Cognition 168 (2017) 312–319
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Cognition
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Original Articles Spatial representation of magnitude in gorillas and orangutans ⇑ Regina Paxton Gazes a,b, , Rachel F.L. Diamond c,g, Jasmine M. Hope d, Damien Caillaud e,f, Tara S. Stoinski a,e, Robert R. Hampton c,g a Zoo Atlanta, Atlanta, GA, United States b Bucknell University, Lewisburg, PA, United States c Department of Psychology, Emory University, Atlanta, GA, United States d Neuroscience Graduate Program, Emory University, Atlanta, GA, United States e Dian Fossey Gorilla Fund International, Atlanta, GA, United States f Department of Anthropology, University of California Davis, Davis, CA, United States g Yerkes National Primate Research Center, Atlanta, GA, United States article info abstract
Article history: Humans mentally represent magnitudes spatially; we respond faster to one side of space when process- Received 1 March 2017 ing small quantities and to the other side of space when processing large quantities. We determined Revised 24 July 2017 whether spatial representation of magnitude is a fundamental feature of primate cognition by testing Accepted 25 July 2017 for such space-magnitude correspondence in gorillas and orangutans. Subjects picked the larger quantity in a pair of dot arrays in one condition, and the smaller in another. Response latencies to the left and right sides of the screen were compared across the magnitude range. Apes showed evidence of spatial repre- Keywords: sentation of magnitude. While all subjects did not adopt the same orientation, apes showed consistent Space tendencies for spatial representations within individuals and systematically reversed these orientations SNARC Ape in response to reversal of the task instruction. Results suggest that spatial representation of magnitude is Pongo phylogenetically ancient and that consistency in the orientation of these representations in humans is likely culturally mediated. Ó 2017 Elsevier B.V. All rights reserved.
1. Introduction bias attention in the opposite direction. As a result, English speak- ing western adults are, in general, quicker to detect cues presented Behavioral and neurobiological evidence indicates that human on the left after being primed with small numbers, and cues pre- adults represent magnitude dimensions spatially (Dehaene, sented on the right after being primed with large numbers Bossini, & Giraux, 1993; Fischer, Castel, Dodd, & Pratt, 2003; (Fischer et al., 2003). Similarly, when making numerical judg- Rusconi, Bueti, Walsh, & Butterworth, 2011). For example, picture ments, English speakers respond faster to small numbers with a the numbers one through 10. If you are like most native English leftward response and large numbers with a rightward response speakers, you pictured them in a horizontal line with one on the (Dehaene et al., 1993). These space-magnitude congruency effects left and 10 on the right. Spatial representation is involved in mag- have been most extensively studied using judgments of number nitude processing generally; it is not confined to processing of (Dehaene et al., 1993), but are also found for comparisons along number specifically (Holmes & Lourenco, 2011; Walsh, 2003). other dimensions such as size (Shaki, Petrusic, et al., 2012), order The orientation of this spatial representation of magnitude varies (Gevers, Reynvoet, & Fias, 2003), and emotional magnitude with culture and task demands (Bachtold, Baumuller, & Brugger, (Holmes & Lourenco, 2011). 1998; Fischer, Shaki, & Cruise, 2009; Shaki & Petrusic, 2005; Orientation of the spatial representation of magnitude varies Shaki, Petrusic, & Leth-Steensen, 2012; van Dijck & Fias, 2011). across cultures, between individuals, and responds flexibly to Across these variations, the spatial representation of magnitude experience. It is influenced by both reading and counting such that is evident in that viewing or thinking about small magnitudes in contrast to English speakers, Palestinians, who read and count biases visual attention to one area of space while large magnitudes from right to left, respond faster on average to small numbers with a rightward response and large numbers with a leftward response (Shaki, Fischer, & Petrusic, 2009; Shaki, Petrusic, et al., 2012). These ⇑ Corresponding author at: Bucknell University, Department of Psychology, 1 Dent Drive, Lewisburg, PA 17837, United States. reliable group-level differences in orientation of the spatial repre- E-mail address: [email protected] (R.P. Gazes). sentation of number are likely caused by long-term memory repre- http://dx.doi.org/10.1016/j.cognition.2017.07.010 0010-0277/Ó 2017 Elsevier B.V. All rights reserved. R.P. Gazes et al. / Cognition 168 (2017) 312–319 313 sentations acquired through cultural experience (van Dijck & Fias, determine the extent to which spatial representation is a funda- 2011). Nonetheless, the orientation of spatial representation of mental basis for magnitude cognition across primates specifically, magnitude is apparently not fixed by culture, as it can vary we tested for spatial-magnitude correspondence in two groups of between individuals even within a cultural group. While English apes: gorillas (Gorilla gorilla gorilla) and orangutans (Pongo pyg- speaking adults performing a parity task show consistent, robust maeus & Pongo abelli) using a task similar to those used in humans. group-level left-to-right representations of number (Wood, These species shared a common ancestor with humans approxi- Willmes, Nuerk, & Fischer, 2008), the few studies that present indi- mately 8 and 15 million years ago respectively (Finstermeier vidual data indicate that as few as 56–66% of individual partici- et al., 2013). Non-human primates share many components of pants show this orientation (Nuerk, Wood, & Willmes, 2005; human magnitude processing abilities; they accurately judge dif- Wood, Nuerk, & Willmes, 2006). The remaining participants either ferences in quantity, order items by magnitude, and show perfor- show no clear orientation or the opposite right-to-left orientation. mance patterns consistent with human numerical estimation, The orientation of spatial representations also changes in response such as the symbolic distance effect and conformity to Weber’s to language priming, numerical range, real-world referents, and law (Beran, 2008; Brannon & Terrace, 2002; Cantlon & Brannon, task instructions (Bachtold et al., 1998; Fischer et al., 2009; Shaki 2006). They additionally show interactions between processing of & Petrusic, 2005; Shaki, Petrusic, et al., 2012; van Dijck & Fias, space and various magnitudes (time: Merritt, Casasanto, & 2011). For example, when asked whether a number is higher or Brannon, 2010; order: Adachi, 2014; Drucker & Brannon, 2014; lower than 6, English speakers show latency differences in opposite Gazes, Lazareva, Bergene, & Hampton, 2014; social dominance: directions when referencing numbers on a ruler (left-to-right) than Dahl & Adachi, 2014). As in humans, there is neural overlap when referencing numbers on a clock face (right-to-left; Bachtold between numerical and spatial processing in the intraparietal sul- et al., 1998). Four is represented on the left as a ‘‘small” number cus of monkeys (Hubbard, Piazza, Pinel, & Dehaene, 2005). when presented with a numerical range from 4 to 9, but on the Based on work with humans, we designed a task for apes that right as a ‘‘large” number when presented in a range from 1 to 5 tests for the presence of a spatial representation of magnitude (Dehaene et al., 1993). Bilingual Russian-Hebrew speakers reverse but does not make assumptions about the orientation of the repre- the orientation of their spatial representation of number depend- sentation. Given the individual variability in orientation shown by ing on the language used to prime the task (Shaki & Fischer, 2008). human adults (Wood et al., 2006), and the fact that apes do not Variability and flexibility in the orientation of spatial represen- have cultural norms to dictate a preferred orientation in spatial tations of magnitude are especially great when humans lack long representation, there is not sufficient evidence to predict a consis- term memories defining prototypical arrangements in a domain. tent orientation of magnitude representation in these species. Apes For example, adults comparing quantities 1–10 (e.g. select the were presented with a task in which they selected either the larger smaller or larger item; Shaki, Petrusic, et al., 2012) show group or smaller of two quantities of dots (Patro & Haman, 2012). Across level spatial representations in culturally preferred directions pairs from small (2 versus 3) to large (9 versus 10) quantities, regardless of task instruction. However, if asked to compare animal response latencies were compared for trials in which the correct sizes (e.g. snail vs. mouse), English speakers organize their repre- choice required a leftward or a rightward response. If spatial repre- sentation with small animals on the left when asked to identify sentation of magnitude is an evolutionarily ancient foundation of the smaller animal in the pair, but reverse this orientation when magnitude processing, apes, like humans, should respond faster instructed to identify the larger animal in the pair. The spatial ori- to one side of space when processing pairs of small quantities entation of Arabic speakers also reverses in response to instruc- and faster to the other side of space when processing large quanti- tions, but in the opposite direction (Shaki, Petrusic, et al., 2012). ties. Critically, if apes represent quantities for which they have no Likewise, human adults judging the smaller or larger quantity in cultural norm similarly to how humans represent uncommon mag- a pair of large, less commonly ordered numerals (6–50; Lee, nitude domains, we should observe that the orientation of the spa- Chun, & Cho, 2016) or in a pair of shape arrays (Lee et al., 2016; tial representation is reversed between conditions in which the Patro & Shaki, 2016) show this same reversal in orientation when animals are required to pick small and pick large. instructions are reversed. Apparently, in the absence of the strong norms governing specific orientation of representations, partici- pants flexibly orient their spatial representations with the to-be- 2. Method detected magnitude on the preferred point-of-reference side of space (left for English speakers, right for Arabic speakers; Patro & 2.1. Subjects and procedure Shaki, 2016). Importantly, this systematic reversal in orientation is diagnostic of the presence of spatial representations- it would Subjects were 9 apes (4 gorillas, 5 orangutans; Table 1) housed not occur if representations did not have spatial properties. Non- at Zoo Atlanta. Subjects were presented with a quantity compar- human animals do not have experience or cultural norms to dictate ison task on a touch screen computer affixed to their indoor hous- a consistent orientation of magnitude representation. Therefore if ing area. Subjects initiated each trial by touching a green start spatial representation of magnitude is a general cognitive process square in the lower center of the screen. Two white squares that exists outside of humans, non-human primates would likely appeared on the left and right sides of the screen, each containing show a similar reversal in orientation based on task instruction. between two and 10 black dots (Fig. 1). Dots were randomly Recent evidence has suggested that animals as distantly related located within the stimulus borders. The total surface area of the to humans as chickens (Gallus domesticus), may process magni- dots presented in each white square was held constant across tudes spatially (Rugani, Vallortigara, Priftis, & Regolin, 2015a, stimuli. This resulted in smaller diameter dots and larger overall 2015b). However, it is probably premature to reach conclusions dot perimeter the more dots were present in a display. The location about the phylogeny of spatial processing of magnitude with evi- of the ”small” and ‘‘large” stimuli in a pair was counterbalanced dence from only humans and chickens, which are separated by pseudo randomly across trials, such that the lesser quantity of dots over 300 million years of divergent evolution, show major differ- appeared on the left and right sides of the screen equally often. ences in brain laterality, and are tested using substantially differ- Subjects indicated their choice by touching within the borders of ent methods (Drucker & Brannon, 2014; Harshaw, 2015; Kumar one of the two stimuli. During training, selection of the correct & Hedges, 1998; Larsson, 2013; Mangalam & Karve, 2015; quantity was reinforced with an auditory reinforcer on 100% of tri- Rogers, Vallortigara, & Andrew, 2013; Shaki & Fischer, 2015). To als, and a food pellet on 80% of trials. Selection of the incorrect 314 R.P. Gazes et al. / Cognition 168 (2017) 312–319
Table 1 Subject demographics, percent left handed responses on the handedness test, first condition received, and regression slopes calculated on response latency difference scores (rightward responses minus leftward responses) across the 8 adjacent test pairs in the pick large and pick small conditions.
Subject name Species Sex Age in years Proportion left First condition Pick large regression Pick small regression handed responses trained slope (p value) slope (p value) Chantek P. hybrid M 35 1.0 Pick Large À43.52 (0.616) À208.95 (0.050)* Charlie G. gorilla gorilla M 17 1.0 Pick Small 47.82 (0.523) À155.92 (0.034)* Dumadi P. abelii M 6 0.28 Pick Large À25.74 (0.689) À78.38 (0.397) Gunther G. gorilla gorilla M 6 0.18 Pick Large À163.26 (0.025)* 54.08 (0.057) Junior P. abelii M 10 0.63 Pick Small 204.96 (0.021)* À185.30 (0.094) Kali G. gorilla gorilla M 7 0.09 Pick Small À101.17 (0.177) 114.79 (0.094) Madu P. abelii F 29 0.55 Pick Large 6.55 (0.853) À15.71 (0.693) Mbeli G. gorilla gorilla M 10 0.97 Pick Large 139.71 (0.050)* À138.49 (0.313) Satu P. pygmaeus M 9 0.54 Pick Small À202.32 (0.005)* 81.05 (0.031)*
* Indicates a slope that differs significantly from 0 (p < 0.05) using an individual linear regression (7 of 18 possible cases).
Example Example Cri cal right orientations. After completion of testing in the first condition Training Pairs Adjacent Test Pairs (either pick large or pick small; Table 1), subjects received training and testing in the other condition. The number of sessions to reach criterion did not differ between the pick small and pick large conditions or between the first and 3-7 2-3 second trained conditions for either training (linear mixed model with subject as a random factor: main effect of condition:
Mpicksmall = 8.56 ± 5.98 sessions, Mpicklarge = 8.33 ± 4.24, t(7) = 0.17, p = 0.870, main effect of training order [first, second]: À 9-2 10-9 Mfirst = 8.56 ± 4.48, Msecond = 8.33 ± 5.81, t(7) = 0.17, p = 0.870) or testing (linear mixed model with subject as a random factor: main
effect of condition: Mpicksmall = 11.89 ± 3.76 sessions, Fig. 1. Example of stimulus pairs presented during training (left; 3–7 and 9–2) and Mpicklarge = 13.89 ± 5.53, t(7) = À1.01, p = 0.346, main effect of testing (right; 2–3 and 10–9). Within a given stimulus quantity all dots were the training order: Mfirst = 12.11 ± 5.04, Msecond = 13.67 ± 4.30, t(7) same size. = 0.83, p = 0.436).
2.2. Handedness testing quantity was followed by a negative auditory cue, no food, and a five-second black-screen time out period. Handedness was measured for each animal using a simple com- All apes received two conditions presented sequentially— a puterized task. Subjects touched a white dot that appeared ran- ‘‘pick large” condition, in which selection of the stimulus with domly in the center and 4 corners of the screen over 150 trials. more dots in the pair resulted in reinforcement, and a ‘‘pick small” The hand used for each touch was recorded, and the proportion condition, in which selection of the stimulus with fewer dots of trials in which the subject used the left hand was calculated resulted in reinforcement. The order of these two conditions was (Table 1). counterbalanced across subjects (Table 1). Each condition con- sisted of a training phase followed by a testing phase. Training ses- 2.3. Data analysis sions contained 102 trials; 6 trials of each of the 17 training pairs. Training pairs consisted of one small magnitude stimulus (2, 3, or All analyses include only trials from test sessions. Response 4) paired with one large magnitude stimulus (5, 6, 7, 8, 9, or 10, latencies on novel test trials were calculated using median laten- excluding pair 4–5; Fig. 1, left; Patro & Haman, 2012). Once sub- cies on correct trials excluding outliers greater than three standard jects performed above 80% correct in 3 consecutive training ses- deviations above the mean (0.53% of trials excluded). To determine sions, they received test sessions containing all remaining whether apes processed the magnitude of the stimuli, accuracy and possible novel pairs of quantities two through 10 (Fig. 1, right). response latencies were analyzed for distance effects and confor- Test sessions consisted of 104 trials; 5 trials of each of the 17 train- mity with Weber’s law, both of which are diagnostic of magnitude ing pairs, plus one of each of the 19 novel test pairs. Of these 19 processing. The distance effect is indicated by higher accuracy and novel test pairs, the critical pairs for spatial-magnitude congruity shorter response latency with increasing differences between the analyses were the 8 pairs consisting of adjacent quantities (2–3, quantities in the pair. Conformity to Weber’s law is indicated by 3–4, 4–5, 5–6, 6–7, 7–8, 8–9, 9–10). This set of critical test pairs higher accuracy and shorter response latency with increasing controlled for the absolute difference between quantities in the ratios of the larger to the smaller of the two quantities in the pair. pairs, and provided continuous measurements from low quantity These effects would be expected regardless of whether apes were comparisons (pair 2–3) through high quantity (pair 9–10) compar- relying on dot quantity or dot size to make their choices, as both isons. Training pairs were reinforced as during training, except that represent magnitude dimensions. 100% of correct trials were accompanied by a food reinforcer. Con- To test for a spatial representation of magnitude, the difference sistent with the partial reinforcement experienced during training, in response latency between correct responses made to the right all choices on test pairs were reinforced with an auditory reinforcer and those made to the left (rightward responses minus leftward only, regardless of whether the response was correct. This non- responses) was calculated for each of the eight critical test pairs differential reinforcement prevented subjects from learning during in which adjacent quantities were presented (i.e. 2–3, 3–4, 4–5, the test trials. Subjects received test trials intermixed with training 5–6, 6–7, 7–8, 8–9, 9–10). For each of the nine subjects in each trials until they had made at least one correct response on every of the two conditions simple regression models were fit to estimate numerical test pair in both the small on the left and small on the intercepts and slopes of the relationship between the quantity and R.P. Gazes et al. / Cognition 168 (2017) 312–319 315 the latency difference scores (Table 1). Spatial representation of detected. Whether the overall slopes of both LMM differed signifi- magnitude would be indicated if animals responded faster to one cantly from zero was tested with t-tests using the Satterthwaite side of space when processing small quantity test pairs (e.g. 2 vs approximation of the degrees of freedom (R package lmerTest; 3; 3 vs 4) and faster to the other side of space when processing Kuznetsova, Brockhoff, & Christensen, 2015). The 0.05 significance large quantity test pairs (e.g. 8 vs 9; 9 vs 10), and reverse this pat- threshold was used in all statistical tests. tern between the pick small and pick large conditions. Unlike The sample size used in this study (9 apes) was planned a priori humans, apes lack cultural norms for representing magnitudes in and corresponded to the total number of apes available. No sub- a particular orientation. This lack of culture may lead individual jects were dropped from the study or from the analyses. apes to show different orientations, resulting in an average slope close to 0. However, if apes reverse the orientation of their repre- sentation of magnitude in response to task instructions, we expect 3. Results a systematic reversal of individual slopes between the pick small and pick large conditions. Such a reversal would be evident as a 3.1. Apes engaged in magnitude processing negative correlation between slopes in the pick small and pick large conditions. We tested for this correlation using Spearman’s Apes performed above chance on novel test trials (mean for all rank correlation test. test pairs combined: M = 77.50 ± 4.30% correct; one sample t-test: t Although apes do not have human-like experience with reading (8) = 19.18, p < 0.001), and on the critical subset of test trials with or counting direction, factors such as species, condition order, or adjacent quantity pairs that were used for the spatial-magnitude individual hand preferences (Fischer & Brugger, 2011) may deter- analyses (2 vs 3; 3 vs 4, 9 vs 10, etc.; M = 71.01 ± 4.73% correct; mine the orientation of spatial representations. To determine the one sample t-test: t(8) = 13.95, p < 0.001). impact of these factors on slope orientation we fitted two Linear Across all training and test pairs, apes showed performance pat- Mixed Models (LMMs; one for pick small and one for pick large) terns consistent with magnitude processing (Cantlon & Brannon, to the latency difference scores. These models included the lower 2006), a prerequisite for spatial-magnitude correspondence. Per- quantity in each adjacent test pair as the independent variable. formance conformed to Weber’s law, with faster response latencies Species, condition order, and handedness were added to the mod- and higher accuracy associated with larger ratios between compar- els as fixed effect control variables interacting with the lower ison quantities (Fig. 2; Spearman’s rank correlation: response quantity in the pair. In addition, the intercept and the slope of latency: r(34) = À0.86, p < 0.001; accuracy: r(34) = 0.97, the regression lines were allowed to vary randomly among sub- p < 0.001). The ratios used for these analyses and shown on the jects following normal distributions centered at zero. x-axis in Fig. 2 were calculated using the number of dots in each LMMs were fitted using software R v.3.1.2 (R Core Team, 2014) stimulus. As expected, the pattern of significance holds when the and R package lme4 (R package lme4; Bates, Machler, Bolker, & ratios are determined using dot diameter as well (Spearman’s rank Walker, 2015). The normality of the random effects and residuals correlation: response latency: r(34) = 0.85, p < 0.001; accuracy: r was carefully inspected using normal-quantile plots and Shapiro (34) = À0.96, p < 0.001). Additionally, performance was consistent tests and no deviation to the assumptions of the LMMs was with the distance effect, with shorter response latencies and higher
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Median Reac on Median Time (ms) 800 50 02460246 Ra o of Comparison S muli Ra o of Comparison S muli
Fig. 2. Median reaction time (left) and average accuracy (right) by the ratio of the quantity of the comparison stimuli in the pair, across all training pairs during test sessions collapsed across pick large and pick small conditions.
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Median Reac on Time (ms) 800 50 1234567 1234567 Distance Distance
Fig. 3. Median reaction time (left) and average accuracy (right) by quantity difference distance across all training and test pairs during test sessions collapsed across the pick small and pick large conditions. 316 R.P. Gazes et al. / Cognition 168 (2017) 312–319 accuracy associated with larger distances between quantities in a 2, 3, and 4 were either always (pick small) or never (pick large) pair (Fig. 3; response latency: F(7) = 27.71, p < 0.001, linear con- reinforced, a distance effect could result from differences in asso- trasts F(1,8) = 45.79, p < 0.001; accuracy: F(7) = 41.50, p < 0.001, ciative strength accrued during training. To determine if this was linear contrasts F(1,8) = 62.82, p<0.001). Because low quantities the case, follow up analyses were conducted on pairs from the pick small condition in which the low quantity stimulus was 4 (i.e. pairs 150 4–5, 4–6, 4–7, 4–8, 4–9, 4–10). Quantity 4 was always reinforced in training and quantities 5, 6, 7, 8, 9, and 10 were never reinforced in 100 training. The relative associative strength of the stimuli was there- 50 fore constant across all distances in this subset of test pairs. The distance effect held across these pairs (response latency: F(5) 0 = 3.84, p = 0.006, linear contrasts F(1,8) = 4.95, p=0.057; accuracy: -300 -200 -100 0 100 200 300 F(5) = 8.17, p < 0.001, linear contrasts F(1,8) = 11.82, p = 0.009), -50 indicating that the distance effect resulted from the ratios of the
Pick Small Slope -100 comparison stimuli, not from differences in the reinforcement his- tory of the stimuli. -150
-200 3.2. Task instruction controlled the orientation of spatial representation -250 Pick Large Slope Like humans comparing animal sizes and large quantities, apes showed systematic reversal of the orientation of their spatial mag- Fig. 4. Negative correlation between spatial-magnitude slopes in the pick small and nitude representation between the pick large and pick small pick large condition for the 9 subjects. Animals with strong negative slopes in the instruction conditions. There was a significant negative correlation pick small condition tended to show strong positive slopes in the pick large between individual slopes of the response latency regression lines condition (lower right quadrant), while animals with strong positive slopes in the between the pick small and pick large conditions (Fig. 4; Spearman pick small condition tended to show strong negative slopes in the pick large condition (upper left quadrant). rank correlation: r(7) = À0.76, p = 0.018) such that subjects who
1900 Kali Gunther Satu
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-1900 Response Latency Difference Score (R-L) 1900 Charlie Chantek 600 Madu
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Fig. 5. Individual data for the pick small (grey circles) and pick large (black squares) conditions across the 8 adjacent test pairs. Response latency difference scores are in milliseconds. Lines indicate best fit regression line (pick small: solid grey; pick large: dashed black). Positive slopes indicate right-to-left spatial-magnitude orientation, negative slopes indicate left-to-right spatial-magnitude orientation. Note: data for Satu pick large 7 vs. 8 and Chantek pick small 8 vs. 9, are not shown and were not included in analysis because these data points were outliers (>3 standard deviations above the mean). R.P. Gazes et al. / Cognition 168 (2017) 312–319 317 showed a right-to-left orientation in the pick small condition leftward bias for small numbers and a rightward bias for large (Fig. 5; positive slope; n = 5) tended to show a left-to-right orienta- numbers (Rugani et al., 2015a, 2015b). Chicks trained to find food tion in the pick large condition (negative slope), and vice versa. The behind a target displaying 5 dots spontaneously chose the display negative correlation also indicates stable individual tendencies for on the left when presented with two identical choice stimuli smal- spatial representation across conditions; animals that showed the ler than the target (2 dots) and the display on the right when pre- strongest spatial representation in one condition also showed the sented with choice stimuli larger than the target (8 dots). This may strongest spatial representation in the other condition. suggest a phylogenetically ancient predisposion to represent quan- tity in a left-to-right orientation. However, concluding that the behavior of chicks in this test is controlled by the same cognitive 3.3. Individual orientations did not differ systematically by species, processes that result in many humans showing a left to right orga- handedness, or training order nization in magnitude processing may be premature for several reasons. First, the behavioral evidence from chicks indicates con- LMM analysis indicated that apes showed individual variability siderable inter-individual differences, with more than half the in orientations of spatial magnitude congruity (likelihood ratio test chicks failing to show the left-to-right orientation (Mangalam & of significance of random effects of subject identity on slopes: pick Karve, 2015). Second, avian brains are highly lateralized compared small: X2 (2, N = 9) = 6.64, p = 0.022; pick large: X2 (2, N = 9) with primates (Harshaw, 2015; Larsson, 2013; Rogers et al., 2013), = 14.51, p < 0.001). Therefore, the mean slope across all tested apes and indeed evidence for laterality in nonhuman primates is mixed was not significantly different from 0 (pick small: t(7.94) = À1.40 (Oleksiak, Postma, van der Ham, Klink, & van Wezel, 2011). Finally, p = 0.20; pick large: t(8.06) = À0.33, p = 0.75). Individual slopes avians and mammals diverged over 300 million years ago (Kumar did not vary systematically by species, handedness, or training & Hedges, 1998), so data from more species across this phyloge- order (LMM, t-tests with Satterthwaite approximation: all netic range are needed before conclusions can be drawn about ps > 0.1). common origins of cognitive processes. While Rugani et al. have addressed many of these points (Rugani, Vallortigara, Priftis, & 4. Discussion Regolin, 2016a, 2016b, 2015a, 2015b), it remains possible that the left-to-right bias seen in humans and chicks may be the result We found evidence for spatial representation of magnitude in of a convergence in behavior based on distinct cognitive processes- nonhuman apes, suggesting that use of space to represent other brain laterality in the chicks and cultural convention in English- dimensions is phylogenetically ancient. Like humans processing speaking humans. In the present study four of the apes showed magnitudes in less familiar domains, apes reversed their orienta- orientations of spatial representation in one direction while three tion of spatial representation based on instruction, such that they showed orientations in the opposite direction. The remaining two accessed this representation from their preferred point of reference apes show no clear orientation. These differences in orientation location in both conditions. Additionally, animals were consistent were not explained by species, training order, or handedness, in the strength of their representations across conditions, with although it remains possible that these differences could be individual animals tending to show either strong or weak effects explained by other idiosyncratic characteristics including experi- under both pick large and pick small instructions. While apes did ence with caregivers. These findings, combined with evidence of not adopt a single orientation as a group, these results indicate flexibility in the spatial orientation of magnitude representation stable tendencies for spatial representation within individuals. in humans based on task instruction (Bachtold et al., 1998; Shaki, Given the extensive experience most adult humans have with Petrusic, et al., 2012), culture (Shaki, Fischer, et al., 2012; Zohar- number lines and reading directions, it is not surprising that group Shai, Tzelgov, Karni, & Rubinsen, 2017), language priming (Shaki level orientations for small number comparisons tend to be consis- & Fischer, 2008), and across individuals (Nuerk et al., 2005; tent across task instructions within human cultures (Ginsburg & Wood et al., 2006) suggest that physiological determinants may Gevers, 2015; Lee et al., 2016; Shaki, Petrusic, et al., 2012). Individ- be of limited importance in determining the orientation of spatial ual differences in orientation and reversals in orientation in representation in primates. response to instructions similar to those shown by apes are only Because total surface area of the dots was controlled in the pre- seen in humans when participants have no preexisting long term sent task, total dot perimeter co-varied positively and dot size co- representation organizing the content of the domain being tested. varied negatively with dot quantity. Previous findings suggest that Like apes, pre-school aged children, who also have limited cultural non-human primates preferentially rely on quantity information experience relative to adults, show variability in spatial orientation over size or surface area (Brannon & Terrace, 2000), but it is not across individuals. For example, while 89% of British preschool possible to determine from our results whether choices in this task children (3–6 years) presented with a line of objects counted them were controlled by quantity, perimeter, or individual dot size. in a linear order, only 60% of those counted in the culturally typical However, discrimination of quantity, size, and perimeter are all left-to-right direction, while 40% counted in the right-to-left direc- magnitude judgments, and gorillas and orangutans showed dis- tion (Shaki, Fischer, & Gobel, 2012). Human adults performing a tance effects and patterns consistent with Weber’s law and typical non-numerical quantity discrimination task similar to the one in of human performance on magnitude comparison tasks. These the current experiment show instruction based reversal of spatial performance patterns indicate that apes were attending to a mag- orientations consistent with that shown by apes (Patro & Shaki, nitude dimension of the stimuli, either size, perimeter, or quantity, 2016). This variability indicates that the tendency to organize and provide additional support for common magnitude represen- information spatially may be a fundamental organizing feature of tation processes in human and non-human primates (Beran, cognition, but that the orientation of those representations is 2008; Brannon & Terrace, 2002). impacted by culture and experience. The spatial organization of cognition shown by the apes may be A limitation of our study is that we only tested ape species, and a basic organizing feature of cognition (de Hevia, Girelli, & Cassia, so cannot confidently draw conclusions outside of great apes. 2012; McCrink & Opfer, 2014; Shaki, Fischer, et al., 2012; Walsh, However, evidence from experiments with much more distantly 2003). Behavioral congruity between magnitude and space is pre- related chicks (Gallus domesticus) may suggest that spatial repre- sent from early in development in humans. Pre-verbal pre- sentation of magnitude may be more widespread among verte- counting infants show interactions between number and space brates. Three day old chicks have been reported to show a (de Hevia, Addabbo, Girelli, & Macchi-Cassia, 2014; de Hevia & 318 R.P. Gazes et al. / Cognition 168 (2017) 312–319
Spelke, 2010; Lourenco & Longo, 2010), and pre-counting children Brannon, E. M., & Terrace, H. S. (2002). The evolution and ontogeny of ordinal as young as 4 years of age show congruity between space and mag- numerical ability. In M. Bekoff & C. Allen (Eds.), The cognitive animal: Empirical and theoretical perspectives on animal cognition (pp. 197–204). Cambridge, MA: nitude (Patro & Haman, 2012). Quantities may be represented MIT Press. topographically in parietal cortex, mimicking representations of Cantlon, J. F., & Brannon, E. M. (2006). Shared system for ordering small and large space (Harvey, Klein, Petridou, & Dumoulin, 2013). Additionally, numbers in monkeys and humans. Psychological Science, 17(5), 401–406. Cutini, S., Scarpa, F., Scatturin, P., Dell’Acqua, R., & Zorzi, M. (2014). Number-space there is overlap in brain areas activated during the processing of interactions in the human parietal cortex: Enlightening the SNARC effect with magnitude and space in humans and non-human primates functional near-infrared spectroscopy. Cerebral Cortex, 24(2), 44–51. (Cutini, Scarpa, Scatturin, Dell’Acqua, & Zorzi, 2014; Hubbard Dahl, C. D., & Adachi, I. (2014). Conceptual metaphorical mapping in chimpansees (Pan troglodytes). eLIFE, 2, e00932. et al., 2005), with the horizontal intraparietal sulcus implicated de Hevia, M. D., Addabbo, M., Girelli, L., & Macchi-Cassia, V. (2014). Human infants’ in both magnitude comparison and spatial attention (Hubbard preference for left-to-right oriented increasing numerical sequences. PLoS One, et al., 2005; Rusconi et al., 2011). The results with apes in the pre- 9(5), e96412. de Hevia, M. D., Girelli, L., & Cassia, V. M. (2012). Minds without language represent sent study combined with evidence from humans therefore add to number through space: Origins of the mental number line. Frontiers in a growing literature that suggests that spatial representation of Psychology, 3, 1–4. magnitude is a fundamental characteristic of at least primate de Hevia, M. D., & Spelke, E. S. (2010). Number-space mapping in human infants. minds, and may be much more widespread among vertebrates. Psychological Science, 21(5), 653–660. Dehaene, S., Bossini, S., & Giraux, P. (1993). The mental representation of parity and number magnitude. Journal of Experimental Psychology-General, 122(3), 371–396. 6. Author note Drucker, C. B., & Brannon, E. M. (2014). Rhesus monkeys (Macaca mulatta) map number onto space. Cognition, 132(1), 57–67. R.P. Gazes, Zoo Atlanta, now at Bucknell University; R. R. Hamp- Finstermeier, K., Zinner, D., Brameier, M., Meyer, M., Kreuz, E., Hofreiter, M., et al. (2013). A mitogenomic phylogeny of living primates. PLoS One, 8(7). ton and R.F.L. Diamond, Department of Psychology, Emory Univer- Fischer, M. H., & Brugger, P. (2011). When digits help digits: Spatial-numerical sity and Yerkes National Primate Research Center; J. Hope, associations point to finger counting as prime example of embodied cognition. Neuroscience Graduate Program, Emory University; D. Caillaud, Frontiers in Psychology, 2(260). Fischer, M. H., Castel, A. D., Dodd, M. D., & Pratt, J. (2003). Perceiving numbers Dian Fossey Gorilla Fund International and Department of Anthro- causes spatial shifts in attention. Nature Neuroscience, 6(6), 555–556. pology, University of California Davis; T.S. Stoinski, Zoo Atlanta and Fischer, M. H., Shaki, S., & Cruise, A. (2009). It takes just one word to quash a SNARC. Dian Fossey Gorilla Fund International. Experimental Psychology, 56(5), 361–366. Gazes, R. P., Lazareva, O. F., Bergene, C. N., & Hampton, R. R. (2014). Effects of spatial This work was supported by Zoo Atlanta and by National training on transitive inference performance in humans and rhesus monkeys. Science Foundation awards IOS-1146316, BCS-1632477, and BCS- Journal of Experimental Psychology: Animal Learning and Cognition, 40(2), 0745573 to R.R. Hampton. J.M. Hope was supported by the BP- 477–489. Initiative funded by NIH grant R25GM097636. We thank Kimberly Gevers, W., Reynvoet, B., & Fias, W. (2003). The mental representation of ordinal sequences is spatially organized. Cognition, 87(3), B87–B95. Burke and Meghan Sosnowski for help testing subjects, Zoo Atlanta Ginsburg, V., & Gevers, W. (2015). Spatial coding of ordinal information in short- primate staff for their support, and Stella Lourenco and Olga Lazar- and long-term memory. Frontiers in Human Neuroscience, 9(8). eva for helpful discussion. Harshaw, C. (2015). Comment on ‘‘Number-space mapping in the newborn chick resembles humans’ mental number line”. Science, 348(6242), 2. All procedures were approved by the Zoo Atlanta research Harvey, B. M., Klein, B. P., Petridou, N., & Dumoulin, S. O. (2013). Topographic review board and Zoo Atlanta is an AZA accredited facility. All representation of numerocity in the human parietal cortex. Science, 341, research complied with the Guide to the Care and Use of Labora- 1123–1126. Holmes, K. J., & Lourenco, S. F. (2011). Common spatial organization of number and tory Animals. emotional expression: A mental magnitude line. Brain and Cognition, 77(2), 315–323. Hubbard, E. M., Piazza, M., Pinel, P., & Dehaene, S. (2005). Interactions between Author Contributions number and space in the parietal cortex. Nature Reviews Neuroscience, 6, 435–448. R.P. Gazes developed the study concept and design. R.P. Gazes, J. M. Kumar, S., & Hedges, B. S. (1998). A molecular timescale for vertebrate evolution. Nature, 392, 917–920. Hope, and R.F.L. Diamond conducted the experiments and R.P. Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. B. (2015). lmerTest: Tests in Gazes and J.M. Hope designed and analyzed the handedness task. linear mixed effects models.
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