Aging, Neuropsychology, and Cognition. A Journal on Normal and Dysfunctional Development

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1 Aging, Neuropsychology, and Cognition A Journal on Normal and Dysfunctional Development ISSN: (Print) (Online) Journal homepage: Object decision test (BORB): normative data for the adult Quebec population and performance in Alzheimer s disease and the semantic variant of primary progressive aphasia Alexandre St-Hilaire, Marie-Claude Blackburn, Maximiliano A. Wilson, Robert Jr. Laforce, Carol Hudon & Joël Macoir To cite this article: Alexandre St-Hilaire, Marie-Claude Blackburn, Maximiliano A. Wilson, Robert Jr. Laforce, Carol Hudon & Joël Macoir (2017): Object decision test (BORB): normative data for the adult Quebec population and performance in Alzheimer s disease and the semantic variant of primary progressive aphasia, Aging, Neuropsychology, and Cognition, DOI: / To link to this article: View supplementary material Published online: 21 Apr Submit your article to this journal View related articles View Crossmark data Full Terms & Conditions of access and use can be found at Download by: [ ] Date: 21 April 2017, At: 05:10

2 Object decision test (BORB): Normative Data for the Adult Quebec Population and Performance in Alzheimer s Disease and the Semantic Variant of Primary Progressive Aphasia Alexandre St-Hilaire 1,2, Marie-Claude Blackburn 1,2, Maximiliano A. Wilson 2,3, Robert Jr. Laforce 4,5, Carol Hudon 1,2, Joël Macoir 2,3 1 École de psychologie, Université Laval, Québec, QC, Canada 2 Centre de recherche de l Institut universitaire en santé mentale de Québec, Québec, QC, Canada 3 Département de réadaptation, Université Laval, Québec, QC, Canada 4 Clinique Interdisciplinaire de Mémoire (CIME), CHU de Québec, Québec, QC, Canada 5 Département des Sciences Neurologiques, Université Laval, Québec, QC, Canada Corresponding author: Joël Macoir; Département de réadaptation, Faculté de médecine, Pavillon Ferdinand-Vandry, Université Laval; 1036, rue de la Médecine, Bureau 4453; Québec, QC, Canada, G1V 0A6; ASH: MCB: MAW: RJL: CH: JM: 1

3 Acknowledgements CH was supported by a salary award from the FRQ-S [26809]. Funding This work was funded by the Réseau québécois de recherche sur le vieillissement, the Canadian Institutes of Health Research (CIHR), the Alzheimer Society of Canada, the Natural Sciences and Engineering Research Council of Canada, the Canadian Institutes of Health Research, the Fonds de recherche du Québec Société et culture [FRQ-SC-2013-NP ] and the Fonds de Recherche du Québec Santé (FRQ-S). 2

4 Object decision test (BORB): Normative Data for the Adult Quebec Population and Performance in Alzheimer s Disease and the Semantic Variant of Primary Progressive Aphasia Abstract Objectives: Object decision (OD) test is one subtest of the Birmingham Object Recognition Battery (BORB). It is useful for differential diagnosis among several neurodegenerative diseases. However, normative data provided with this battery count on very few subjects and do not control for the effect of age, which limits interpretability. The purpose of Study 1 was to provide normative data for the OD test of the BORB (version A - hard). The objectives of Study 2 were to establish the diagnostic validity of this task and predictive validity of the normative data in the case of the semantic variant of primary progressive aphasia (svppa) and Alzheimer s disease (AD). Methods: Based on multiple linear regressions, equations to calculate Z-scores corrected for age were provided for 130 participants aged from 47 to 89 years. Performance of 20 healthy participants was compared to that of 14 individuals with svppa and 18 with AD. Results: After controlling for confounders, participants with svppa had a lower total score than controls and AD participants. AD participants had a poorer performance than controls only when chimeric objects were considered. Among those with a deficit on the total score of the test, 94% (17/18, including 12 with svppa) were correctly identified as having a pathological condition (svppa or AD). Discussion: This test could help refine differential diagnosis between svppa and AD patients, especially before the deficits of episodic memory show up. Key words: Norms; Object recognition; Alzheimer s disease; Primary progressive aphasia; Assessment 3

5 Introduction The object decision task assesses perceptual knowledge of the visual form of objects ( I know this to be a real/familiar thing ), i.e. the structural description that would be a gateway to the conceptual knowledge of an object. The difficulty in associating a percept to a concept is called associative agnosia and it may lead to poor performance on an object decision task. For instance, compared to healthy controls, impaired performance on object decision has been found in the case of the semantic variant of primary progressive aphasia (svppa) (Patterson et al., 2006; Rogers, Lambon Ralph, Hodges, & Patterson, 2004; Zannino et al., 2014) and, to a lesser extent, in Alzheimer s disease (AD) (Tippett, 2004; Zannino et al., 2014). However, the tasks used in most of these studies (Patterson et al., 2006; Rogers et al., 2004; Zannino et al., 2014), and particularly those used in svppa, are experimental so the stimuli are not always available for clinical use. The sole set of published normative data for an object decision test are those of the Birmingham Object Recognition Battery (BORB) (Humphreys & Riddoch, 1993). This test of the BORB battery is of interest for differential diagnosis among neurodegenerative disorders, especially when performance is considered in relation with other cognitive test scores. Indeed, the object decision test of the BORB has a significant predictive value and increases specificity (i.e., reducing false positive) in the identification of older individuals at greater risk to progress to AD (Belleville, Fouquet, Duchesne, Collins, & Hudon, 2014; Belleville, Gauthier, Lepage, Kergoat, & Gilbert, 2014). The BORB is composed of 14 subtests that assess neuropsychological disorders of visual object recognition (Humphreys & Riddoch, 1993). These subtests assess low-level aspects of visual perception (using same-different matching of basic perceptual features such as orientation, length, position, and object size), intermediate-level visual processes (e.g., overlapping figures 4

6 task), higher-level visual processes (e.g., matching objects from different viewpoints), access to stored perceptual knowledge about objects (object decision test), access to semantic knowledge (functional and associative matching), and access to names of objects (picture naming). Each of these steps can be selectively impaired, thus leading to a particular type of visual agnosia. The BORB has been validated among patients with left brain damage which have a poor performance compared to right brain damaged individuals. Nonetheless, because these normative data were derived from a very small sample of healthy participants (n = 13), which may not be representative of the healthy population, these norms present several limitations. First, due to the small sample, data are presented as a whole, and are not adjusted for the influence of sociodemographic variables. Second, normative data are presented in the form of means and standard deviations only, which leads to a non-normal distribution and difficulties to interpret extreme values. In regard to the above-mentioned limitations, normative data were derived for the object decision test of the BORB (subtest 10; version A hard), tailored for a large sample of adults from Quebec (Canada; Study 1). Also, in order to accurately discriminate between normal and pathological cognitive functioning in this population, we aimed to examine the diagnostic validity of this test and the predictive validity of the normative data for two clinical populations, svppa and AD (Study 2). STUDY 1: NORMATIVE DATA Methods Participants 5

7 Researchers from Quebec City (Canada) were invited to share anonymized data from Frenchspeaking healthy volunteers whose mother tongue was French and who had completed the object decision test of the BORB as part of other research studies approved by local Research Ethics Boards. We had consent to use the data presented in this article for secondary analyses, as stipulated in the information and consent documentation given to participants of the primary studies. All participants scored within normal range on the Montreal Cognitive Assessment (MoCA 26) (Nasreddine et al., 2005) or the Mini-Mental State Examination (MMSE 26) (Folstein, Folstein, & McHugh, 1975), indicating normal cognition. Participants had no significant depressive symptomatology based on screening results from the Geriatric Depression Scale (cut-offs were 10 for the 30-item GDS) (Yesavage, 1988). All participants self-reported good mental and physical health (i.e., no history of neurological disease, current untreated psychiatric illness, traumatic brain injury, and untreated medical conditions that could interfere with cognitive performance). The normative sample consisted of 130 community-dwelling participants (66 women and 64 men), aged between 47 and 89 years (mean age = 67.2 years; SD = 8.2) and having between 5 and 23 years of formal education (mean education level = 14.5 years; SD = 3.5). Highly educated men and women aged over 55 were overrepresented in our sample compared with actual Quebec demographics (Institut de la statistique du Québec, 2006) (Table 1). The number of women in our sample was similar to Quebec demographics (50.8% vs. 50.3% in Quebec) (Government of Canada, 2015). Material and Procedure 6

8 The object decision task of the BORB (version A hard) is a 32-item subtest in which participants are asked to look carefully at black and white line drawings of animals (n = 28) and tools (n = 4). Half the pictures are constructed by combining parts of two different animals (e.g., the body of a cow with the head of a donkey) or tools (e.g., the handles of pliers with the blades of a scissor) and thus, they represent chimeric objects. The other half of the pictures consists in real objects. Each picture was presented one at a time on separate pages. Items were administered in the order predefined by the authors of the battery. For each item, participants were asked whether or not each picture depicted a real animal or object. Each participant had to reply yes (real) or no (unreal) as the examiner presented the drawings. They did not have to provide the names of the animals/objects. Correct answers were credited one point each. There was no time limit and it took participants about two minutes to complete the test. Figure 1 shows an example of the items of the task. The scoring sheet is available in the Appendix. Statistical Analyses To identify the possible confounders influencing performance, a multiple linear regression analysis was performed for the object decision test with age, education, and gender as predictors. Residuals for the object decision test were normally distributed (skewness and kurtosis values between -1 and 1 in absolute value) (Tabachnick & Fidell, 2013). Age and education were entered in the analyses as continuous variables, while gender was coded 0 for men and 1 for women. Interactions between predictors were tested (continuous variables were centered and interaction terms were created by multiplication: age*education, age*gender, education*gender, age*education*gender). None of the interactions were significant so they were not retained in the final models. Visual and statistical analyses were conducted to 7

9 verify the underlying assumptions of the regression models (normality of residuals, homogeneity of variance, linearity, multicollinearity and outliers using common criteria) (Tabachnick & Fidell, 2013). Inspection of the data revealed that two items of the object decision test (items 3 and 30; i.e., deer/goat and snake/tortoise) tended to have very high error rates (96.2% and 88.5%, respectively). It seems that these items are too discrete and thus go undetected even by healthy adults. However, more than 50% of participants gave good responses to all other items. Thus, these two items were excluded from the data set and the regression analysis was repeated. Both regressions with and without items 3 and 30 are presented in Table 3. All statistical analyses were performed using SPSS software (version 21.0) with the alpha level set at.05. Results Table 2 shows the characteristics of the normative sample according to its demographic variables. Table 3 illustrates the regression coefficients and intercepts for each condition. Correlations were significant between total performance on the object decision test and age (r = -.392; p <.001), but not with education (r =.063; p =.478) or gender (r pb = -.134; p =.130). With respect to performance on the object decision test without items 3 and 30, correlations were also significant with age (r = -.391; p <.001), but not with education (r =.063; p =.478) or gender (r pb = -.119; p =.177). Since education and gender did not significantly correlate with any conditions, the effects of these variables were not taken into account in the regression equations. The final model accounted for 15.3% of the variance of the total performance on the object decision test and only included age, R² =.153, F (1, 128) = , p <.001. The final model for performance on the object decision test without items 3 and 30 also accounted for 15.3% of the variance of performance (age: R² =.153, F (1, 128) = , p <.001). Based on the results 8

10 from the regression models, Table 4 reports equations to calculate Z-scores for performance on the object decision test of the BORB, according to the effect of age. In order to ease calculation of Z-scores based on the regression formulas, a Microsoft Excel spreadsheet containing automatic formulas has been prepared. Clinicians and researchers can download the file from the website of the journal (see Supplementary materials) or by writing to the corresponding author of the manuscript. Discussion The main objective of this study was to establish normative data for the object decision test of the BORB. To that end, we used a sample of 130 adults aged 47 to 89 years from Quebec (Canada). The results of linear multiple regression models indicated that neither education nor gender explained a significant proportion of the total score on the object decision test. Nevertheless, the age of participants was a significant predictor of the total score of the test. More precisely, as the age of participants increased, performance decreased. We cannot rule out the possibility that performance declines in elderly participants because the sensory system undergoes age-related changes and also is often affected by eye diseases (e.g., cataracts, glaucoma). Moreover, as other authors alleged (McKendrick, Weymouth, & Battista, 2010; Robnett, 2013), we can argue that the elderly have more difficulty to focus attention to visual details. Indeed, it has been described that, compared to younger adults, the elderly generally identify more readily global features before local ones when presented in a stimulus containing both global and local features (Gottlob & Madden, 1999). This effect, called the global interference effect, would be more pronounced during aging due to an inhibitory breakdown (Roux & Ceccaldi, 2001). Thus, it is possible that the elderly base more their judgment (real vs. chimeric object) on coarse visual information instead of details. When stimuli require attention to more fine visual details in order to decide 9

11 whether or not the object is real, the elderly would fail to recognize them as non-existing chimeric objects. Finally, in regard to the object decision test, a study showed that performance involving stored perceptual knowledge deteriorates when age increases, especially beyond 40 years of age, while semantic knowledge is preserved in older participants (Ehrle, Goudour, Legrand, & Bakchine, 2008). It was argued by these authors that the decrease in visual acuity due to aging could lead to a gradual decline in the sharpness of the stored perceptual knowledge in long-term memory. Although the current study used an incidental sampling method, the normative data presented here were built from a respectable sample of adults and older adults living in community. Since there were fewer participants with a low level of education, greater variability in scores may be present in these subsamples. Nevertheless, this seems unlikely since education did not affect performance in the present sample. More importantly, our sample did not comprise people aged 90 years and older. Thus, the application of regression formulas for people over this age should be interpreted with caution since it represents estimated scores. One should note, however, that the extent of ages of the current normative data exceeds that of Humphreys and Riddoch (1993) (which was between 50 and 80 years). Overall, contrarily to the present normative study, it is noteworthy that the effect of age was not taken into account in the original normative data (Humphreys & Riddoch, 1993), probably because of the small size of their sample (13 participants). Finally, we present normative data for the object decision test with and without the two items that were extremely error-prone for the normative sample. We argue that this limits the number of errors due to visual discrimination rather than to difficulties in associating the percept to a concept. 10

12 The use of regression equations to calculate Z-scores for performance on the object decision test has the advantage of better estimating the expected performance of a participant given his personal characteristics. To illustrate the difference between these two methods, let us imagine four participants aged 50, 60, 70, and 80, respectively. Based on the regression equations from Table 4, the participants would have a deficient performance for raw scores of 24, 23, 22, and 21, respectively (Z -1.65; 5 th percentile). If we use the normative data from Humphreys and Riddoch (1993), which are not corrected for the effect of age, all participants, no matter their age, would have a deficient performance for a raw score of 23 (Z -1.65; 5 th percentile), increasing the rate of false-positives for older adults. The present data seem therefore to better suit the specific effects of the age of the participants. STUDY 2: DIAGNOSTIC AND PREDICTIVE VALIDITY In order to accurately discriminate between normal and pathological cognitive functioning, the aim of Study 2 was to establish the diagnostic validity of the object decision test and the predictive validity of the normative data. Diagnostic validity refers to the magnitude of the deficits that can be found in clinical populations on the object decision test, by comparing their performance to those of control participants. Predictive validity is the usefulness of the test to classify participants on a binary classifier system (e.g., healthy, not healthy). Methods Participants 11

13 To establish the diagnostic validity of the test, data from 18 participants with probable AD and 14 participants with svppa were compared to those of a subsample of 20 healthy participants. To establish the predictive validity, data from the same three groups were compared. The subsample of healthy participants was randomly generated using the SPSS COMPUTE command, which selected a random sample among participants of Study 1 approaching the assigned value (n = 20), considering the number of subjects in the clinical conditions. These 20 healthy people were not included in the normative data in Study 1. They were between 50 and 84 years old and had between 4 and 23 years of formal education. One should note that these participants did not differ significantly from the normative sample in terms of age (p =.741), education (p =.350), gender (p =.827), general cognition on MoCA (p =.972), and raw score for total performance on the object decision test with all 32 items (p =.664) and without items 3 and 30 (p =.613). AD is a neurodegenerative disease characterized by a disproportionate atrophy in the medial, basal, and lateral temporal lobe, and in the medial parietal cortex (McKhann et al., 2011). Probable AD was determined according to current diagnostic criteria (McKhann et al., 2011) and based on medical records and history (e.g., diagnosis of AD from a medical doctor and/or participants taking an approved pharmacological treatment for dementia [memantine, donepezil, galantamine, or rivastigmine]), consensus among clinicians and results from a comprehensive neuropsychological assessment. The neuropsychological battery comprised tests of verbal (16- item Free and Cued Recall (Dion et al., 2014; Van der Linden et al., 2004)) and non-verbal (Rey Osterrieth or Taylor Complex Figure Tests (Osterrieth, 1944; Tremblay et al., 2015)) episodic memory, language (Boston Naming Test (Kaplan, Goodglass, & Weintraub, 1983; Mack, Freed, Williams, & Henderson, 1992)), semantic memory (Pyramids and Palm Trees Test (Callahan et 12

14 al., 2010; Howard & Patterson, 1992)), visuoperceptual skills (Rey Osterrieth or the Taylor Complex Figure Tests (Osterrieth, 1944; Tremblay et al., 2015), Clock Drawing Test (Yamamoto et al., 2004), Size Match Task of the BORB (Humphreys & Riddoch, 1993)), executive functions (verbal fluency (Canadian Study of Health and Aging Working Group, 1994; St-Hilaire et al., 2016), D-KEFS Trail Making Test and Color-Word Interference Test (Delis, Kaplan, & Kramer, 2001)), and working memory/attention (WAIS-III Letter-Number Sequencing and Digit Symbol- Coding (Wechsler, 1997)). In accordance with McKhann et al. (2011), AD participants had impairment (Z -1.50) in verbal and/or non-verbal total learning or total delayed recall of recently learned information. There was also evidence of impairment in at least one other cognitive domain. The mean performance on the MoCA was 19.6 (SD = 3.1), which is equivalent to a MMSE score of (Saczynski et al., 2015; Trzepacz, Hochstetler, Wang, Walker, & Saykin, 2015). Also, all AD participants had a functional impairment as revealed by the Alzheimer s Disease Cooperative Study/Activities of Daily Living scale, based on the information provided by the participant and an informant/caregiver (Galasko et al., 1997). AD diagnosis was not applied when there was evidence of a stroke temporally related to the onset or worsening of the cognitive impairment or prominent features of other dementia as those stated by McKhann et al. (2011). The svppa is also a neurodegenerative disease characterized by atrophy, usually more extensive in the left hemisphere, of the anterior temporal lobes (Gorno-Tempini et al., 2011). The diagnosis of probable svppa was based on the most recent criteria for diagnosis of PPA (Gorno- Tempini et al., 2011) according to neuropsychological testing and clinical judgment of three authors of this paper (JM, MAW, RJL), who are speech-language pathologist, neuropsychologist, and behavioral neurologist, respectively. In accordance with Gorno-Tempini et al. (2011), the 13

15 most prominent clinical feature of svppa was difficulty with word-finding, word meaning and multi-modal semantic processing. Moreover, associative agnosia is commonly observed in svppa (Kertesz, Jesso, Harciarek, Blair, & McMonagle, 2010) and figured among the criteria for semantic dementia (i.e., previous name of svppa) proposed by Neary et al. (1998). The mean score of participants with svppa on the MoCA was 19.2 (SD = 2.9; MMSE equivalent to 24-25). Material and procedure The object decision test of the BORB was administered to all subjects (healthy, AD, svppa) using the same procedure and scoring method as in Study 1. Statistical Analyses We compared the total performance between healthy, AD, and svppa participants with ANCOVAs controlling for age, education, and general cognition as assessed with the MoCA. Gender was not significantly correlated with any dependant variables listed in Table 5 for AD, svppa, or healthy participants so it was not included in the ANCOVAs. In addition to the traditional p-values, the effect sizes (partial eta squared; η 2 p ) are also reported. Like R 2, partial eta squared values indicate the proportion of the variance explained by the main factor (e.g., diagnosis) when the effect of the other factors is controlled (e.g., age, education, global cognition). They were computed as follow: systematic variance of a factor/(systematic variance of a factor + error variance). Partial eta squared values ranging from 0.01 to 0.06 indicate a small effect of the main factor while eta squared ranging from 0.06 to 0.14 and higher than 0.14 indicate moderate and strong effects, respectively (Cohen, 1988). Cohen s d effect sizes, calculated as the difference of the means of two groups divided by the weighted pooled standard deviations of these groups, are also reported in Table 5, in order to quantify the magnitude of the 14

16 difference between conditions on the BORB s object decision test (i.e., healthy vs. AD, healthy vs. svppa, AD vs. svppa). Cohen s d ranging from 0.20 to 0.50 indicate small effect of a factor on performance while Cohen s d ranging from 0.50 to 0.80 and 0.80 and higher suggest moderate and large effects, respectively (Cohen, 1988). Results Sociodemographic data for the three groups appear in Table 5. AD participants were older than the two other groups, but educational level was similar among groups. General cognition was better for healthy participants, but very close to the two clinical groups. Post hoc analyses following an ANCOVA controlling for the effect of age, education, and general cognition showed a significant effect of diagnosis on performance on the object decision test (Table 5). With respect to diagnostic validity, participants with svppa showed a significantly poorer total performance (raw score on 32) in comparison with those with AD or controls (mean = 19.2, 23.8, and 26.1, respectively, F (2, 46) = 7.599, p =.001, η 2 p = 0.25). The same pattern of results was found for the object decision test when items 3 and 30 were removed (mean = 18.9, 23.3, and 25.9, respectively, F (2, 46) = 7.770, p =.001, η 2 p = 0.25). When performance only for chimeric objects (raw score on 16) was tested, once again, participants with svppa had a significantly lower performance than AD and healthy participants (mean = 6.2, 9.7, 12.4, respectively, F (2, 46) = 6.337, p =.004, η 2 p = 0.22). Although the total performance (/32) of participants with AD did not significantly differ from that of healthy controls, the former showed a significantly lower performance than healthy participants when only chimeric objects (/16) were considered. Concerning predictive validity, when using our normative data at a cut-score of SD (5 th percentile; both with and without items 3 and 30), the detection of svppa among healthy 15

17 participants was excellent (accuracy: 91%; sensitivity: 86%; specificity: 95%). In AD, specificity was elevated, but sensitivity was poorer (accuracy: 63%; sensitivity: 28%; specificity: 95%). Overall, among those with a deficit (Z -1.65) on the total object decision test, the percentage of participants who were correctly identified as having a pathological condition (svppa or AD) was very high (positive predictive value: 94%; 17/18). Among those with a performance above SD, 56% (19/34; negative predictive value) of participants were correctly identified as cognitively healthy. Discussion The objective of Study 2 was to verify the capacity of the BORB s object decision test and our normative data to detect differences in performance between healthy participants, individuals with AD, and those with svppa. Almost all patients (12/14) with svppa had a performance below SD (5 th percentile). It is noteworthy that two svppa patients achieved a score closer to that of healthy controls (Z = and -0.53). This could be due to the fact that only two options (YES/NO) were available for each item. This might have facilitated a score above chance by simply guessing. Nonetheless, our normative data detected large deficits on the object decision test for most svppa participants. This provides validity to the current normalization. Patients with svppa typically show associative agnosia and impaired object knowledge (Kertesz et al., 2010; Neary et al., 1998). In the object decision test, after controlling for the effect of age, education, and general cognition, participants with svppa had poorer performance on this task in comparison to both AD and healthy participants. Moreover, performance for chimeric objects was clearly affected, while performance for real objects was not affected. Similar results were found in other studies that compared svppa and healthy controls on other object decision tasks (Adlam et al., 2006; Patterson et al., 2006; Rogers et al., 2004). As suggested by Zannino et al. 16

18 (2014), performance on experimental object decision tests was impaired in svppa, particularly for chimeric objects. This could be explained by the fact that these patients may rely on verbalizable rules to solve the task (e.g., items could be endorsed/rejected based on the ability to name them or name their two component parts, meaning that if only one component can be named, the item is endorsed as real). Nonetheless, the faulty verbally-based semantic representations in svppa would prevent the affected individuals to perform well. On the opposite, in an alternative version of the object decision task in which the drawings were not an arrangement of component parts of different objects, but rather deformed real objects, individuals with svppa performed better because the contribution of verbal knowledge was reduced in solving the task (Zannino et al., 2014). Thus, it seems that patients with svppa show difficulty in recognizing an amalgam of combined objects, but not distorted objects. This seems to be a consequence of the progressive semantic deterioration (or disconnection from structural descriptions) involving atrophy of the anterior temporal lobes, especially on the left side (Adlam et al., 2006; Patterson et al., 2006; Rogers et al., 2004; Zannino et al., 2014). An alternative explanation comes from Postle (2015) who postulated that high-level visual perception deterioration in svppa may be due to the early deterioration of the anterior temporal lobes This would, in turn, impact the functioning of the inferior and lateral temporo-occipital cortex. However, there is still ongoing debate on whether the poor performance on object decision tasks in svppa is due to the degradation of stored perceptual knowledge about objects or is the indirect result of a breakdown of semantic memory. This debate is beyond the scope of the present study and has been addressed in previous studies (Patterson et al., 2006; Rogers et al., 2004; Zannino et al., 2014). 17

19 In the present study, AD participants showed comparable performance on the total score of the BORB s object decision test in comparison to healthy participants. Tippett, Blackwood, and Farah (2003) also showed a non-significant difference between AD and healthy adults on the object decision test of the BORB after having controlled for the effect of impairment in low-level aspects of perception. Indeed, in AD, brain areas V4 and V2 of the visual cortex are suspected to generate weakened or distorted visual input of basic shapes, which may slightly impact higherlevel recognition (Tippett, 2004; Tippett et al., 2003). However, when only chimeric objects were studied, we found that the performance was affected in AD in comparison to healthy sample, while it was preserved for the detection of real objects. Beyond the above-mentioned possible low-level visual perceptual deficits, patients with AD often have a semantic deficit, although less apparent or less severe than that of svppa patients (Zannino et al., 2014). The better performance of persons with AD on the object decision test, in comparison to svppa, may be due to the relative preservation of the anterior temporal and occipital lobes in the initial stages of AD, and to a greater heterogeneity of the cognitive profiles among individuals. Indeed, the initial stages of AD are more associated with deterioration of the medial, basal, and lateral temporal lobes (Johnson, Fox, Sperling, & Klunk, 2012; McKhann et al., 2011). Although sensitivity was poor in AD, the object decision test could nonetheless be useful in the detection of AD patients since it was previously shown to be among the six tests that led to the best overall diagnostic accuracy between progressive and stable mild cognitive impairment (MCI) when followed over 4.5 years (Belleville, Fouquet, et al., 2014; Belleville, Gauthier, et al., 2014). Indeed, while a deficit in episodic memory increases sensitivity for progressive MCI, deficits on the perceptual domain are thought to increase specificity (Belleville, Gauthier, et al., 2014). 18

20 Although the performance on object decision differs between the groups under study, the inclusion of a lower-level visual task, such as those contained in the BORB, could have shed some light onto the discussion about the cognitive mechanism involved in a higher level visual processing task. Another peculiarity is that AD participants had a better performance than svppa when only real objects of the BORB were analysed, while healthy participants did not had a better performance in comparison to clinical samples. This is probably a difference due to the heterogeneity of the performance in AD. It should be kept in mind that AD and svppa are not homogeneous subgroups in terms of deficits, especially AD. However, all AD and svppa participants were administered the MoCA and we controlled for the effect of global cognition on performance. Although the sample of AD participants is small, the sample of svppa is appreciable compared to previous studies (n < 10). The overall performance of these two clinical populations on the BORB s object decision test provided an overview of the extent of the expected deficits and could help the clinician to guide the diagnosis or encourage him to lead further investigations if the score falls below SD, which was a sign of a pathological condition for 94% of our sample. Conclusion In sum, the current article presents normative data for the BORB s object decision test in Quebec adults. This represents a valuable addition to the limited norms currently available for this test. Moreover, the test is very quick to administer, sensitive to impairments in svppa and could help refine the differential diagnosis of AD patients, especially before the deficits of episodic memory shows up. Disclosure Statement 19

21 No potential conflict of interest was reported by the authors. 20

22 References Adlam, A. L., Patterson, K., Rogers, T. T., Nestor, P. J., Salmond, C. H., Acosta-Cabronero, J., & Hodges, J. R. (2006). Semantic dementia and fluent primary progressive aphasia: two sides of the same coin? Brain, 129, doi: /brain/awl285 Belleville, S., Fouquet, C., Duchesne, S., Collins, D. L., & Hudon, C. (2014). Detecting early preclinical Alzheimer's disease via cognition, neuropsychiatry, and neuroimaging: qualitative review and recommendations for testing. Journal of Alzheimer's disease, 42, S doi: /jad Belleville, S., Gauthier, S., Lepage, E., Kergoat, M. J., & Gilbert, B. (2014). Predicting decline in mild cognitive impairment: a prospective cognitive study. Neuropsychology, 28, doi: /neu Callahan, B. L., Macoir, J., Hudon, C., Bier, N., Chouinard, N., Cossette-Harvey, M.,... Potvin, O. (2010). Normative data for the Pyramids and Palm Trees Test in the Quebec-French population. Archives of Clinical Neuropsychology, 25, doi: /arclin/acq013 Canadian Study of Health and Aging Working Group. (1994). Canadian study of health and aging: study methods and prevalence of dementia. Canadian Medical Association Journal, 150, Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ, USA: Erlbaum Associates. Delis, D. C., Kaplan, E., & Kramer, J. H. (2001). Delis-Kaplan Executive Function System (D KEFS) Examiner s manual. San Antonio: TX: The Psychological Corporation. Dion, M., Potvin, O., Belleville, S., Ferland, G., Renaud, M., Bherer, L.,... Hudon, C. (2014). Normative data for the Rappel libre/rappel indicé à 16 items (16-item Free and Cued Recall) in the elderly Quebec-French population. The Clinical Neuropsychologist, 28, doi: / Ehrle, N., Goudour, A., Legrand, A., & Bakchine, S. (2008). Vieillissement normal : vers une dégradation des représentations structurales, auditives et visuelles, des objets? [Towards a deterioration of the structural and perceptive representations of objects in physiological aging?]. Psychologie & NeuroPsychiatrie du vieillissement, 6, doi: /pnv Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, doi: / (75) Galasko, D., Bennett, D., Sano, M., Ernesto, C., Thomas, R., Grundman, M., & Ferris, S. (1997). An inventory to assess activities of daily living for clinical trials in Alzheimer's disease. The Alzheimer's Disease Cooperative Study. Alzheimer Disease and Associated Disorders, 11, S doi: / Gorno-Tempini, M. L., Hillis, A. E., Weintraub, S., Kertesz, A., Mendez, M., Cappa, S. F.,... Grossman, M. (2011). Classification of primary progressive aphasia and its variants. Neurology, 76, doi: /wnl.0b013e e6 Gottlob, L. R., & Madden, D. J. (1999). Age differences in the strategic allocation of visual attention. Journals of Gerontology. Series B, Psychological Sciences and Social Sciences, 54, P doi: /geronb/54b.3.p165 21

23 Government of Canada. (2015). Population by sex and age group, by province and territory (Proportion of, female). Statistics Canada. Retrieved from Howard, D., & Patterson, K. (1992). The Pyramids and Palm Trees Test: A test for semantic access from words and pictures. Bury St Edmunds: Thames Valley Test Company. Humphreys, G. W., & Riddoch, J. M. (1993). Birmingham Object Recognition Battery (BORB): Psychology Press. Institut de la statistique du Québec. (2006). Population de 25 ans et plus, selon le plus haut degré de scolarité atteint, le sexe et le groupe d âge [Population aged 25 and over by highest level of education attained, sex and age group]. Retrieved from Johnson, K. A., Fox, N. C., Sperling, R. A., & Klunk, W. E. (2012). Brain imaging in Alzheimer disease. Cold Spring Harbor Perspectives in Medicine, 2. doi: /cshperspect.a Kaplan, E. F., Goodglass, H., & Weintraub, S. (1983). The Boston Naming Test. Philadelphia: Lea & Febiger. Kertesz, A., Jesso, S., Harciarek, M., Blair, M., & McMonagle, P. (2010). What is semantic dementia?: a cohort study of diagnostic features and clinical boundaries. Archives of Neurology, 67, doi: /archneurol Mack, W. J., Freed, D. M., Williams, B. W., & Henderson, V. W. (1992). Boston Naming Test: shortened versions for use in Alzheimer's disease. Journal of Gerontology, 47, P doi: /geronj/47.3.p154 McKendrick, A. M., Weymouth, A. E., & Battista, J. (2010). The effect of normal aging on closed contour shape discrimination. Journal of Vision, 10, doi: / McKhann, G. M., Knopman, D. S., Chertkow, H., Hyman, B. T., Jack, C. R., Jr., Kawas, C. H.,... Phelps, C. H. (2011). The diagnosis of dementia due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimer's & Dementia, 7, doi: /j.jalz Nasreddine, Z. S., Phillips, N. A., Bédirian, V., Charbonneau, S., Whitehead, V., Collin, I.,... Chertkow, H. (2005). The Montreal Cognitive Assessment, MoCA: A Brief Screening Tool For Mild Cognitive Impairment. Journal of the American Geriatrics Society, 53, doi: /j x Neary, D., Snowden, J. S., Gustafson, L., Passant, U., Stuss, D., Black, S.,... Benson, D. F. (1998). Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology, 51, doi: /wnl Osterrieth, P. A. (1944). Le test de copie d'une figure complexe; contribution à l'étude de la perception et de la mémoire. [Test of copying a complex figure; contribution to the study of perception and memory.]. Archives de Psychologie, 30, Patterson, K., Lambon Ralph, M. A., Jefferies, E., Woollams, A., Jones, R., Hodges, J. R., & Rogers, T. T. (2006). "Presemantic" cognition in semantic dementia: six deficits in search of an explanation. Journal of Cognitive Neuroscience, 18, doi: /jocn Postle, B. R. (2015). Semantic Long Term Memory. In B. R. Postle (Ed.), Essentials of Cognitive Neuroscience (pp ): John Wiley & Sons. 22

24 Robnett, R. H. (2013). Analyzing the effect of aging on occupation with an emphasis on cognition and perception. In J. C. O'Brien & J. W. Solomon (Eds.), Occupational analysis and group process. St. Louis, Mo: Elsevier. Rogers, T. T., Lambon Ralph, M. A., Hodges, J. R., & Patterson, K. (2004). Natural selection: The impact of semantic impairment on lexical and object decision. Cognitive Neuropsychology, 21, doi: / Roux, F., & Ceccaldi, M. (2001). Does aging affect the allocation of visual attention in global and local information processing? Brain and Cognition, 46, doi: /brcg Saczynski, J. S., Inouye, S. K., Guess, J., Jones, R. N., Fong, T. G., Nemeth, E.,... Marcantonio, E. R. (2015). The Montreal Cognitive Assessment: Creating a Crosswalk with the Mini- Mental State Examination. Journal of the American Geriatrics Society, 63, doi: /jgs St-Hilaire, A., Hudon, C., Vallet, G. T., Bherer, L., Lussier, M., Gagnon, J. F.,... Macoir, J. (2016). Normative data for phonemic and semantic verbal fluency test in the adult French-Quebec population and validation study in Alzheimer's disease and depression. The Clinical Neuropsychologist, 30, doi: / Tabachnick, B. G., & Fidell, L. S. (2013). Using multivariate statistics (6th ed ed.). Boston: Pearson Education. Tippett, L. J. (2004). From segmentation to imagination: testing the integrity of the ventral visual processing pathway in Alzheimer's disease. In A. Cronin-Golomb & P. R. Hof (Eds.), Vision in Alzheimer's disease (Vol. 34, pp ). Basel: Karger. Tippett, L. J., Blackwood, K., & Farah, M. J. (2003). Visual object and face processing in mildto-moderate Alzheimer's disease: from segmentation to imagination. Neuropsychologia, 41, doi: /s (02) Tremblay, M. P., Potvin, O., Callahan, B. L., Belleville, S., Gagnon, J. F., Caza, N.,... Macoir, J. (2015). Normative data for the Rey-Osterrieth and the Taylor complex figure tests in Quebec-French people. Archives of Clinical Neuropsychology, 30, doi: /arclin/acu069 Trzepacz, P. T., Hochstetler, H., Wang, S., Walker, B., & Saykin, A. J. (2015). Relationship between the Montreal Cognitive Assessment and Mini-mental State Examination for assessment of mild cognitive impairment in older adults. BMC Geriatrics, 15, 107. doi: /s Van der Linden, M., Coyette, F., Poitrenaud, J., Kalafat, M., Calicis, F., Wyns, C.,... Membres du GREMEM. (2004). L épreuve de rappel libre/rappel indicé à 16 items (RL/RI-16). In M. Van der Linden, S. Adam, A. Agniel, & Membres du GRENEM (Eds.), L'évaluation des troubles de la mémoire : présentation de quatre tests de mémoire épisodique avec leur étalonnage (pp ). Marseille: Solal. Wechsler, D. (1997). WAIS-III Wechsler Adult Intelligence Scale (3e ed.). San Antonio, TX: The Psychological Corporation. Yamamoto, S., Mogi, N., Umegaki, H., Suzuki, Y., Ando, F., Shimokata, H., & Iguchi, A. (2004). The clock drawing test as a valid screening method for mild cognitive impairment. Dementia and Geriatric Cognitive Disorders, 18, doi: / Yesavage, J. A. (1988). Geriatric Depression Scale. Psychopharmacology Bulletin, 24, Zannino, G. D., Perri, R., Monaco, M., Caltagirone, C., Luzzi, S., & Carlesimo, G. A. (2014). The special status of verbal knowledge in semantic memory: evidence from performance 23

25 of semantically impaired subjects on verbalizable and non-verbalizable versions of the object decision task. Brain and Language, 128, doi: /j.bandl

26 Table 1. Highest education level reached (% of the population) in the present sample compared to actual Quebec demographics Age No high-school diploma Present sample At least high-school diploma Education No high-school diploma Quebec demographics At least high-school diploma Note. The second and third left columns contain the proportion of participants in the sample, while the last two columns contain the percentages of people in the Quebec population having the indicated age and education (Institut de la statistique du Québec, 2006). 26

27 Table 2. Distribution of participants in the normative sample (n = 130) Characteristics N (%) Age (7.7) (13.1) (21.5) (23.1) (14.6) (16.2) (3.8) Gender (men/women) 64/66 (49.2/50.8) Education Elementary (5-7 years) 3 (2.3) High-School (8-12 years) 40 (30.8) College (13-14 years) 24 (18.5) University undergraduate 37 (28.5) (15-17 years) University graduate 16 (12.3) (18-19 years) University postgraduate 10 (7.6) (20-23 years) 27

28 Table 3. Coefficients for multiple linear regression analyses Variable B β t p Object decision test (subtest 10) All test items a Age ,817 <.001 Object decision test (subtest 10) Items 3 and 30 excluded b Age <.001 Notes: a Intercept = ; Square root of the mean square residual = b Intercept = ; Square root of the mean square residual = 2.294; see the text for an explanation regarding exclusion of items 3 and

29 Table 4. Normative equations to calculate corrected Z-scores for age on the object decision test of the BORB Variable n Corrected Z-score for age All test items (/32) 130 Raw score [ (-0.120*Age)] / Items 3 and 30 excluded (/30) 130 Raw score [ (-0.118*Age)] / Notes. Age: participant s age (continuous variable; between 47 and 89). Equation denominators corresponded to residual standard deviations of each models. For example, for a 60-year-old person with a raw score of 26, the equation (/32) should be: Z-score = 26 - [ (-0.120*60)] / =

30 Table 5. Comparison of participants with Alzheimer s disease, the semantic variant of primary progressive aphasia and healthy participants on sociodemographic variables and the object decision test of the BORB Characteristics Healthy (n = 20) AD (n = 18) svppa (n = 14) p Effect size (Cohen s d) H vs. AD H vs. svppa AD vs. svppa Sociodemographic Age, mean (SD) 67.9 (8.5) 74.9 (7.6) 65.1 (10.0).006 a 0.87* * Education, mean (SD) 13.7 (4.9) 13.9 (2.9) 16.1 (4.4).219 a Female, n (%) 10 (50.0) 7 (38.9) 2 (14.3).100 b MoCA, mean (SD) d 27.8 (1.6) 19.6 (3.1) 19.2 (2.9) <.001 a 3.34* 3.86* 0.11 Object decision test All test items, /32, mean (SD) 26.1 (2.6) 23.8 (4.0) 19.2 (3.7).001 c * 1.19* Items 3 and 30 excluded, /30, mean (SD) 25.9 (2.6) 23.3 (3.8) 18.9 (3.9).001 c * 1.17* Chimeric objects, /16, mean (SD) 12.4 (1.4) 9.7 (3.6) 6.2 (2.7).004 c 1.03* 3.07* 1.08* Real objects, /16, mean (SD) 13.6 (1.8) 14.2 (1.7) 13.0 (1.7).046 c * Notes. H = Healthy; AD = Alzheimer s disease; svppa = Semantic variant of primary progressive aphasia Cohen s d: 0.20 to 0.50 = small effect; 0.50 to 0.80 = moderate effect; 0.80 and higher = large effect (Cohen, 1988). a One-way ANOVA; b Chi-square; c ANCOVA controlling for effect of age, education and general cognition (MoCA); d MMSE scores equivalent to 30 (healthy) and 24 (AD and svppa) (Saczynski et al., 2015) * = significant Sidak post-hoc analysis for one-way ANOVA and one-way ANCOVA. 30

31 Figure 1. Sample stimuli The drawing on the left side represents an unreal animal while the one on the right side depicts a real animal (Humphreys & Riddoch, 1993, pages 164 and 185). Reproduced with the permission of Psychology Press, Taylor and Francis Group and the authors. 31

32 16 A. ST-HILAIRE ET AL. Appendix Scoring sheet for the object decision test of the BORB (version A hard) English Verbatim instructions: I will show you drawings of animals and tools. Is this [animal or tool] real or not? Does it exist in this way in real life? [Repeat the instruction as many times as necessary to ensure that the patient understands the task. Get the patient s attention to the drawings to avoid perseverations in his responses.] Français Consignes verbales: Je vais vous montrer des dessins d animaux et d objets. Est-ce que cet [animal ou outil] est réel ou non? Existe-t-il sous cette forme dans la vraie vie? [Répétez les consignes autant de fois que nécessaire pour vous assurer de la bonne compréhension de la tâche par le patient. Assurez-vous d attirer l attention du patient sur chaque dessin pour éviter les réponses persévératives.] Page N Target (Cible) Yes (Oui) No (Non) Camel (Chameau) Cow/Donkey (Vâche/Âne) Deer/Goat (Cerf/Chèvre) Dog/Donkey (Chien/Âne) Goat/Deer (Chèvre/Cerf) Cockerel (Jeune coq) Horse/Fox (Cheval/Renard) Lion/Monkey (Lion/Singe) Donkey (Âne) Pliers/Scissors (Pinces/Ciseaux) Scissors/Pliers (Ciseaux/Pinces) Duck (Canard) Giraffe (Girafe) Horse (Cheval) Screwdriver/Screw (Tournevis/Vis) Seal/Sheep (Phoque/Mouton) Kangaroo (Kangourou) Sheep/Seal (Mouton/Phoque) Leopard (Léopard) Monkey (Singe) Swan/Tortoise (Cygne/Tortue) Mouse (Souris) Pig (Cochon) Rabbit (Lapin) Rhino/Sheep (Rhinocéros/Mouton) Screwdriver (Tournevis) Seahorse (Hippocampe) Tortoise/Snake (Tortue/Serpent) Zebra/Tiger (Zèbre/Tigre) Snake/Tortoise (Serpent/Tortue) Squirrel (Écureuil) Tiger (Tigre)

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