Université de Reims Champagne-Ardenne, Reims, France Laboratoire HANDIReSP (EA4047), Université de Versailles Saint-Quentin-En-Yvelines, Versailles, France c Service de Psychiatrie de l’Adulte et d’Addictologie, Centre Hospitalier de Versailles, Le Chesnay, France d Laboratoire de Psychopathologie et Neuropsychologie (EA 2027), Université Paris Lumières, Paris 8, St. Denis, France b
ABSTRACT
It is now largely accepted that patients with schizophrenia have a deficit to attribute mental states to others, such as intentions, needs and motivations but also to perform memory tasks. According to one hypothesis, these impairments may be due to an early visual attention deficit during the encounter of social stimuli. Another hypothesis posits a robust correlation between intention attribution and autobiographical memory that results in impaired recollection of past events making it difficult to infer others’ intentions. In sum, the link between intention attribution and encoding process is yet to be explored in patients with schizophrenia. The objective of the present study is to contribute to this debate by investigating whether schizophrenic patients’ recollection can be boosted by an attentional cueing on relevant information and to determine the influence of two different situational contexts: attribution of intentions or physical causality scripts. By using a supraliminal attentional cue, we made relevant areas of our material more salient across two conditions: attribution of intentions (AI) and physical causality with human characters (PCCH). The results confirmed expected deficit of explicit memory in schizophrenia patients while attentional cueing on relevant areas for intentions attribution or physical causality had no effect on recollection in any group. However, it seems that the recollection performances are highly influenced by the nature of intentions attribution. Also, it is the first time that the material used for the assessment of theory of mind performances has been tested with a recognition test.
1. Introduction Social cognition represents a high priority area for the study of schizophrenia due to its strong association with the functional outcome (Couture, Penn, & Roberts, 2006; Fett, Viechtbauer, Penn, van Os, & Krabbendam, 2011; Lam, Raine, & Lee, 2014; MartínezDomínguez, Penadés, Segura, González-Rodríguez, & Catalán, 2015). Among the different social cognitive abilities, theory of mind (ToM) refers to the capacity to infer mental states (i.e. intentions, beliefs, needs…) in order to understand and predict others’ behavior (Premack & Woodruff, 1978). A consensus emerged during the past decades regarding ToM impairment in patients with schizophrenia (for reviews, see Brüne, 2005; Kronbichler, Tschernegg, Martin, Schurz, & Kronbichler, 2017; Sprong, Schothorst, Vos, Hox, & Van Engeland, 2007). In general, theory of mind in schizophrenia is tested using verbal (Corcoran & Frith, 2003; Janssen, Krabbendam, Jolles, & Van Os, 2003) or non-verbal tasks based on successive comic strips depicting sequences of actions (Sarfati & Hardy-Baylé, 1999; Langdon, Coltheart, & Ward, 2006; Vistoli, Brunet-Gouet, Lemoalle, Hardy-Baylé, & Passerieux, 2011) in which participants are generally asked to decide whether the last picture is congruent or not regarding the preceding three images. One of the comic strips paradigm available having a control condition is based on the work of Brunet, Sarfati, Hardy-Baylé, and Decety (2000). This material involves a condition with physical causality (reasoning about the weight, location, speed, and the physical
⁎
Corresponding author. E-mail address: [email protected] (A. Oker).
https://doi.org/10.1016/j.concog.2018.11.007 Received 27 December 2017; Received in revised form 24 October 2018; Accepted 25 November 2018 1053-8100/ © 2018 Elsevier Inc. All rights reserved.
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properties of objects but in the presence of a person) and a condition with an attribution intention towards a person (reasoning about the need, belief or desire of a person). Studies using this material revealed an impaired theory of mind performance in patients with schizophrenia (Bara, Ciaramidaro, Walter, & Adenzato, 2011; Roux, Brunet-Gouet, Passerieux, & Ramus, 2016; Vistoli et al., 2011, 2015). It has also been reported that patients with schizophrenia have poor performance in several memory tasks (Reichenberg & Harvey, 2007) and particularly in episodic memory (Cirillo & Seidman, 2003; Rushe, Woodruff, Murray, & Morris, 1999). More precisely, patients seem to have difficulties in two critical aspects of episodic memory (i.e. conscious recollection and autobiographical memory, for a review see Danion, Huron, Vidailhet, & Berna, 2007). Concerning episodic memory, clusters of arguments tend to show an overlap between autobiographical memory and theory of mind (Corcoran & Frith, 2003; Dimaggio, Salvatore, Popolo, & Lysaker, 2012; Perner, 2000; Rabin & Rosenbaum, 2012; Rabin, Gilboa, Stuss, Mar, & Rosenbaum, 2010; Spreng & Grady, 2010; Spreng, Mar, & Kim, 2009; Suddendorf & Corballis, 1997). For example, Corcoran and Frith (2003) found a robust relationship1 between autobiographical memory and theory of mind performances (as measured with the hinting task2) in patients with schizophrenia. Moreover, the authors found out that participants with schizophrenia tended to recollect odd or negative events when they were asked to answer standard autobiographical memory questions. The authors suggested that patients’ poor recollection of events could mislead them when attributing other’s intentions (Corcoran & Frith, 2003). Recent neuroimaging studies concur with this overlap (Spreng & Grady, 2010). According to this fMRI study, autobiographical memory, prospection and theory of mind shared a common pattern of brain activity including midline structures in the frontal and parietal lobes operating within the default mode network (the DMN, for a review see Mothersill, Knee-Zaska, & Donohoe, 2016). In line with these results, in a large meta-analysis conducted on more than 30 neuroimaging studies, Spreng et al. (2009) concluded that even if autobiographical memory and theory of mind have been previously studied as distinct, these two cognitive processes exhibited extensive functional overlap. Indeed, this meta-analyse showed that there is a convergence between theory of mind and autobiographical memory in prefrontal area (rostral anterior cingulate gyrus), in medial temporal area (parahippocampal cortex and amygdala), in medial parietal lobe (precuneus and posterior cingulate cortex) and in lateral area (jonction temporo-parietal junction and superior temporal sulcus). However, according to another hypothesis, theory of mind impairments may also be due to an early visual attention deficit, which could alter the selection and the process of relevant social cues to attribute intentions to others (Bjorkquist & Herbener, 2013; Rassovsky, Green, Nuechterlein, Breitmeyer, & Mintz, 2004; Sergi, Rassovsky, Nuechterlein, & Green, 2006). Generally, these works focused on visual perception of emotionally charged images for less than 100 ms and suggested that impaired social perception appears to be influenced by abnormalities in early aspect of visual processing in individuals with schizophrenia. For instance, regarding social perception, Maher, Mashhoon, Ekstrom, Lukas, and Chen (2016) have shown that N1703 amplitudes didn’t differ between faces and non-socially relevant stimuli in patients with schizophrenia. Others studies also suggested a connection between early visual processes and social perceptual deficits in schizophrenia (Rassovsky, Horan, Lee, Sergi, & Green, 2011; Sergi & Green, 2003). According to Rassovsky et al. (2011) because social perception consists of fast visual identification of socially relevant cues (facial expressions, gaze directions etc…), “It is therefore possible that early visual perceptual deficits, … impose limits on the amount of visual information that can be processed at a given time, which in turn could reduce one’s ability to process socially relevant visual information and result in failures to identify briefly available social cues” (pg. 294). Moreover, Roux et al. (2016) shed light on the time course of social context processing during intention attribution in patients with schizophrenia. In their study, the authors evaluated ToM performances using comic strips (with intention attribution and physical reasoning conditions) while performing eye tracking recording in order to assess processing time dedicated to intention attribution. They stated that compared to control subjects, patients with schizophrenia were slower in intention attribution but not in physical reasoning. In conclusion, authors highlighted that schizophrenia was characterized by a delay in intention attribution related to a slowdown of social context processing. Based on their findings, Sergi and Green (2003) and Sergi et al. (2006) also suggested an association between early visual processes and social perceptual deficits in schizophrenia. In Sergi et al. (2006) authors conducted a study of structural equation modelling to correlate early visual processing (evaluated by visually masked stimulus of 12.5 ms), social perception and functional status of patients. Results showed that early visual processing was highly correlated (via multiple regression analysis) to social perception compared to functional status in patients with schizophrenia. It can be proposed that if theory of mind impairments are related to deficits of early visual attention, these combined disorders should also impact long-term memory. The idea of an intimate relationship between memory and attention has been widely defended by Cowan and Conway. According to the initial description of Cowan (1998), “there is an intricate relation between memory and attention in a model of processing” (pg. 27). In his model, a central executive module (similar to Baddeley’s model, 1986) directs attention to the stimulus involved in a cognitive task, and provides a processing ‘in’ (write) and ‘out’ (read) contents toward what’s called a ‘focus of attention’ module. This focus of attention works as a magnifying glass in the activated part of the short-term memory and thus, writes and reads contents of the short-term memory. According to Cowan, this process provides a long-term storage of some features automatically. However, attentional processing required by the task results in more elaborate encoding which is critical for voluntary retrieval later on (Cowan, 2011). Thus, the more intense the attention, the easier the retrieval. On the other hand, Conway (2001) has proposed a model based on a constructivist view of autobiographical memory (Piolino, Desgranges, Eustache, & Eustache, 2000). According to Conway (2001), when we are retrieving a memory, the retrieved information
1
By the means of Pearson’s r excluding logical memory and IQ. 10 short vignettes to read in which it’s presented an interaction between two characters. “All of these end with one of the characters dropping a very obvious hint. The subject is asked what the character really meant when he/she said this” (Corcoran, Mercer, & Frith, 1995). 3 The N170 ERP component is a right hemisphere lateralized negativity peaking around 170 ms after stimulus-onset, and a reliable marker of face detection. 2
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is not just the information itself; it is more likely a construct involving past experiences and a model of self-integrity and coherence. Thus, the retrieval process depends on the context, prior experiences, the relevance of the task for the subject and the personal involvement of the subject to the stimulus. 2. Present work The aim of this study is to contribute to the debate on whether the theory of mind impairment is due to a bottom-up cognitive process such as early visual attention deficit. In cognitive psychology, bottom-up processing (or data-driven processing) can be defined by a cognitive task which is triggered from the perception of the stimulus or the sensory-motor data itself. On the contrary, top-down processing is required for a cognitive task which need prior knowledge, contextual information and inferences already stored in the system. In 1970, this distinction has first appeared in the field of visual perception (Gregory, 1970) then it became a reference for other cognitive tasks and information processing involving central and peripheral nervous system. We propose an experiment in which early perceptual cues are used on comic strip series to evaluate theory of mind performance on schizophrenia patients’ recollection. The general idea is to verify whether by triggering experimentally a bottom-up process provided by a supraliminal cue on critical regions to perform the theory of mind task has an impact on the recollection. The regions of interest for eye movements on the comic strips (Vistoli et al., 2015) have been evaluated and determined in a previous eyetracking study (Roux et al., 2016). In the pilot study, 18 participants without any medical or past psychiatric illness were recruited. The authors recorded participants’ ocular fixations on the comic strips used for evaluating theory of mind and computed a heat map based on duration of fixations in order to define regions of interest (ROI) needed to accomplish the task (Appendix A, Roux et al., 2016). In the present work, a flashed red light was used to capture patients’ attention towards critical features of the comics (as defined by the ROI in Roux et al. (2016). We hypothesize that while patients with schizophrenia have an automatic inability to process bottom-up information, a visual cue which brings their attention to the ROI would result in better ToM task accuracy and recollection. 3. Methods 3.1. Subjects 42 individuals of two groups have been recruited as a control group and patients with schizophrenia. The demographic and clinical characteristics of participants are shown in Table 1. Schizophrenia, schizoaffective disorder or schizophreniform disorders were diagnosed based on the DSM-IV-R criteria. Patients were interviewed by senior psychiatrists. Patients were stable and were recruited from community mental health centers and outpatient clinics in the Versailles area. All of the participants were naturally French speaking. They had no current or past neurological pathology (as epilepsy, former coma or head trauma) neither drugs addiction or clinical alcoholism. Thus, participants with neurological or substance abuse comorbidities were excluded from the study. Senior psychiatrists have not found other comorbidities which could led to alter the subjects’ performance. All of them volunteered for the experiment and had eyesight normal or corrected-tonormal. Control group was constituted from individuals without any psychiatric or neurological pathology. All participants gave their written informed consent to participate in the study according to French regulations. 3.2. Procedure and experimental conditions Experimental procedure was authored and executed by the E-prime software 2.0. The subject was placed to 60 cm from the computer screen with a refresh rate of 85 Hz. The black and white thumbnails were presented successively on a white background. Table 1 Demographical and clinical characteristics of participants. Patients
Sex
Age (in years) Premorbid verbal IQ Education Level Lateralisation Cognitive Empathy Affective Empathy Total Empathy Schizophrenia duration (in years) Treatment (equivalent chlorpromazine) PANSS P PANSS N PANSS T PSP
Controls
Analysis
Female
Male
Female
Male
Chi2
df
3
18
8
13
p
3.08
1
0.079
Mean (SD)
Mean (SD)
t
df
p
38.4 (12.2) 27.5 (4.26) 11.2 (1.86) 47.6 (56.9) 50.9 (9.3) 32.4 (5.2) 83.3 (11.3) 15 (10.2) 497 (375) 14.3 (4.84) 19.1 (5.72) 69.2 (17.9) 58.1 (18.1)
37.3 29.7 13.9 68.6 56.2 32.5 88.7
0.295 −1.35 −4.56 −1.35 −2.09 −0.0990 −1.73
40 40 38 40 40 40 40
0.769 0.182 0.000 0.185 0.0430 0.921 0.091
100
(12.7) (5.85) (1.88) (50) (6.82) (4.06) (8.61)
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3.3. Intention attribution phase The Brunet et al.’s (2000) non-verbal intention attribution test was carried out on a microcomputer. This test was composed of four-pictures comic-strips. Participants had to look at first three pictures, presented one after another and then decide by using the keyboard whether the fourth picture is a logical end to the story or not (congruent versus incongruent). The type of causality involved in the comic strips varied according to two experimental conditions. In the intention attribution (IA) condition, the participants were presented with 24 scenarios depicting a character whose behavior was driven by a specific intention; participants had to infer the character’s intention to understand the scenario. In the physical causality with characters (PCCh) condition, the participants were presented another set of 24 scenarios depicting a character whose movement was determined by a physical causality; participants had to reason on the mechanical properties of human bodies (e.g., gravity) in order to understand the scenario. The task was implicit as the participants were not informed about the differences between AI and PCCh. Moreover, in order to see whether attentional cues on intention attribution would impact patients’ recollection, we introduced visual saliency reinforcement to stimuli: most relevant areas of the first three pictures were colored in red for a very short period of time. To determine these pertinent areas, maxima from fixation heat maps from Roux et al.’s work (2016) were extracted. In this work, Roux et collaborators recorded ocular movements with same comic strip material and attribution intention task on control subjects. Then they determined which regions were hit by participants’ ocular movement for every comic strip. We used this ROI in order to determine the localization of our attentional cues. Therefore, in our experiment we had 2 experimental conditions within 2 modalities
• Types of attribution: Intention Attribution (IA) and Physical causality with characters (PCCh). • Attentional Cuing: IA and PCCh without or with cuing (IA-C or PCCh-C). Thus, every subject was seeing 48 comic strips in three equal sessions just after a training session. Therefore, 16 comic strips were distributed (IA/IA-C/PCCh/PCCh-C) across three sessions while randomizing every presentation of those. The Fig. 1 depicts an example of this intention attribution task with IA-Cueing. Every thumbnail was presented for 2000 ms. The fourth thumbnail was presented until the subject’s response and for a maximum of 5000 ms. Thumbnails were separated from each other by a white background in which a fixation point was inserted for 1500 ms at the center. The apparition of attentional cueing started 100 ms after the presentation of the thumbnails in Attentional Cueing condition. These cues, in the shape of a transparent red flash on the pertinent regions of the strips was presented during 70 ms. While a stimulus above the threshold of sensation or of awareness is defined such as supraliminal, this stimulus onset asynchrony keeps our attentional cue at a supraliminal level. According to Posner and Cohen (1984), every prime should be under the 300 ms in order not to distract the subjects’ attention but to mobilize it. Therefore, we used 70 ms as the threshold between the subliminal and supraliminal level with this kind of stimulus according in-house pretests with our materials. While the current research question is to explore whether mobilizing bottom-up process can lead to better realization of the ToM task without distracting the subjects, an attentional cueing of 70 ms duration has been used.
Fig. 1. An example of this intention attribution task with IA-Cueing. The task is to see all first three thumbnails and decide whether the 4. Thumbnail is a congruous or not with the scenario. 101
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3.4. Recognition phase At the end of the intention attribution phase, we conducted a picture recognition task in order to assess the impact of the attentional cueing of the relevant regions. The task consisted in looking at thumbnails extracted from the comic strips and to indicate after each thumbnail whether this picture had been seen during the intention attribution task. 72 miniatures were presented to the subjects. Half of these items were unseen by the participants and other half has been seen during the first phase. Regarding already seen items, half of them had been proposed with attentional cues during the first phase while the other half had been seen without attentional cues. In the recognition task, these items were randomly presented without any cues. Every trial started with a fixation point presented for 1500 ms. Then, miniatures of comic strips were presented on the screen until the participant’s response. All items were separated with 200 ms intervals. In order to assure that the recognition task assessed the content of long-term memory, we gave a 15 min break between the intention attribution phase and the recognition phase of our experiment (this break was also needed for changing e-prime scripts and explaining the new instructions). Indeed, given the fact that this level of concentration for realizing two different tasks is hard to maintain for people with schizophrenia, we deliberately gave the opportunity to subjects to take a rest. 4. Results The mean response latencies and correct response rates presented here were calculated across subjects for each experimental condition (see Table 1). Latencies that under 100 ms and of incorrect responses were eliminated for the analysis. Separate repeatedmeasures analyses of variance (ANOVA) were performed on latencies and correct response rates as between-subject factor ‘ patients group’ and ‘control group’ and as within subject factor of item type ‘IA/IA-C/PCCh/PCCh-C’ for intention attribution task and ‘Past Seen items with cue, Past Seen items without cue and New Items’ for recognition task. For every Anova presented here we verified that the data is conform to normality, tested by the means of Kolmogorov–Smirnov test. 4.1. Intention attribution task The analysis of variance has revealed a main effect of Group (F = 16.09, p < 0.0005) on correct responses rates. The difference between two populations was the following: 69.15% for patients and 83% for control groups’ correct answers globally. Regarding latency; the analysis of variance has also revealed a main effect of Group (F = 10.5, p < 0.005) and item type (F = 57.47, p < 0.0000). Indeed, patients have a mean of correct answer of 2133 ms while the control subjects present 1840 ms globally. At the same time, within all subjects, intention attribution condition (AI) processing seems to be much longer (i.e. 2027 ms) than Physical causality with characters (PCCh) processing (i.e. 1852 ms). The analysis of variance did not reveal any interaction between type of attribution and attentional cueing across populations (see Graph 1). 4.2. Recognition task The analysis of variance has revealed a significant effect of Group on correct responses rates (F = 52.3, p < 0.000*). The accuracy of discrimination of new and old miniatures of comic strip was 71.5% for the patients with schizophrenia group and 80% for the control group. Regarding correct response latencies, we also observed a significant difference between the two populations (F = 6.76, p < 0.01). According to this result, for correct accuracy of recognition task, patients require 1660 ms while the control patients need a mean of 1414 ms. However, an interesting result is provided concerning already seen items. Finally, although there was no difference between previously miniatures of thumbnails seen with or without attentional cue, there was a difference in regard of the type of items presented. Indeed, the analysis has revealed a difference between AI condition (60%) and PCCh (69%) condition (F = 12.9, p < 0.001) for accuracy. Again, the same pattern occurred for the latency. AI condition processing was slower (1636 ms) than Pcch condition processing (1529 ms) (F = 7.3, p < 0.001) (see Graph 2).
Correct Answers for Intention Attribution Task 100% 80% 60% 40% 20% 0% AI
LP Patients
Control
Graph 1. Descriptive statistics of percentage of correct answers for intention attribution task. 102
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Correct Answers for Recognition Task 100% 80% 60% 40% 20% 0% AI
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Graph 2. Descriptive statistics of percentage of correct answers for recognition task.
4.3. Signal Detection Theory (SDT) analysis We also conducted a signal detection theory (Green & Swets, 1966; Macmillan & Creelman, 1990) analysis regarding the global performances of recognition task. This methodology allows measurement of both attention-specific factors measured by the nonparametric index of perceptual sensitivity d′, and response bias, measured by B (Grier, 1971). For every subject, a d′ and B index has been calculated and submitted to Wilcoxon test. The results showed a significant difference between d′ of schizophrenia patients (average = 1.7) and control group (average = 1.11): Z = −1.902; p < 0.05 for global recognition task. 5. Discussion It is now largely accepted that patients with schizophrenia have a deficit to attribute mental states to others, such as intentions, needs and motivations (Brüne, 2005; Sprong et al., 2007) and to perform memory tasks (Reichenberg & Harvey, 2007). According to one hypothesis, these impairments may be due to a deficit of early visual attention, (Bjorkquist & Herbener, 2013). Another hypothesis posits a robust correlation between intention attribution and autobiographical memory that results in the fact that impaired recollection of past events makes it difficult to infer others’ intentions (Corcoran & Frith, 2003). In sum, when there are recollection impairments on intentionality in schizophrenia, according to Bjorkquist and Herbener (2013), this is because of a deficit of early visual attention (a bottom-up process). However, according to Corcoran and Frith (2003), intention attribution in schizophrenia impairments may be due to generalized autobiographical memory difficulties. In this paper, we present an experiment in which we triggered a bottom-up process by using a supraliminal attentional cue in order to explore (1) whether this cue would improve intention attribution of comic strip characters in patients with schizophrenia and (2) whether this cue would impact patient’s recollection performances. 5.1. For attribution intention task The results showed that our attentional cue had no impact on the performance of attribution intention in any group. However, it seems that we were able to replicate the results of Brüne (2005) and Sprong et al. (2007); patients with schizophrenia have poorer performance than the control group for performing attribution intention task although they’re taking their time more than the control group. Of great interest, in any group, correct answers of comic strips presenting Physical causality with characters (PCCh) seems to need lesser latencies than comic strips presenting Attribution Intention (AI). Thus, for each group, analysis of results on the correct answers show that attribution intention needs more cognitive process than physical causality for the coherent recognition of events. 5.2. For recollection task Results from the recollection task indicate that we replicated for the first time the recollection deficit of patients with schizophrenia with a material designed to assess theory of mind. One of the main contributions of our paper is to show that for the first time a comic strip based attribution intention stimuli has been tested in the long-term memory. According to the results, the presence of characters with attribution intention or physical causality does not itself improve recollection of schizophrenia patients since the overall memory performance as well as the latencies for the correct answer were lower than control subjects. Interesting enough, across any group, the physical causality with characters seems to be better remembered (69%) than characters with attribution intention (60%) according to the analysis of variance. However, the main latency for correct answers were higher for characters with attribution intention than physical causality. These results highlight that there are none statistical differences regarding the modality of attribution task between patients with schizophrenia and control patients. Thus, the main difficulties that patients encounter seem to be a generalized effect on long-term memory. However, patients with schizophrenia seem to be impaired in recognition task but more for memory traces coding intentions than physical causality. 103
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6. Conclusion Our results show that a supraliminal attentional cue under the form that we designed to trigger bottom-up cognitive processes does not improve neither intention attribution nor autobiographical memory. However, interesting enough, we find out that when providing the correct answer, the latencies needed for the cognitive task does not differ from schizophrenia patients than control patients. Again, while providing the correct answer, the latency difference needed in order to process stimuli with psychical causality and characters with an intention are not statistically different between patients with schizophrenia and control patients. Regarding the recollection, the visual attentional cue presented during 70 ms and placed on the pertinent parts of the comic strip in order to accomplish the intention attribution task did not result in any recollection improvement in any group. This result is not consistent with the hypothesis of Bjorkquist and Herbener (2013) regarding deficit of early visual attention. The use of 70 ms as a choice of supraliminal attentional cue can be seen as a limitation of our study. In fact, it can be argued that a 70 ms red flash was not sufficient to make pertinent areas of the comic strip more salient and to mobilize the participants’ attention, although according to Posner and Cohen (1984) it should have. However, given the fact that patients with schizophrenia have general neurocognitive impairments, the use of an attentional may not constitute a good candidate to mobilize attentional skills. Further study should increase gradually the duration of the attentional cue from 70 to 300 ms which is the limit in order to mobilize attention according to Posner and Cohen (1984). Finally, and most importantly, patients with schizophrenia exhibit better recollection performances with physical casualty than characters with intention. These results show that schizophrenia patients, when they remember seeing a comic strip, they remember much more strips involving physical causality than characters with intention. One could argue, given the fact that widely acknowledged overall long-term memory impairment exists in schizophrenia, recollection performance should not be different according the nature of the stimuli. Our results show that autobiographical deficits of schizophrenia patients tend to be different across the nature of the stimuli. To the best of our knowledge, this is the first demonstration that schizophrenia patients are impaired in recognition task but more for intentionality than physical causality, tested with comic strip based material (Vistoli et al., 2011). Deficits of long-term memory present differential profiles according the encoding conditions as intentional or incidental and according to retrieval strategies as free recall or recognition (for a review see Bonner-Jackson, Yodkovik, Csernansky, & Barch, 2008). For instance, according to Bonner-Jackson and collaborators, incidental encoding strategy improves overall recognition memory among individuals with schizophrenia. Normally, a supraliminal attentional cue or at least under the form that we that we used in our study should have triggered an incidental encoding which would establish an improvement of attribution intention and recollection of those items. Our results show that although incidental encoding would improve overall recognition performance in individuals with schizophrenia, this is not the case for stimuli in which characters are presenting an intention. In the field of episodic memory, the fact that intention attribution seems to be impaired for schizophrenia patients in every day, the recollection of intentions suffer more than physical causality. If early visual attention deficit theory of schizophrenia patients cannot be validated from our study, the best candidate to explain our results is Corcoran and Frith’s theory (2003). In their work, Corcoran and Frith (2003) found a robust relationship between the abilities to recollect events from the past and the ability to understand the mental states of others. These authors conclude that this result can be best explained by the fact that mentalizing is accomplished using inductive or analogical reasoning since to solve these social inference problems one can rely upon information gathered in the past, which is a complex topdown cognitive process. The fact that participants performed faster the task for physical causality than characters with intentions can also be explained by the nature and organization of the memory traces in human memory. In our everyday life, we are exposed to more diverse types of physical objects and the reasoning behind their use and attributes are much more different from people’s intentions, which tend to be similar toward us. Thus, memory traces for intentions are in nature more agglutinated and represent a higher cognitive cost than memory traces for physical objects whose are more distinct and easier to differentiate. This organization of long-term human memory (Oker & Versace, 2010) can explain why participants were faster to infer physical causality in our experiment. In sum, the results of our experiment seem to provide further arguments in favor of Corcoran and Frith (2003) view along with theories of a strong relationship between the autobiographical memory and theory of mind performances. Besides, as Conway (2001) states that although episodic memory is highly dependent to sensory-perceptual information, autobiographical memory is an integrated system of all prior experiences, sensorimotor or cognitive, including a sense of self. Thus, given the theory of mind deficits of patients with schizophrenia, in the light of current results, it is understandable that their recollection performance reflects their own attribution intention performances. Finally, our results provide arguments for physicians and other researchers whom are constantly developing new cognitive remediation or cognitive training programs for patients with schizophrenia. While the theory of mind impairments is generally the focus of those programs, the use of a supraliminal attentional cue as proposed in the present study cannot be recommended. These programs should be more focused on higher level cognitive process such as metacognition for instance. Acknowledgements This research was partially funded by a grant from the Agence Nationale de la Recherche: ANR-11-EMCO- 0007. We are very thankful to Dr. Graziella Zanatta, Dr. Erica Martins, Elisabeth Massé, and all the members of the Adult Psychiatric Service at Versailles Hospital for their support, and their help for the participant’s recruitment, along this work.
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Appendix A
Without cuing
Eye tracking Data
Condition within cuing
Without cuing
Eye tracking Data
Condition within cuing
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Appendix B. Supplementary material Supplementary data to this article can be found online at https://doi.org/10.1016/j.concog.2018.11.007.
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