Cognition and Emotion

ISSN: 0269-9931 (Print) 1464-0600 (Online) Journal homepage: http://www.tandfonline.com/loi/pcem20

Visuospatial and mathematical dysfunction in major depressive disorder and/or panic disorder: A study of parietal functioning Brady D. Nelson & Stewart A. Shankman To cite this article: Brady D. Nelson & Stewart A. Shankman (2015): Visuospatial and mathematical dysfunction in major depressive disorder and/or panic disorder: A study of parietal functioning, Cognition and Emotion, DOI: 10.1080/02699931.2015.1009003 To link to this article: http://dx.doi.org/10.1080/02699931.2015.1009003

Published online: 24 Feb 2015.

Submit your article to this journal

Article views: 114

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=pcem20 Download by: [University of Sheffield]

Date: 05 November 2015, At: 17:15

COGNITION AND EMOTION, 2015 http://dx.doi.org/10.1080/02699931.2015.1009003

Visuospatial and mathematical dysfunction in major depressive disorder and/or panic disorder: A study of parietal functioning Brady D. Nelson1 and Stewart A. Shankman2 1

Department of Psychology, Stony Brook University, Stony Brook, NY, USA Department of Psychology, University of Illinois at Chicago, Chicago, IL, USA

2

Downloaded by [University of Sheffield] at 17:15 05 November 2015

(Received 16 July 2014; accepted 9 January 2015)

The parietal cortex is critical for several different cognitive functions, including visuospatial processing and mathematical abilities. There is strong evidence indicating parietal dysfunction in depression. However, it is less clear whether anxiety is associated with parietal dysfunction and whether comorbid depression and anxiety are associated with greater impairment. The present study compared participants with major depression (MDD), panic disorder (PD), comorbid MDD/PD and controls on neuropsychological measures of visuospatial processing, Judgement of Line Orientation (JLO), and mathematical abilities, Wide Range Achievement Test (WRAT) Arithmetic. Only comorbid MDD/PD was associated with decreased performance on JLO, whereas all psychopathological groups exhibited comparably decreased performance on WRAT Arithmetic. Furthermore, the results were not accounted for by other comorbid disorders, medication use or psychopathology severity. The present study suggests comorbid depression and anxious arousal are associated with impairment in visuospatial processing and provides novel evidence indicating mathematical deficits across depression and/or anxiety. Implications for understanding parietal dysfunction in internalising psychopathology are discussed. Keywords: Anxiety; Depression; Mathematical abilities; Parietal cortex; Visuospatial processing.

The interplay between cognition and emotion is critical to various forms of psychopathology. The parietal cortex is one region that is important for emotional arousal (Heller, 1993; Heller, Nitschke, Etienne, & Miller, 1997), and there is evidence that variations in arousal can interfere with cognitive functions that share similar neural substrates. For example, Shackman et al. (2006) found that threatof-shock increased physiological arousal and selectively disrupted cognitive processes (e.g., visuospatial

working memory) that are asymmetrically associated with the right frontal and parietal regions. The authors in that article suggested that the task-irrelevant arousal competed for limited resources with ongoing cognitive functions that also involved the right parietal region. Therefore, conditions characterised by aberrant emotional arousal may be particularly vulnerable to disruptions in parietal functions. There is a robust literature indicating parietal dysfunction in depression. Indeed, several studies

Correspondence should be addressed to: Stewart A. Shankman, Department of Psychology, University of Illinois at Chicago, 1007 W. Harrison St. (M/C 285), Chicago, IL 60607, USA. E-mail: [email protected] © 2015 Taylor & Francis

1

Downloaded by [University of Sheffield] at 17:15 05 November 2015

NELSON AND SHANKMAN

have tested the hypothesis of low-emotional arousal in depression using parietal electroencephalography (EEG) asymmetry and shown that a reduced relative right parietal EEG asymmetry is associated with increased depressive symptoms (Blackhart, Minnix, & Kline, 2006; Rabe, Debener, Brocke, & Beauducel, 2005) and differentiates remitted depression from controls (Henriques & Davidson, 1990; Stewart, Towers, Coan, & Allen, 2011). However, some investigations have failed to find an association between parietal EEG asymmetry and depression (Debener et al., 2000; Henriques & Davidson, 1991; Nitschke, Heller, Palmieri, & Miller, 1999; Schaffer, Davidson, & Saron, 1983). One possible explanation for the mixed findings is unmeasured comorbid anxiety, which is posited to be associated with increased emotional arousal. Indeed, several studies have reported that comorbid depression and anxiety are associated with a greater relative right parietal EEG asymmetry (Bruder et al., 1997; Kentgen et al., 2000; Mathersul, Williams, Hopkinson, & Kemp, 2008; Metzger et al., 2004). Other studies have examined parietal dysfunction in depression and anxiety using neuropsychological measures of perceptual asymmetry. For example, several investigations have used the chimeric faces task (Levy, Heller, Banich, & Burton, 1983) to examine hemispatial bias, such that changes in left hemispatial bias indicate changes in right parietal activity (Green, Morris, Epstein, West, & Engler, 1992). As expected, depression has been associated with a reduced left hemispatial bias (i.e., reduced right parietal activity) and anxiety has been associated with an increased left hemispatial bias (i.e., increased right parietal activity; Heller, Etienne, & Miller, 1995; Jaeger, Borod, & Peselow, 1987; Keller et al., 2000). Perceptual asymmetry has also been examined using dichotic listening tasks, as the difference in performance accuracy to the left and right ears provides information on hemispheric lateralisation. Across several studies depression has been associated with a greater right ear advantage (i.e., decreased right temporoparietal activity) and anxiety disorders have been associated with a greater left ear advantage (i.e., increased right temporoparietal activity; Bruder, Wexler, Stewart, Price, & Quitkin, 1999; Pine et al.,

2

COGNITION AND EMOTION, 2015

2000; Wexler & Goodman, 1991). Furthermore, in one of the most thorough dichotic listening investigations using Diagnostic and Statistical Manual of Mental Disorders (DSM)-determined diagnoses, Bruder, Schneier, Stewart, McGrath, and Quitkin (2004) found that anxiety with or without a comorbid depressive disorder was associated with a smaller right ear advantage (consistent with decreased left parietal activity) relative to depression only and controls. Despite the supporting evidence, there are still limitations to the literature on parietal functioning in depression and anxiety. First, several theorists have distinguished between two subtypes of anxiety disorders or dimensions—anxious apprehension [e.g., generalised anxiety disorder (GAD)] and anxious arousal [e.g., panic disorder (PD)], and suggested that the former is associated with increased left frontal regions while the latter is associated with increased right parietal regions (Heller & Nitscke, 1998; Heller et al., 1997). Few studies have examined the role of comorbid anxious arousal and those that did largely relied on self-report symptoms in non-clinical samples. Second, the literature on depression and anxiety and parietal functioning has primarily focused on measures of EEG and perceptual asymmetry. The parietal cortex is critical for a number of different cognitive functions, including attention, executive functioning, mathematical abilities and visuospatial processing (Collette et al., 2005; Constantinidis, Bucci, & Rugg, 2013; Kolb & Whishaw, 1996; Malhotra, Coulthard, & Husain, 2009; Rivera, Reiss, Eckert, & Menon, 2005). There is also strong evidence for hemispheric lateralisation for several of these functions. For example, right parietal regions have been associated with visuospatial processing in neuroimaging (Clements et al., 2006; Deutsch, Bourbon, Papanicolaou, & Eisenberg, 1988) and lesion studies (Tranel, Vianna, Manzel, Damasio, & Grabowski, 2009; Treccani, Torri, & Cubelli, 2005). Conversely, left parietal regions have been associated with mathematical abilities in neuroimaging (Chochon, Cohen, van de Moortele, & Dehaene, 1999), lesion (Boller & Grafman, 1983; Jackson & Warrington, 1986) and cortical stimulation studies (Whalen, McCloskey, Lesser, & Gordon, 1997). While the right parietal–

Downloaded by [University of Sheffield] at 17:15 05 November 2015

A STUDY OF PARIETAL FUNCTIONING

visuospatial association has been more robustly found than the left parietal–math association, acalculia (a disorder in math abilities) has been consistently reported in patients suffering lesions in left parietal regions (particularly the angular gyrus) relative to other regions (Mayer et al., 2003). Additionally, it is important to highlight that these (and other) cognitive functions involve additional regions outside the left and right parietal cortices (Ng et al., 2000; Pinel & Dehaene, 2010), respectively, and are affected by dysfunction in other brain areas. To date, a small number of studies have found an association between depression and impaired visuospatial processing (Coello, Ardila, & Rosselli, 1990; Paradiso, Hermann, Blumer, Davies, & Robinson, 2001) and mathematical performance (Lagace, Kutcher, & Robertson, 2003). However, it is unclear whether anxiety disorders characterised by heightened emotional arousal (e.g., PD, a disorder often associated with heightened anxious arousal, McNally, 2002) are also associated with these cognitive deficits and whether comorbid depression and anxiety are associated with greater impairment. The present study aimed to address these limitations and compared participants with DSM-IV diagnosed: (1) major depressive disorder (MDD) without a lifetime history of an anxiety disorder, (2) PD without a lifetime history of depression, (3) comorbid MDD and PD and (4) healthy controls on two separate tasks that measured visuospatial processing, Benton’s Judgement of Line Orientation (JLO) test (Benton, Varney, & Hamsher, 1978), and mathematical abilities, the Wide Range Achievement Test—3 (WRAT-3) Arithmetic subtest (Wilkinson, 1993). This study was designed to extend the extant EEG and perceptual asymmetry literature on parietal functioning in depression in a novel way—by using alternative neuropsychological measures that primarily involve parietal cognitive functions

(visuospatial and mathematical abilities) and a well-defined clinical sample that allowed for comparison of the independent and interactive effects of depression and anxious arousal on parietal functioning. The present study had two primary hypotheses. First, the study hypothesised that MDD (with or without comorbid PD) would be associated with decreased performance on the JLO. However, few studies that have examined comorbid depression and anxiety have generally found abnormal right parietal activity in comorbid relative to “pure” depressed groups (Bruder et al., 1997; Kentgen et al., 2000; Mathersul et al., 2008; Metzger et al., 2004). It is therefore possible that only comorbid MDD and PD will be associated with decreased performance on JLO. Second, only a few studies have specifically examined left parietal functioning in depression and anxiety and in those that did, the conditions were associated with impaired performance (Bruder et al., 2004; Lagace et al., 2003). Therefore, we tentatively hypothesised that both MDD and/or PD would be associated decreased performance on WRAT Arithmetic.

METHOD Participants The sample consisted of 39 individuals with current MDD and no current or lifetime history of an anxiety disorder (MDD only), 27 individuals with current PD and no current or lifetime history of MDD or dysthymia (PD only), 54 individuals with current MDD and current PD (comorbid MDD/PD) and 65 controls with no lifetime history of an Axis I disorder.1 Diagnosis was examined as two 2-level factors, depression status (present vs. absent) and panic status (present vs. absent), instead of one 4-level factor in order to

1

The sample from the present study has been reported elsewhere (e.g., Shankman et al., 2013). Specifically, the larger study consisted of 191 participants, including those with current MDD only (n = 40), current PD only (n = 28), comorbid MDD/PD (n = 58) or healthy controls (n = 65). Six participants (one MDD only, one PD only and four comorbid MDD/ PD) did not complete the JLO and WRAT and were excluded from analyses. The six participants who did not complete the JLO and WRAT did not differ from the MDD-only, PD-only and comorbid MDD/PD participants who did complete the JLO and WRAT on demographics or psychopathology severity (i.e., BAI, HRSD and GAF; ps > .10). COGNITION AND EMOTION, 2015

3

Downloaded by [University of Sheffield] at 17:15 05 November 2015

NELSON AND SHANKMAN

examine main effects and interactions of MDD and PD on neuropsychological performance. Diagnoses were made via the Structured Clinical Interview for DSM-IV (First, Spitzer, Gibbon, & Williams, 2002) and based on criteria defined by the DSM-IV (American Psychiatric Association, 1994). All interview assessments were conducted by S. A. Shankman and advanced clinical psychology doctoral students who were trained to criterion by S. A. Shankman. See Shankman et al. (2013) for additional details regarding the sample and diagnostic procedures. MDD-only participants were required to have no current or past history of an anxiety disorder. PD-only and comorbid MDD/PD participants were allowed to meet criteria for additional current and past anxiety disorders. Both MDD-only and comorbid MDD/PD participants were required to have an age of onset of first depressive disorder (dysthymia or MDD) before 18, because the neuropsychological measures were administered as part of a larger study on early-onset depression (Shankman et al., 2013). Control participants were required to have a 24-item Hamilton Rating Scale for Depression (HRSD; Hamilton, 1960) and Beck Anxiety Inventory (BAI; Beck, Epstein, Brown, & Steer, 1988) score of less than 8. Seven participants (three MDD only, two PD only, one comorbid MDD/PD and one control) did not complete the BAI. Exclusion criteria included a lifetime diagnosis of schizophrenia or other psychotic disorder, bipolar disorder or dementia; inability to read or write English; history of head trauma with loss of consciousness; or being left-handed (as confirmed by the Edinburgh Handedness Inventory, range +20 to +100; Oldfield, 1971). Participants were recruited through advertising in the community (e.g., flyers, Internet postings) and mental health clinics in the greater Chicago area. All participants gave informed consent and were paid for their participation.

Neuropsychological tasks

orientation and angles of lines in space (Benton et al., 1978). The test consisted of 5 practice items followed by 30 test items. For each item, a stimulus card was shown at the top of the test booklet and a response card was shown at the bottom of the test booklet. Participants were asked to match a pair of partial-length lines appearing on the stimulus card to 2 of the 11 numbered fulllength lines appearing on the reference card. The 11 full-length lines on the reference card formed a semicircle and were separated by 18-degree intervals. A response was scored as correct only when both lines chosen on the stimulus card matched the lines on the reference card. During the practice trials, participants were corrected if they made a mistake but received no feedback during the 30 test items. The total number of correct items was out of 30 and there was no time limit to the test. The JLO has two alternate forms (H and V) that consist of the same 30 items presented in slightly different sequences. All participants completed form V. Four participants (two MDD only, one comorbid MDD/PD and one control) had JLO scores that were greater than three standard deviations below the mean and these outliers were excluded from analyses. WRAT-3 Arithmetic subtest The WRAT-3 Arithmetic subtest measures counting, basic arithmetic and written computation (Wilkinson, 1993) and consists of oral (15 items) and written (40 items) arithmetic sections. Participants were given 15 minutes to complete as many of the written arithmetic items as possible and the total number of correct items was out of 55. The WRAT-3 Arithmetic subtest has two versions (Blue and Tan). All participants completed the Tan version.

RESULTS

Judgement of Line Orientation (JLO)

Demographics and clinical characteristics

The JLO test was designed to evaluate visuospatial skills by assessing the ability to judge the

Demographics and clinical characteristics are presented in Table 1. Diagnostic groups were matched

4

COGNITION AND EMOTION, 2015

A STUDY OF PARIETAL FUNCTIONING

Downloaded by [University of Sheffield] at 17:15 05 November 2015

Table 1. Demographics and clinical characteristics

Demographics Age (years; SD) Sex (%; female) Race (%; Caucasian) Education Grade 7–12 (without graduating high school; %) Graduated high school or high school equivalent (%) Part college (%) Graduated two-year college (%) Graduated four-year college (%) Part graduate/professional school (%) Completed graduate/professional school (%) Clinical characteristics GAF (SD) HRSD (SD) BAI (SD) Age of onset of first depressive disorder (year) Age of onset of PD (year) Lifetime alcohol abuse/dependence disorder (%) Lifetime drug abuse/dependence disorder (%) Lifetime GAD (%) Lifetime OCD (%) Lifetime PTSD (%) Lifetime social phobia (%) Lifetime specific phobia (%) Current psychiatric medications Any medication (%) SSRI/SNRI (%) Tricyclic/tetracyclic antidepressant (%) Atypical antidepressant (%) Atypical antipsychotic (%) Benzodiazepine (%) Other (%)

Comorbid MDD/PD (n = 54)

Control (n = 65)

MDD only (n = 39)

PD only (n = 27)

32.6 (13.3) 59.4 42.2

30.7 (11.2) 59.5 51.4

34.1 (13.4) 63.0 48.1

35.9 (11.6) 69.8 49.1

0.0 7.8 28.1 0.0 35.9 21.9 6.3

0.0 0.0 48.6 0.0 27.0 5.4 5.4

0.0 3.7 18.5 14.8 44.4 14.8 3.7

5.7 3.8 43.4 3.8 24.5 7.5 11.3

88.8 (7.5)a 1.4 (1.7)a 1.7 (2.0)a – – 6.3a a 1.6 – – – – –

53.9 (7.1)b 24.4 (7.9)b,c 14.3 (11.1)b 13.6 – 43.2b,c b,c 27.0 – – – – –

59.0 (8.2)b,c 8.2 (7.0)b 14.1 (9.7)b – 20.9 25.9b 14.8b 25.9a 0.0b 7.4b 7.4b 22.2

52.2 (6.1)b 26.7 (8.8)b,c 21.7 (13.2)b,c 13.4 16.0 52.9b,c 41.4b,c 1.9b 15.1a 32.1a 35.8a 18.9

27.0 18.9 2.7 0.0 0.0 8.1 8.1

25.9 22.2 0.0 0.0 0.0 7.4 0.0

43.4 20.8 5.7 7.5 5.7 22.6 13.2

– – – – – – –

SD, standard deviation; SSRI, selective serotonin reuptake inhibitor; SNRI, serotonin-norepinephrine reuptake inhibitor. Means or percentages with different superscripts across rows were significantly different in pairwise comparisons (p < .05, χ2 test for categorical variables and Tukey’s honestly significant difference test for continuous variables).

on age, education, sex and race. MDD-only, PD-only and comorbid MDD/PD participants did not differ on current psychiatric medication use. MDD-only and comorbid MDD/PD participants did not differ on age of onset of first depressive disorder and PD-only and comorbid MDD/PD participants did not differ on age of onset of PD. MDD-only and comorbid MDD/PD participants had greater rates of lifetime alcohol abuse/dependence

disorder and lifetime substance abuse/dependence disorder relative to PD-only participants but did not differ from each other. Comorbid MDD/PD participants had greater rates of lifetime obsessive– compulsive disorder (OCD), post-traumatic stress disorder (PTSD) and social phobia relative to PDonly participants, and PD-only participants had greater rates of lifetime GAD relative to comorbid MDD/PD participants. As expected, control COGNITION AND EMOTION, 2015

5

NELSON AND SHANKMAN

26

JLO (total correcti)

participants had higher global assessment of functioning (GAF) scores relative to MDD-only, PDonly and comorbid MDD/PD participants; MDD-only and comorbid MDD/PD participants had higher HRSD scores relative to PD-only and control participants; and PD-only and comorbid MDD/PD participants had higher BAI scores relative to control participants.

24

PD 22

Downloaded by [University of Sheffield] at 17:15 05 November 2015

Age was negatively associated with JLO at a trend level, r(181) = −.15, p < .06, and WRAT Arithmetic, r(181) = −.26, p < .001. Education differentiated scores on JLO, F(6, 174) = 4.52, MSE = 73.47, p < .001, g2p = .14, and WRAT Arithmetic, F(6, 174) = 6.67, MSE = 138.34, p < .001, g2p = .19, such that more education was related to better performance. Women (M = 22.72; SD = 4.47) had lower scores than men (M = 25.22; SD = 3.37) on JLO, F(1, 179) = 15.77, MSE = 264.71, p < .001, g2p = .08, but there were no sex differences on WRAT Arithmetic, F(1, 179) = 2.17, MSE = 53.08, ns. Finally, Caucasian participants (M = 24.84; SD = 3.33) had higher scores than non-Caucasian participants (M = 22.59; SD = 4.72) on JLO, F(1, 179) = 13.33, MSE = 226.52, p < .001, g2p = .07, but there were no racial differences on WRAT Arithmetic, F(1, 179) = 1.10, MSE = 27.03, ns. Therefore, age, education, sex and race were included as covariates for all analyses involving JLO, and age and education were included as covariates for all analyses involving WRAT Arithmetic.

Neuropsychological performance Diagnostic group differences in neuropsychological performance were examined using analysis of covariance (ANCOVA) with depression status (present vs. absent) and panic status (present vs. absent) entered as between-subjects factors and the above demographics entered as covariates.

6

COGNITION AND EMOTION, 2015

WRAT Arithmetic (total correct)

20

Demographics and neuropsychological performance

Non-PD

Non-MDD

MDD

44

42 Non-PD PD

40

38

Non-MDD

MDD

Figure 1. Diagnostic group differences on the JLO (top) and WRAT Arithmetic (bottom). Error bars represent standard error.

Judgement of Line Orientation (JLO) Figure 1 (top) displays means (and standard errors) for each diagnostic group on JLO performance. Results indicated a trend level main effect of depression status, F(1, 173) = 3.39, MSE = 50.34, p < .07, g2p = .02, that was qualified by a depression status × panic status interaction, F(1, 173) = 5.27, MSE = 89.08, p < .05, g2p = .03. Follow-up analyses indicated that comorbid MDD/PD participants had lower scores on JLO relative to MDD-only, F(1, 84) = 4.87, MSE = 78.82, p < .05, g2p = .06, PD-only, F(1, 74) = 7.19, MSE = 108.07, p < .01, g2p = .09 and control participants, F(1, 111) = 4.47, MSE = 66.09, p < .05, g2p = .04. MDD-only, PD-only and control participants did not differ on JLO performance (ps > .25). Across the entire sample comorbid MDD/PD participants had the lowest GAF scores and, relative to PD-only participants, had greater rates of lifetime OCD, PTSD, social phobia, alcohol abuse/dependence disorder and substance abuse/ dependence disorder. Therefore, it is possible that

Downloaded by [University of Sheffield] at 17:15 05 November 2015

A STUDY OF PARIETAL FUNCTIONING

the impairment in JLO performance was not due to the comorbidity between MDD and PD but rather increased psychopathological severity. To address this issue, we conducted an additional analysis that included GAF scores and lifetime alcohol abuse/dependence disorder, substance abuse/ dependence disorder, GAD, OCD, PTSD, social phobia and specific phobia diagnoses as additional covariates. Results again indicated a depression status × panic status interaction, F(1, 165) = 8.36, MSE = 113.34, p < .01, g2p = .05, indicating that comorbid MDD/PD participants still demonstrated impaired JLO performance relative to MDD-only, PD-only and control participants even after controlling for GAF severity and all other comorbid lifetime disorders. WRAT Arithmetic Figure 1 (bottom) displays means (and standard errors) for each diagnostic group on WRATArithmetic performance. Results indicated a main effect of panic status, F(1, 175) = 5.12, MSE = 5.12, p < .05, g2p = .03, that was qualified by a depression status × panic status interaction, F(1, 175) = 4.38, MSE = 81.64, p < .05, g2p = .02. Follow-up analyses indicated that MDD-only, PD-only and comorbid MDD/PD participants had lower scores on WRAT Arithmetic relative to controls, F(1, 97) = 7.71, MSE = 136.68, p < .01, g2p = .07; F(1, 87) = 8.81, MSE = 167.85, p < .01, g2p = .09; F(1, 113) = 8.90, MSE = 161.37, p < .01, g2p = .07, respectively. MDD-only, PD-only and comorbid MDD/PD participants did not differ on WRAT-Arithmetic performance (ps > .52). It is possible that poor performance on WRAT Arithmetic could have been due to a deficit in psychomotor processing speed and not mathematical abilities given that the test was timed. To address this issue, we also compared diagnostic groups on the total number of WRAT-Arithmetic items that were attempted (i.e., total correct + total incorrect) using an ANCOVA with depression status (present vs. absent) and panic status (present vs. absent) entered as between-subjects factors and age and education entered as covariates. Results

indicated no main effects of depression status, F(1, 175) = 2.19, MSE = 44.21, ns, panic status, F(1, 75) = 2.16, MSE = 43.58, ns, or depression status × panic status interaction, F(1, 175) = 1.22, MSE = 24.64, ns. These results suggest that the poor WRAT-Arithmetic performance by MDD and/or PD participants was not necessarily due to slowed psychomotor processing speed or an inability to attempt a comparable number of test questions. Medication Finally, we examined whether medication use differentiated JLO and WRAT-Arithmetic performance. Within the MDD-only, PD-only and comorbid MDD/PD participants, a one-way analysis of variance was conducted with medication status (currently taking psychiatric medication vs. not currently taking psychiatric medication) entered as a between-subjects factor for each performance variable. Results were non-significant for all analyses (ps > .75) indicating that current medication use did not account for the results.

DISCUSSION The present study examined neuropsychological performance on measures of visuospatial processing (JLO) and mathematical abilities (WRAT Arithmetic) in a sample of participants with MDD only, PD only, comorbid MDD/PD and controls. There were several noteworthy findings. First, individuals with comorbid MDD/PD exhibited decreased performance on JLO relative to controls and the other two psychopathology groups, and this was not due to greater symptom severity or comorbidity of other psychopathological conditions in the participants with comorbid MDD/PD. Second, individuals in all three psychopathology groups exhibited decreased performance on WRAT Arithmetic relative to controls, and this was not due to slowed psychomotor processing speed or an inability to attempt a comparable number of test questions. Finally, current psychiatric medication status was not related to JLO or WRAT-Arithmetic performance. These results provide novel evidence for the presence of cognitive impairment mediated (in COGNITION AND EMOTION, 2015

7

Downloaded by [University of Sheffield] at 17:15 05 November 2015

NELSON AND SHANKMAN

part) by parietal regions in depression and anxiety. Specifically, comorbid depression and anxious arousal appear to contribute to visuospatial deficits. Depression has previously been associated with decreased performance on the JLO (Coello et al., 1990; Paradiso et al., 2001); however, these studies did not examine the role of comorbid anxiety. Interestingly, other research has reported visuospatial processing deficits in comorbid depression and anxiety relative to depression only and controls (Suslow et al., 2004). The present finding of mathematical dysfunction in those with depression and/or anxiety is also quite novel. There have only been a limited number of studies that have examined the relationship between mood disorders and mathematical dysfunction (Lagace et al., 2003). Furthermore, we do not know of any study that has examined the association between mathematical abilities and anxious arousal (e.g., PD). Thus, this is some of the first evidence to suggest that MDD and/or PD are associated with comparable levels of mathematical dysfunction. The present study has important implications for the neurobiology of depression and anxiety. For example, the valence–arousal model is a neuropsychological model of emotion and psychopathology consisting of separate valence and arousal dimensions (Heller, 1993). In the original model, the valence dimension was associated with activity in frontal brain regions (with positive emotions implemented by the left frontal region and negative emotions implemented by the right frontal region) and the arousal dimension was associated with activity in the right parietal region. Depression and anxiety were posited to be associated with differing patterns of frontal and parietal brain activity, specifically decreased left frontal and right parietal activity in depression and increased right frontal and right parietal activity in anxiety. The valence–arousal model (Heller, 1993; Heller et al., 1997) has been well-supported regarding its prediction of decreased and increased right parietal activity in depression and anxiety, respectively. However, depression and anxiety are highly comorbid (Kessler, Chiu, Demler, & Walters, 2005) and it is less clear what pattern of right parietal activity to expect in those with both conditions.

8

COGNITION AND EMOTION, 2015

The valence–arousal model appears to suggest that the opposing effects of depression and panic will cancel each other out, resulting in a “normal” level of right parietal activity for those with both conditions (Heller & Nitschke, 1998). However, the present study found that comorbid MDD/PD was associated with impaired performance on a primarily right parietal task (JLO) relative to MDD-only, PD-only and control participants (who did not differ). These results are in contrast with the conjectured “normal” level of right parietal activity in comorbid depression and anxiety but are consistent with prior parietal EEG asymmetry (Bruder et al., 1997; Kentgen et al., 2000; Mathersul et al., 2008; Metzger et al., 2004) and dichotic listening studies (Bruder et al., 1999; Pine et al., 2000), which found that comorbid depression and anxiety differed from depression only and controls (although see Bruder et al., 2004). Nelson et al. (2012) also found that comorbid depression and anxiety were associated with impaired performance on a primarily right frontal task (design fluency) relative to depression only and controls. Taken together, evidence suggests that the functional capabilities of the right hemisphere may be compromised in comorbid depression and anxiety, and that the presence of both conditions does not result in “normal” brain functioning. The left parietal region has been largely ignored in theoretical and neuropsychological models of depression and anxiety (Shankman & Klein, 2003). Neuroimaging studies have reported left parietal dysfunction in depression (Müller, Cieslik, Laird, Fox, & Eickhoff, 2013) and PD (Meyer, Swinson, Kennedy, Houle, & Brown, 2000; Nordahl et al., 1990, 1998). The present study found impaired mathematical performance (a predominately left parietal function) in depression and anxiety, and it is possible that the underlying cerebral dysfunction contributes to other neuropsychological impairments. For example, the left parietal region has also been implicated in memory, language and social cognition (Müller et al., 2013). Future research is needed to more definitely determine the role of left parietal dysfunction (and subsuming functions) in depression and anxiety.

Downloaded by [University of Sheffield] at 17:15 05 November 2015

A STUDY OF PARIETAL FUNCTIONING

Research on the cerebral lateralisation of emotion has predominately focused on frontal asymmetry and the relative contribution of approach and withdrawal motivation in those with depression and/or anxiety (Davidson, 1992, 1998). The present study highlights the importance of parietal dysfunction in depression and anxiety and specifically the right hemisphere hypothesis of emotion that arose from the study of stroke patients (e.g., Borod, Koff, Perlman Lorch, & Nicholas, 1986). This hypothesis posits that the right hemisphere is specialised for processing emotions (Borod et al., 1998) and dysfunction in this area of the brain is related to affective psychopathology. However, research has been mixed as to whether strokes in the right parietal region are associated with poststroke depression (Carson et al., 2000; Narushima, Kosier, & Robinson, 2003). Future research is needed to better understand the role of parietal regions in the development and maintenance of depression and anxiety. It is important to note that the present study was not designed to tease apart the sub-operations that may be disrupted in visuospatial processing and math abilities in depression and anxiety. There are several cognitive functions that may have been disrupted and contributed to the pattern of results. For example, poor JLO performance could be attributed to deficits in attentional capacity or visuospatial perception. Furthermore, poor WRAT-Arithmetic performance could have been the result of deficits in arithmetic facts, calculation procedures or lexical processing (McCloskey, 1992). There also could have been impairment in particular working memory functions that are implemented by the parietal cortex, including inhibition, shifting and updating (Collette et al., 2005). Future research is therefore needed to better understand the more specific cognitive functions that are impaired in these more global deficits. The present study had several limitations that warrant consideration. First, and most importantly, WRAT Arithmetic and JLO are not uniquely associated with left and right parietal cortices (Ng et al., 2000; Pinel & Dehaene, 2010), and it is possible that dysfunction in other brain regions may have contributed to the pattern of

results. Second, the present study did not include effort testing, and it is possible that decreased performance was due to low motivation and not a lateralised deficit in neurocognitive abilities. However, we did not find diagnostic group differences on the number of items attempted on WRAT Arithmetic. We also did not include a measure of premorbid intellectual capabilities, and it is possible that decreased performance was due to group differences in IQ. Third, the neuropsychological tasks were presented in a fixed order (JLO presented before WRAT Arithmetic), and it is possible that order effects may have influenced the results. Finally, PD-only and comorbid MDD/PD participants were allowed to meet criteria for other anxiety disorders—thus, the findings for PD may have been due to anxiety in general, rather than PD specifically. However, given the large comorbidity among anxiety disorders, only requiring one anxiety disorder may have resulted in a less representative sample (Kessler et al., 2005). In conclusion, the present study indicated visuospatial deficits in comorbid MDD/PD and mathematical impairment in MDD and/or PD. Importantly, the results were not accounted for by comorbid substance disorders, psychiatric medication use or psychopathology severity. The present study highlights the importance of assessing parietally mediated cognitive functions in depression and anxiety, and future research is needed to better characterise the specific cognitive deficits that are common and unique to depression and anxiety disorders. Acknowledgements We would like to thank Neil H. Pliskin for his assistance with the selection of neuropsychological tests.

Disclosure statement No potential conflict of interest was reported by the authors.

Funding This study was supported by NIMH [grant number R21 MH080689] awarded to S. A. Shankman. COGNITION AND EMOTION, 2015

9

NELSON AND SHANKMAN

Downloaded by [University of Sheffield] at 17:15 05 November 2015

REFERENCES American Psychiatric Association. (1994). Diagnostic and Statistical Manual of Mental Disorders (4th ed.). Washington, DC: Author. Beck, A. T., Epstein, N., Brown, G., & Steer, R. A. (1988). An inventory for measuring clinical anxiety: Psychometric properties. Journal of Consulting and Clinical Psychology, 56, 893–897. doi:10.1037/0022006X.56.6.893 Benton, A. L., Varney, N. R., & Hamsher, K. D. S. (1978). Visuospatial judgment: A clinical test. Archives of Neurology, 35, 364–367. doi:10.1001/archneur. 1978.00500300038006 Blackhart, G. C., Minnix, J. A., & Kline, J. P. (2006). Can EEG asymmetry patterns predict future development of anxiety and depression? A preliminary study. Biological Psychology, 72, 46–50. doi:10.1016/j. biopsycho.2005.06.010 Boller, F., & Grafman, J. (1983). Acalculia: Historical development and current significance. Brain and Cognition, 2, 205–223. doi:10.1016/0278-2626(83) 90010-6 Borod, J. C., Cicero, B. A., Obler, L. K., Welkowitz, J., Erhan, H. M., Santschi, C., … Whalen, J. R. (1998). Right hemisphere emotional perception: Evidence across multiple channels. Neuropsychology, 12, 446–458. doi:10.1037/0894-4105.12.3.446 Borod, J. C., Koff, E., Perlman Lorch, M., & Nicholas, M. (1986). The expression and perception of facial emotion in brain-damaged patients. Neuropsychologia, 24, 169–180. doi:10.1016/0028-3932(86)90050-3 Bruder, G. E., Fong, R., Tenke, C. E., Leite, P., Towey, J. P., Stewart, J. E., … Quitkin, F. M. (1997). Regional brain asymmetries in major depression with or without an anxiety disorder: A quantitative electroencephalographic study. Biological Psychiatry, 41, 939–948. doi:10.1016/S0006-3223(96)00260-0 Bruder, G. E., Schneier, F. R., Stewart, J. W., McGrath, P. J., & Quitkin, F. (2004). Left hemisphere dysfunction during verbal dichotic listening tests in patients who have social phobia with or without comorbid depressive disorder. The American Journal of Psychiatry, 161, 72–78. doi:10.1176/appi.ajp.161.1.72 Bruder, G. E., Wexler, B. E., Stewart, J. W., Price, L. H., & Quitkin, F. M. (1999). Perceptual asymmetry differences between major depression with or without a comorbid anxiety disorder: A dichotic listening study. Journal of Abnormal Psychology, 108, 233–239. doi:10.1037/0021-843X.108.2.233

10

COGNITION AND EMOTION, 2015

Carson, A. J., MacHale, S., Allen, K., Lawrie, S. M., Dennis, M., House, A., & Sharpe, M. (2000). Depression after stroke and lesion location: A systematic review. The Lancet, 356, 122–126. doi:10.1016/ S0140-6736(00)02448-X Chochon, F., Cohen, L., van de Moortele, P. F., & Dehaene, S. (1999). Differential contributions of the left and right inferior parietal lobules to number processing. Journal of Cognitive Neuroscience, 11, 617–630. doi:10.1162/089892999563689 Clements, A. M., Rimrodt, S. L., Abel, J. R., Blankner, J. G., Mostofsky, S. H., Pekar, J. J., … Cutting, L. E. (2006). Sex differences in cerebral laterality of language and visuospatial processing. Brain and Language, 98, 150–158. doi:10.1016/j.bandl.2006.04.007 Coello, E., Ardila, A., & Rosselli, M. (1990). Is there a cognitive marker in major depression? International Journal of Neuroscience, 50(3–4), 137–145. doi:10.3109/ 00207459008987167 Collette, F., Van der Linden, M., Laureys, S., Delfiore, G., Degueldre, C., Luxen, A., & Salmon, E. (2005). Exploring the unity and diversity of the neural substrates of executive functioning. Human Brain Mapping, 25, 409–423. doi:10.1002/hbm.20118 Constantinidis, C., Bucci, D. J., & Rugg, M. (2013). Cognitive functions of the posterior parietal cortex [E-Book]. doi:10.3389/978-2-88919-176-5 Davidson, R. J. (1992). Anterior cerebral asymmetry and the nature of emotion. Brain and Cognition, 20, 125–151. doi:10.1016/0278-2626(92)90065-T Davidson, R. J. (1998). Affective style and affective disorders: Perspectives from affective neuroscience. Cognition & Emotion, 12, 307–330. doi:10.1080/ 026999398379628 Debener, S., Beauducel, A., Nessler, D., Brocke, B., Heilemann, H., & Kayser, J. (2000). Is resting anterior EEG alpha asymmetry a trait marker for depression? Findings for healthy adults and clinically depressed patients. Neuropsychobiology, 41, 31–37. doi:10.1159/000026630 Deutsch, G., Bourbon, W. T., Papanicolaou, A. C., & Eisenberg, H. M. (1988). Visuospatial tasks compared via activation of regional cerebral blood flow. Neuropsychologia, 26, 445–452. doi:10.1016/0028-3932(88) 90097-8 First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (2002). Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Clinician Version (SCID-CV). Washington, DC: American Psychiatric Press.

Downloaded by [University of Sheffield] at 17:15 05 November 2015

A STUDY OF PARIETAL FUNCTIONING

Green, J., Morris, R. D., Epstein, C. M., West, P. D., & Engler, H. F. (1992). Assessment of the relationship of cerebral hemisphere arousal asymmetry to perceptual asymmetry. Brain and Cognition, 20, 264– 279. doi:10.1016/0278-2626(92)90020-M Hamilton, M. (1960). A rating scale for depression. Journal of Neurology, Neurosurgery & Psychiatry, 23, 56–61. doi:10.1136/jnnp.23.1.56 Heller, W. (1993). Neuropsychological mechanisms of individual differences in emotion, personality, and arousal. Neuropsychology, 7, 476–489. doi:10.1037/ 0894-4105.7.4.476 Heller, W., Etienne, M. A., & Miller, G. A. (1995). Patterns of perceptual asymmetry in depression and anxiety: Implications for neuropsychological models of emotion and psychopathology. Journal of Abnormal Psychology, 104, 327–333. doi:10.1037/0021-843X. 104.2.327 Heller, W., & Nitscke, J. B. (1998). The puzzle of regional brain activity in depression and anxiety: The importance of subtypes and comorbidity. Cognition & Emotion, 12, 421–447. doi:10.1080/0269993983 79664 Heller, W., Nitschke, J. B., Etienne, M. A., & Miller, G. A. (1997). Patterns of regional brain activity differentiate types of anxiety. Journal of Abnormal Psychology, 106, 376–385. doi:10.1037/0021-843X. 106.3.376 Henriques, J. B., & Davidson, R. J. (1990). Regional brain electrical asymmetries discriminate between previously depressed and healthy control subjects. Journal of Abnormal Psychology, 99, 22–31. doi:10. 1037/0021-843X.99.1.22 Henriques, J. B., & Davidson, R. J. (1991). Left frontal hypoactivation in depression. Journal of Abnormal Psychology, 100, 535–545. doi:10.1037/0021-843X. 100.4.535 Jackson, M., & Warrington, E. K. (1986). Arithmetic skills in patients with unilateral cerebral lesions. Cortex, 22, 611–620. doi:10.1016/S0010-9452(86) 80020-X Jaeger, J., Borod, J. C., & Peselow, E. D. (1987). Depressed patients have atypical hemispace biases in the perception of emotional chimeric faces. Journal of Abnormal Psychology, 96, 321–324. doi:10.1037/0021843X.96.4.321 Keller, J., Nitschke, J. B., Bhargava, T., Deldin, P. J., Gergen, J. A., Miller, G. A., & Heller, W. (2000). Neuropsychological differentiation of depression and anxiety. Journal of Abnormal Psychology, 109, 3–10. doi:10.1037/0021-843X.109.1.3

Kentgen, L. M., Tenke, C. E., Pine, D. S., Fong, R., Klein, R. G., & Bruder, G. E. (2000). Electroencephalographic asymmetries in adolescents with major depression: Influence of comorbidity with anxiety disorders. Journal of Abnormal Psychology, 109, 797– 802. doi:10.1037/0021-843X.109.4.797 Kessler, R. C., Chiu, W. T., Demler, O., & Walters, E. E. (2005). Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the national comorbidity survey replication. Archives of General Psychiatry, 62, 617–627. doi:10.1001/archpsyc.62.6.617 Kolb, B., & Whishaw, I. Q. (1996). Fundamentals of human neuropsychology (4th ed.). New York, NY: Worth. Lagace, D. C., Kutcher, S. P., & Robertson, H. A. (2003). Mathematics deficits in adolescents with bipolar I disorder. The American Journal of Psychiatry, 160, 100–104. doi:10.1176/appi.ajp.160.1.100 Levy, J., Heller, W., Banich, M. T., & Burton, L. A. (1983). Asymmetry of perception in free viewing of chimeric faces. Brain and Cognition, 2, 404–419. doi:10.1016/0278-2626(83)90021-0 Malhotra, P., Coulthard, E. J., & Husain, M. (2009). Role of right posterior parietal cortex in maintaining attention to spatial locations over time. Brain, 132, 645–660. doi:10.1093/brain/awn350 Mathersul, D., Williams, L. M., Hopkinson, P. J., & Kemp, A. H. (2008). Investigating models of affect: Relationships among EEG alpha asymmetry, depression, and anxiety. Emotion, 8, 560–572. doi:10.1037/ a0012811 Mayer, E., Reicherts, M., Deloche, G., Willadino-Braga, L., Taussik, I., Dordain, M., … Annoni, J.-M. (2003). Number processing after stroke: Anatomoclinical correlations in oral and written codes. Journal of the International Neuropsychological Society, 9, 899– 912. doi:10.1017/S1355617703960103 McCloskey, M. (1992). Cognitive mechanisms in numerical processing: Evidence from acquired dyscalculia. Cognition, 44, 107–157. doi:10.1016/0010-0277(92) 90052-J McNally, R. J. (2002). Anxiety sensitivity and panic disorder. Biological Psychiatry, 52, 938–946. doi:10.1016/ S0006-3223(02)01475-0 Metzger, L. J., Paige, S. R., Carson, M. A., Lasko, N. B., Paulus, L. A., Pitman, R. K., & Orr, S. P. (2004). PTSD arousal and depression symptoms associated with increased right-sided parietal EEG asymmetry. Journal of Abnormal Psychology, 113, 324–329. doi:10.1037/0021-843X.113.2.324 Meyer, J. H., Swinson, R., Kennedy, S. H., Houle, S., & Brown, G. M. (2000). Increased left posterior COGNITION AND EMOTION, 2015

11

Downloaded by [University of Sheffield] at 17:15 05 November 2015

NELSON AND SHANKMAN

parietal-temporal cortex activation after {d}-fenfluramine in women with panic disorder. Psychiatry Research: Neuroimaging, 98, 133–143. doi:10.1016/ S0925-4927(00)00048-2 Müller, V. I., Cieslik, E. C., Laird, A. R., Fox, P. T., & Eickhoff, S. B. (2013). Dysregulated left inferior parietal activity in schizophrenia and depression: Functional connectivity and characterization. Frontiers in Human Neuroscience, 12, 1–11. doi:10.3389/ fnhum.2013.00268 Narushima, K., Kosier, J. T., & Robinson, R. G. (2003). A reappraisal of poststroke depression, intraand inter-hemispheric lesion location using metaanalysis. The Journal of Neuropsychiatry & Clinical Neurosciences, 15, 422–430. doi:10.1176/appi.neu ropsych.15.4.422 Nelson, B. D., Sarapas, C., Robison-Andrew, E. J., Altman, S. E., Campbell, M. L., & Shankman, S. A. (2012). Frontal brain asymmetry in depression with comorbid anxiety: A neuropsychological investigation. Journal of Abnormal Psychology, 121, 579– 591. doi:10.1037/a0027587 Ng, V. W. K., Eslinger, P. J., Williams, S. C. R., Brammer, M. J., Bullmore, E. T., Andrew, C. M., … Benton, A. L. (2000). Hemispheric preference in visuospatial processing: A complementary approach with fMRI and lesion studies. Human Brain Mapping, 10, 80–86. doi:10.1002/(SICI)1097-0193(200006) 10:23.0.CO;2-2 Nitschke, J. B., Heller, W., Palmieri, P. A., & Miller, G. A. (1999). Contrasting patterns of brain activity in anxious apprehension and anxious arousal. Psychophysiology, 36, 628–637. doi:10.1017/S00485772999 72013 Nordahl, T. E., Semple, W. E., Gross, M., Mellman, T. A., Stein, M. B., Goyer, P., … Cohen, R. M. (1990). Cerebral glucose metabolic differences in patients with panic disorder. Neuropsychopharmacology, 3, 261–272. Nordahl, T. E., Stein, M. B., Benkelfat, C., Semple, W. E., Andreason, P., Zametkin, A., … Cohen, R. M. (1998). Regional cerebral metabolic asymmetries replicated in an independent group of patients with panic disorder. Biological Psychiatry, 44, 998–1006. doi:10.1016/S0006-3223(98)00026-2 Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97–113. doi:10.1016/0028-3932(71)90067-4 Paradiso, S., Hermann, B. P., Blumer, D., Davies, K., & Robinson, R. G. (2001). Impact of depressed mood on neuropsychological status in temporal lobe

12

COGNITION AND EMOTION, 2015

epilepsy. Journal of Neurology, Neurosurgery, & Psychiatry, 70, 180–185. doi:10.1136/jnnp.70.2.180 Pine, D. S., Kentgen, L. M., Bruder, G. E., Leite, P., Bearman, K., Ma, Y., & Klein, R. G. (2000). Cerebral laterality in adolescent major depression. Psychiatry Research, 93, 135–144. doi:10.1016/S0165-1781(00) 00101-3 Pinel, P., & Dehaene, S. (2010). Beyond hemispheric dominance: Brain regions underlying the joint lateralization of language and arithmetic to the left hemisphere. Journal of Cognitive Neuroscience, 22, 48–66. doi:10.1162/jocn.2009.21184 Rabe, S., Debener, S., Brocke, B., & Beauducel, A. (2005). Depression and its relation to posterior cortical activity during performance of neuropsychological verbal and spatial tasks. Personality and Individual Differences, 39, 601–611. doi:10.1016/j. paid.2005.02.005 Rivera, S. M., Reiss, A. L., Eckert, M. A., & Menon, V. (2005). Developmental changes in mental arithmetic: Evidence for increased functional specialization in the left interior parietal cortex. Cerebral Cortex, 15, 1779–1790. doi:10.1093/cercor/bhi055 Schaffer, C. E., Davidson, R. J., & Saron, C. (1983). Frontal and parietal electroencephalogram asymmetry in depressed and nondepressed subjects. Biological Psychiatry, 18, 753–762. Shackman, A. J., Sarinopoulos, I., Maxwell, J. S., Pizzagali, D. A., Lavric, A., & Davidson, R. J. (2006). Anxiety selectively disrupts visuospatial working memory. Emotion, 6, 40–61. doi:10.1037/ 1528-3542.6.1.40 Shankman, S. A., & Klein, D. N. (2003). The relation between depression and anxiety: An evaluation of the tripartite, approach-withdrawal and valence-arousal models. Clinical Psychology Review, 23, 605–637. doi:10.1016/S0272-7358(03)00038-2 Shankman, S. A., Nelson, B. D., Robison-Andrews, E. J., Sarapas, C., Campbell, M. L., Altman, S. E., … Gorka, S. M. (2013). A psychophysiological investigation of threat and reward sensitivity in individuals with panic disorder and/or depression. Journal of Abnormal Psychology, 122, 322–338. doi:10.1037/ a0030747 Stewart, J. L., Towers, D. N., Coan, J. A., & Allen, J. J. B. (2011). The oft‐neglected role of parietal EEG asymmetry and risk for major depressive disorder. Psychophysiology, 48, 82–95. doi:10.1111/ j.1469-8986.2010.01035.x Suslow, T., Dannlowski, U., Lalee-Mentzel, J., Donges, U. S., Arolt, V., & Kersting, A. (2004). Spatial

A STUDY OF PARIETAL FUNCTIONING

Wexler, B. E., & Goodman, W. K. (1991). Cerebral laterality, perception of emotion, and treatment response in obsessive-compulsive disorder. Biological Psychiatry, 29, 900–908. doi:10.1016/0006-3223(91) 90056-R Whalen, J., McCloskey, M., Lesser, R. P., & Gordon, B. (1997). Localizing arithmetic processes in the brain: Evidence from a transient deficit during cortical stimulation. Journal of Cognitive Neuroscience, 9, 409–417. doi:10.1162/jocn.1997.9.3.409 Wilkinson, G. S. (1993). Wide Range Achievement Test – Third Edition. Austin, TX: Wide Range.

Downloaded by [University of Sheffield] at 17:15 05 November 2015

processing of facial emotion in patients with unipolar depression: A longitudinal study. Journal of Affective Disorders, 83, 59–63. doi:10.1016/j.jad.2004.03.003 Tranel, D., Vianna, E., Manzel, K., Damasio, H., & Grabowski, T. (2009). Neuroanatomical correlates of the Benton facial recognition test and judgment of line orientation test. Journal of Clinical and Experimental Neuropsychology, 31, 219–233. doi:10.1080/ 13803390802317542 Treccani, B., Torri, T., & Cubelli, R. (2005). Is judgment of line orientation selectively impaired in right brain damaged patients? Neuropsychologia, 43, 598–608. doi:10.1016/j.neuropsychologia.2004.07.008

COGNITION AND EMOTION, 2015

13