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1 475222 PSS XX X 10.1177/0956797612475222Saj et al. Hemispatial Neglect Distorts the Mental Time Line research-article 2013 Research Report Psychological Science 2014, Vol. 25(1) 207 –214 © The Author(s) 2013 Patients With Left Spatial Neglect Also Reprints and permissions: sagepub.com/journalsPermissions.nav Neglect the “Left Side” of Time DOI: 10.1177/0956797612475222 pss.sagepub.com 1 1 2 Arnaud Saj , and , Orly Fuhrman , Patrik Vuilleumier 3 Lera Boroditsky 1 Department of Neurology and Neurosciences, University Hospital of Geneva, University of Geneva; 2 3 Department of Psychology, Stanford University; and Department of Cognitive Science, University of California, San Diego Abstract Previous research suggests that people construct mental time lines to represent and reason about time. However, is the ability to represent space truly necessary for representing events along a mental time line? Our results are the first to demonstrate that deficits in spatial representation (as a function of left hemispatial neglect) also result in deficits in representing events along the mental time line. Specifically, we show that patients with left hemispatial neglect have difficulty representing events that are associated with the past and, thus, fall to the left on the mental time line. These results demonstrate that representations of space and time share neural underpinnings and that representations of time have specific spatial properties (e.g., a left and a right side). Furthermore, it appears that intact spatial representations are necessary for at least some types of temporal representation. Keywords spatial memory, time perception Received 5/24/12; Revision accepted 12/20/12 However, a key question remains: Are spatial repre- Time is a fundamental aspect of human experience. What sentations truly necessary for representing events in time? are the cognitive and neural underpinnings of people’s In the study reported here, we investigated whether defi- representations of time? There are many components of cits in spatial representation, as caused by left hemispa- mental time (e.g., temporal order, duration, rhythm, deic- tial neglect following right-brain damage, also result in tic time). In the research reported here, we focused on deficits in representing events along the mental time line. representations of events along the mental time line. Specifically, we asked whether patients with left hemis- Spatial representations of time (in time lines, clocks, and patial neglect have difficulty representing events that fall calendars) are widespread around the world. Languages forward, back, to the left on their mental time line. also rely heavily on spatial words (e.g., ) to talk about the order of events (e.g., Lesions of the right hemisphere, and more specifically ahead, behind of the inferior parietal lobe, commonly give rise to spatial Clark, 1973; Lakoff & Johnson, 1980; Traugott, 1978). neglect. Patients affected with this syndrome exhibit severe Previous research suggests people also construct mental disturbance in the ability to detect, identify, and move time lines to represent and reason about time. Irrelevant spatial information affects people’s judgments of tempo- toward objects or events in the contralesional (left) side of space, even in the absence of sensory or motor deficits ral order (Boroditsky, 2000; Boroditksy & Gaby, 2010; Boroditsky & Ramscar, 2002; Núñez, Motz, & Teuscher, (Driver & Vuilleumier, 2001; Heilman & Valenstein, 1979). In clinical tests, patients show a right-shift bias when asked 2006), and people seem to have implicit associations between parts of space and time (Fuhrman & Boroditsky, 2010; Gevers, Reynvoet, & Fias, 2003; Ishihara, Keller, Corresponding Author: Rossetti, & Prinz, 2008; Miles, Nind, & Macrae, 2010; Lera Boroditsky, Department of Cognitive Science, University of Santiago, Lupiáñez, Pérez, & Funes, 2007; Torralbo, California, San Diego, 9500 Gilman Dr., La Jolla, CA 92093-0515 E-mail: [email protected] Santiago, & Lupiáñez, 2006; Weger & Pratt, 2008).

2 208 Saj et al. to bisect lines and when performing object-cancellation demonstrated that healthy people who read from left to right also represent time as proceeding from left to right, tasks (Azouvi et al., 2002). In daily activities, patients may with earlier or past events on the left and later or future leave food uneaten on the left side of their plates, fail to events on the right (e.g., Fuhrman & Boroditsky, 2010; groom the left side of their faces, or miss words on the left Ouellet, Santiago, Israeli, & Gabay, 2010; Tversky, side of a printed page when reading (Azouvi et al., 2002). Kugelmass, & Winter, 1991). The left-to-right organization The inability to attend to contralesional space is not lim- ited to the visual modality and can also affect auditory and of time has been observed across a wide range of left-to- tactile representations centered around the body or around right reading populations, including francophone partici- an object (Driver & Vuilleumier, 2001; Saj & Vuilleumier, pants (e.g., Cienki, 1998), like those included in our study. These observations motivated our prediction that 2007; Vuilleumier, 2007). hemispatial neglect might lead to a distortion in the rep- Furthermore, spatial neglect can be manifested in the resentation of the mental time line. Specifically, patients inability to generate or adequately maintain a normal rep- resentation of the contralesional space. In representational with left hemispatial neglect who are from cultures that neglect, which is sometimes dissociated from visual read from left to right should show a selective deficit in neglect, patients have trouble accessing the left side of a representing events as belonging to the past (on the left of the mental time line) as opposed to the future (on the mental space when asked to draw objects from memory or right of the mental time line). retrieve landmarks or locations from the left side of a familiar landscape or map (Bisiach & Luzzatti, 1978; Rode et al., 2010). Representational neglect is also present for Method conventionally spatialized number arrangements (e.g., numbers as they are represented along the number line or Participants around a clock face; Fischer, 2001; Vuilleumier, Ortigue, & Twenty-one French-speaking participants were included Brugger, 2004; Zorzi, Priftis, & Umiltà, 2002). in this study (7 right-hemisphere stroke patients exhibit- If intact spatial representations are indeed necessary ing spatial neglect, 7 right-hemisphere stroke patients for representing events along the mental time line, then with no neglect symptoms, and 7 healthy control partici- patients who show left hemispatial neglect should also pants; see Table 1 for demographic information for the neglect the “left side” of time. Previous work has Table 1. Demographic and Clinical Data of Patients Representational Bell cancellation task Scene Line Participant group and Schooling Flower Left Central Right Clock copy patient (years) Etiology Age bisection Gender Hemispatial neglect 83 M 7 H 50.66 Patient 1 2 0 3 3 2 6 Patient 2 69 F 9 H 13.14 15 5 11 3 3 3 Patient 3 F 9 H 32.29 5 3 0 2 2 3 72 15 M 12 I 44.65 81 5 2 1 1 3 Patient 4 Patient 5 57 M 7 I 25.64 15 5 10 3 3 3 Patient 6 M 9 H 20.42 12 2 5 2 2 3 60 6 Patient 7 20 I 62.55 13 4 F 2 2 2 75 No hemispatial neglect Patient 1 74 F 12 H 4.20 1 0 0 0 0 1 44 M 22 I − Patient 2 2 0 3 0 0 0 4.86 Patient 3 82 M 17 I − 3.06 0 1 0 0 0 0 Patient 4 M 22 I − 1.21 1 0 1 0 0 0 66 1 Patient 5 M 7 I 1.82 70 0 0 0 0 0 Patient 6 59 M 12 I 2.20 1 1 1 0 0 0 1 68 F 9 I 2.13 1 0 Patient 7 0 0 0 Note: Line-bisection results are mean errors in percentage of maximal possible errors. Bell-cancellation results are the number of omitted bells in the left, central, and right parts of the test sheet (out of 15, 5, and 15 bells, respectively, in each of these parts). The representational task entailed drawing from memory a clock and a flower; performance was coded from 0 (no omission) to 4 (severe omissions on the contralateral side). The scene-copy task entailed copying a scene that included four distinct elements from the left to the right of the sheet; performance was coded from 0 (no omission) to 4 (severe omissions on the contralateral side). M = male; F = female; H = hemorrhagic; I = ischemic.

3 Hemispatial Neglect Distorts the Mental Time Line 209 patients with and without neglect). Patients had been age), whereas foods that “David will like to eat in 10 admitted to the Neurology Department at the University years” would appear with a black top hat above them (as Hospital of Geneva presenting with a first focal right- a cue for older age). hemisphere stroke (hemorrhagic or ischemic; see Fig. 1). Participants were then shown line drawings of 10 food Neglect was assessed using standard clinical tests (Saj, items (an egg, corn, a hamburger, spaghetti, ice cream, an apple, grapes, a cake, a sandwich, and a pear), pre- Verdon, Vocat, & Vuilleumier, 2012; Verdon, Schwartz, sented one at a time, on a computer screen. Half of the Lovblad, Hauert, & Vuilleumier, 2010): line bisection food items had a picture of a white cap above them (indi- (Schenkenberg, Bradford, & Ajax, 1980), bell cancellation cating the past), and half had a picture of a black top hat (Gauthier, Dehaut, & Joanette, 1989), and scene copy (Gainotti, Messerli, & Tissot, 1972; see Table 1 for clinical above them (indicating the future). Which items were associated with the past and which with the future was test results). None of the patients showed a memory or counterbalanced across participants. All items (whether executive-function deficit. Seven patients presented per - associated with the past or the future) were centered sistent left hemispatial neglect on repeated testing and along the vertical midline of the screen. For each item, were prospectively recruited for the study. participants were asked to name the food and say whether it was a food that “David liked 10 years ago” or Procedure “will like 10 years from now.” This procedure was fol- All participants completed four blocks of a memory lowed for each item. After participants had seen all 10 experiment. Each block contained an encoding phase, items, they proceeded to the recall test. followed by a recall-test phase and then a recognition- test phase. All participants were tested in French. Recall-test phase. In the recall test, participants were asked to freely recall all of the food items mentioned in During the encoding phase, partici- the encoding phase. For each item they recalled, they Encoding phase. pants learned about a fictional man named David. In the further needed to indicate whether it was something “David liked 10 years ago” or “will like 10 years from first block, participants were told the following: now.” The experimenter wrote down the participants’ responses. After participants had listed everything they Today, David is 40 years old. In the first part of this could recall, they proceeded to the recognition-test study, you will learn about things that David liked to eat 10 years ago (when he was 30 years old) and phase. things that he will like to eat in 10 years (when he - For the recognition test, par Recognition-test phase. will be 50 years old). ticipants were shown pictures of 14 items (the 10 items Participants were further instructed that foods that from the encoding phase and 4 new items they had not “David liked to eat 10 years ago” would appear with a seen before). Pictures were again presented one at a picture of a white cap above them (as a cue for younger time, centered on the vertical midline of the screen (just Fig. 1. Areas of lesion overlap across all patients, shown on axial slices of a normalized MRI brain template. The different colors indicate the num- ber of patients with damage to a given area (violet = 1; red = 7). The lateral brain images show that maximum overlap arose in the right temporo- parietal junction.

4 210 Saj et al. as in the encoding phase, except that the pictures were Results shown without hats pictured above them). For each item, As predicted, (French-speaking) patients with left hemis- participants were asked to indicate whether they had - patial neglect showed a specific deficit when remember seen the item during the encoding phase. If participants ing and attributing items to the past (on the left side of indicated that they had seen the item before, they were their mental time lines). The main results of interest are then asked whether it was something “David liked 10 shown in Figure 2 (recall memory) and Figure 3 (recogni- years ago” or something he “will like 10 years from now.” tion memory). Results of additional analyses are included The experimenter wrote down the participants’ responses. in the Supplemental Material available online (Recall The same procedure (including the encoding phase, Memory: Further Analyses, Recognition Memory: Further the recall phase, and the recognition phase) was then Analyses, and Tables S1 and S2). repeated three times with new sets of items. Whereas participants learned about things David liked to eat in Block 1, they learned about things he had in his apart- Recall-memory results ment (a clock, a desk, a kettle, a vase, a telephone, a lamp, a toaster, a refrigerator, a stool, and a television) in Overall, patients with left hemispatial neglect recalled Block 2, about things he liked to wear (a shoe, a shirt, slightly fewer items (66%) than did patients without pants, a watch, a sock, a tie, a scarf, a boot, a belt, and a neglect (83%) or healthy control participants (78%), but coat) in Block 3, and about things he liked to do (sailing, t = p these differences were not significant, (12) = 1.61, roller-skating, painting, playing football, playing the gui- .13, and t (12) = 1.26, p = .23, respectively. The overall tar, reading, flying a kite, playing tennis, skiing, and play- recall rate of patients with neglect also did not differ sig- ing the trumpet) in Block 4. nificantly from that of the two control groups combined, Past Items Recalled as Past Items Future Items Recalled as Past Items Past Items Recalled as Future Items Future Items Recalled as Future Items Future Past Patients With Left Hemispatial Neglect Patients Without Neglect Healthy Control Participants 0 80 60 40 2002 04 06 08 Percentage of Items Fig. 2. Results from the recall-test phase. The graph shows the percentage of items recalled as belonging to the past and to the future as a function of participant group. Items fell into four categories: items associ- ated with the future at encoding that were incorrectly recalled as belonging to the past; items associated with the past at encoding that were correctly recalled as belonging to the past; items associated with the future at encoding that were correctly recalled as belonging to the future; and items associated with the past at encoding that were incorrectly recalled as belonging to the future. All “past” responses appear to the left of the midline, and all “future” responses appear to the right of the midline.

5 Hemispatial Neglect Distorts the Mental Time Line 211 Past Items Recognized as Past Items Future Items Recognized as Past Items Past Items Recognized as Future Items Future Items Recognized as Future Items Future Past Patients With Left Hemispatial Neglect Patients Without Neglect Healthy Control Participants 60 02 06 08 20 04 80 40 0 Percentage of Items Fig. 3. Results from the recognition-test phase. The graph shows the percentage of recognized items identified as belonging to the past and the future as a function of participant group. Items fell into four categories: items associated with the future at encoding that were incorrectly recognized as belonging to the past; items associated with the past at encoding that were correctly recognized as belonging to the past; items associated with the future at encoding that were correctly recognized as belonging to the future; and items associated with the past at encoding that were incorrectly recognized as belong- ing to the future. All “past” responses appear to the left of the midline, and all “future” responses appear to the right of the midline. When it came to items belonging to the future, patients = .10. Because the data from the two con- p t (19) = 1.72, trol groups did not differ in any direct comparisons (all with neglect did not show the same pattern of deficits. p s > .15), for brevity, we report results comparing data Patients with neglect did not recall significantly fewer items that had been associated with the future than did from the group of patients with neglect with the com- bined data from the two control groups (we have noted = .35, members of the two control groups, t (19) = 0.96, p all cases in which results from this combined analysis nor were they significantly worse at correctly recalling differed from those of separate analyses). = p “future” items as belonging to the future, t (19) = 1.75, .10. Patients with neglect incorrectly recalled slightly Planned direct comparisons of the recalled items revealed a pattern of selective deficit for “past” items in more “future” items as belonging to the past (14%) than did patients without neglect (6%) or healthy control par - patients with neglect. Overall, patients with neglect t (19) = 2.96, p < .05, d = 1.36; however, recalled fewer items that had been associated with the ticipants (3%), this difference was reliable relative only to the healthy past (64%) than did patients without neglect (85%) or (12) = 3.02, p < .05, and not to the group control group, t healthy control participants (82%), t (19) = 2.42, p < .05, d of patients without neglect, (12) = 1.72 , p = 1.11. Patients with neglect also correctly recalled = .11. t fewer “past” items as belonging to the past (26%) than - did patients without neglect (80%) or healthy control par Recognition-memory results ticipants (79%), p t d = 3.01. In con- (19) = 6.57, < .001, All three groups of participants were accurate in identify- trast, patients with neglect incorrectly recalled more ing the new items as new (control group = 100% correct, “past” items as belonging to the future (37%) than did nonneglect group = 99% correct, neglect group = 97% patients without neglect (5%) or healthy control partici- correct), with no differences between groups. For the old = 2.73. t (19) = 5.96, p < .001, d pants (3%),

6 212 Saj et al. items, patients with neglect showed slightly impaired rec- consequently misattributing past events to the future. ognition overall (80% correct) relative to patients without This kind of representational crowding is analogous to (12) = 1.64, t p neglect (90%), = .13, and healthy control what has been seen with spatial layouts. t < .01. p (12) = 3.16, All of the patients with neglect included in our study participants (95%), showed evidence of both perceptual and representa- Planned direct comparisons of the hit responses (old tional spatial neglect on a standard neurological test bat- items that participants identified as old) revealed a pat- tern of selective deficit for “past” items in patients with tery. It would be interesting for future work to examine the patterns of temporal representation when different neglect. Overall, these patients attributed fewer items to types of spatial neglect are dissociated (see Doricchi, the past (23%) than did patients without neglect (50%), < .01, d = 2.81, or healthy control partici- Guariglia, Gasparini, & Tomaiuolo, 2005; Saj & Vuilleumier, t (12) = 4.87, p t (12) = 8.02, pants (52%), p 2007; Verdon et al., 2010; Vuilleumier, Valenza, Mayer, < .01, d = 4.63. Patients with Réverdin, & Landis, 1998). It would also be interesting neglect also correctly identified fewer “past” items as to test patients with neglect of right space after left- belonging to the past (19%) than did patients without = 2.86, or healthy p hemispheric damage, but such symptomatology is rare t (12) = 4.96, < .001, d neglect (74%), p because of the usual right-hemisphere dominance for control participants (84%), t = d < .0001, (12) = 16.02, 9.25. In addition, again, patients with neglect incorrectly spatial processing (Beis et al., 2004). identified more “past” items as belonging to the future In addition to the construction of time lines as explored t (60%) than did patients without neglect (16%), in this article, previous studies that included patients with (12) = 6.18, p < .001, d = 3.57, or healthy control participants neglect have demonstrated impaired processing of tem- p t = 6.11. d < .001, poral dynamics; patients have difficulty directing atten- (12) = 10.58, (11%), tion in time (Husain, Shapiro, Martin, & Kennard, 1997) In contrast, patients with neglect did not attribute and seem to have a distorted estimation of tone dura- more “future” items to the past (18%) than did partici- tions, especially when the tones are presented in the s > .65). p pants in the two control groups (16% each; all neglected field—that is, the left ear (e.g., Becchio & The two control groups did not differ from one another in any of the direct comparisons (all p s > .2). Bertone, 2006; Calabria et al., 2011; see also Frassinetti, Magnani, & Oliveri, 2009). Taken together, these data converge to suggest that some neural substrates (e.g., in Discussion posterior parietal cortical areas) are shared for the repre- When reasoning about time, people construct mental sentation of external spatial information and the repre- time lines according to the spatial schemes afforded by sentation of temporal information (Bueti & Walsh, 2009; Oliveri et al., 2009; Walsh, 2003). their culture. Our results suggest that an intact ability to represent space is necessary for accurate temporal repre- sentation. They demonstrate that a distortion in spatial Conclusion representation (i.e., unilateral neglect symptoms) pre- dicts a distortion in the way memorized events are repre- Are spatial representations truly necessary for represent- sented along the mental time line. ing events in time? Our results demonstrate that deficits We asked participants to remember a series of events in spatial representation (as a function of left hemispatial that were associated with either the past or the future. We neglect) also result in deficits in representing events hypothesized that participants would naturally represent along the mental time line. Specifically, our findings show these events on a “mental time map,” placing past events that patients with left hemispatial neglect have difficulty to the left and future events to the right in their mind’s representing events that fall to the left on the mental time eye (following the reading and writing directionality of line. their language, French). The performance of healthy control participants and Author Contributions patients with no neglect showed symmetrical access to O. Fuhrman and L. Boroditsky developed the study concept. items belonging to the past and to the future. However, O. Fuhrman spearheaded the study design, with contributions patients with neglect recalled fewer items that were asso- by P. Vuilleumier, A. Saj, and L. Boroditsky. Testing and data ciated with the past than did participants in the other collection were performed by A. Saj under the direction of groups. Patients with neglect also mislabeled items P. Vuilleumier. L. Boroditsky analyzed and interpreted the data, belonging to the past as “future” items significantly more with contributions from A. Saj and O. Fuhrman. L. Boroditsky often than did participants without neglect. This pattern drafted the manuscript, with critical revisions provided by of results suggests that patients with neglect were crowd- P. Vuilleumier, A. Saj, and O. Fuhrman. All authors approved ing past events to the right in their mental time map and the final version of the manuscript for submission.

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