Elsevier

Cognition

Volume 132, Issue 1, July 2014, Pages 57-67
Cognition

Rhesus monkeys (Macaca mulatta) map number onto space

https://doi.org/10.1016/j.cognition.2014.03.011Get rights and content

Highlights

  • Monkeys represent ordinal information about identical objects.

  • Monkeys map number onto space.

  • The space–number mapping has evolutionary, rather than purely cultural, roots.

Abstract

Humans map number onto space. However, the origins of this association, and particularly the degree to which it depends upon cultural experience, are not fully understood. Here we provide the first demonstration of a number–space mapping in a non-human primate. We trained four adult male rhesus macaques (Macaca mulatta) to select the fourth position from the bottom of a five-element vertical array. Monkeys maintained a preference to choose the fourth position through changes in the appearance, location, and spacing of the vertical array. We next asked whether monkeys show a spatially-oriented number mapping by testing their responses to the same five-element stimulus array rotated ninety degrees into a horizontal line. In these horizontal probe trials, monkeys preferentially selected the fourth position from the left, but not the fourth position from the right. Our results indicate that rhesus macaques map number onto space, suggesting that the association between number and space in human cognition is not purely a result of cultural experience and instead has deep evolutionary roots.

Introduction

Number and space are integrally linked in the human mind (Bueti and Walsh, 2009, Fias and Fischer, 2005, Hubbard et al., 2005). A prominent behavioral manifestation of this interaction is the SNARC (Spatial–Numerical Association of Response Codes) effect, whereby smaller numbers are associated with one side of space and larger numbers with the other. In the original demonstration of the SNARC effect, subjects making parity judgments (i.e. odd or even) were faster to respond to smaller numbers with a left-side response key and larger numbers with a right-side response key (Dehaene, Bossini, & Giraux, 1993). This pattern has been replicated in a variety of experimental paradigms and populations (reviewed in Fias and Fischer (2005)), including in the auditory modality among both blind and sighted subjects (Castronovo & Seron, 2007), indicating that the number–space mapping is amodal. Interestingly, in cultures that read from right to left the SNARC effect can be attenuated or even reversed, suggesting that experience may drive the mapping of number onto space (Shaki and Fischer, 2008, Shaki et al., 2009, Zebian, 2005).

Although the specific orientation of the SNARC effect varies with cultural conventions for reading direction, its presence across cultures suggests that the spatial mapping of numbers may be a universal cognitive strategy (Gobel, Shaki, & Fischer, 2011). In fact, preschool children, who have not begun learning to read, are quicker and more accurate at finding an object hidden in a numbered compartment when compartment numbers increase from left to right rather than right to left, indicating they expect numbers to increase from left to right (Opfer and Furlong, 2011, Opfer et al., 2010). These results suggest that spatial–numerical associations are not a product of extensive formal education or reading experience. Moreover, even preverbal infants, who have not yet learned to count or use measurement tools like rulers, are sensitive to the relationship between number and space (de Hevia & Spelke, 2010). When habituated to dot arrays (i.e. non-symbolic numbers) presented in either increasing or decreasing order, eight-month-old infants looked longer (indicating a novelty response) to line lengths presented in the opposite, but not the same, order. Furthermore, when infants were shown several exemplars of dot arrays paired with lines such that the line length either increased (positive pairing) or decreased (inverse pairing) with number of dots, infants extracted the rule from the positive but not the inverse pairing. Infants also showed a preference for positive pairings between numbers and line lengths over inverse pairings. These findings indicate that human infants have a predisposition to relate number to space and that our privileged number–space mapping does not depend upon language. An important question then is whether number is mapped onto space in any nonhuman species.

Rugani and colleagues found evidence for a left-to-right mental number line in baby chickens. First, they showed that 5-day-old domestic chicks (Gallus gallus) could learn to identify the third, fourth, or sixth hole in a series of ten identical holes sagittal to the chicks’ starting point, even when distance between holes was varied (Rugani, Regolin, & Vallortigara, 2007). Critically, when the line of holes was rotated 90° so that it was horizontal to the chicks’ starting point, chicks that had learned to select the fourth hole preferentially approached the fourth hole from the left, and rarely the fourth hole from the right. This finding was investigated further in newborn chicks and adult nutcrackers (Nucifraga columbiana). When trained to select the fourth (or sixth) item in a sagitally-oriented line of sixteen identical items, both species preferentially chose the fourth (or sixth, respectively) item from the left – but not the right – in a horizontally-oriented line (Rugani, Kelly, Szelest, Regolin, & Vallortigara, 2010). However, when inter-element distances were varied during training or test, chicks were equally likely to choose the correct position from the left or the right (Rugani, Vallortigara, Vallini, & Regolin, 2011). The authors interpret their results as evidence for asymmetric processing of number and space. They posit that the purely ordinal aspect of the array is bilaterally represented in the left and right cerebral hemispheres, whereas the purely spatial aspect is unilaterally represented in the right hemisphere, biasing attention to the left side of space only when spatial cues (such as constant inter-element distance) could be used to complete the task. This explanation seems viable in birds, who have lateralized visual fields and a complete crossing of nerves at the optic chiasm, coupled with minimal interhemispheric connections (lack of corpus callosum), which results in visual information from one side of space being represented almost entirely in the opposite hemisphere (Larsson, 2013, Rogers et al., 2013). This strong lateralization likely underlies the numerous behavioral asymmetries observed in birds (Rogers et al., 2013). Primates, on the other hand, receive visual information from both sides of space in each cerebral hemisphere, due to frontally placed eyes, only partial crossing of nerves at the optic chiasm, and communication between the hemispheres (Larsson, 2013). Thus although Rugani and colleagues found a SNARC-like effect in a non-human species, the mechanism driving this effect could be different from that driving the effect in humans. Exploring whether monkeys orient numerical representations spatially might yield more information about the evolutionary precursors of the spatial mapping of number in humans.

The SNARC effect depends upon the ordinality inherent in number representation. The ability to identify a particular ordinal position in a sequence is crucial for many everyday activities, such as following directions (i.e. take the third right) or locating a car in a parking lot (i.e. in the eighth spot of the fifth row). Using numbers to denote rank or ordinality is theoretically distinguished from using numbers to denote quantity or cardinality. Indeed, behavioral (Franklin et al., 2009, Rubinsten and Sury, 2011, Turconi et al., 2006), neurological (Butterworth, 1997, Turconi and Seron, 2002), and neuroimaging (Tang et al., 2008, Turconi et al., 2004, Zorzi et al., 2011) evidence indicates that distinct cognitive processes are engaged when accessing the ordinal rather than the cardinal meaning of numbers. A broad range of animal species can compare sets to choose the greater or lesser numerical value: birds (e.g. Aïn et al., 2008, Bogale et al., 2011, Roberts, 2010), fish (e.g. Agrillo et al., 2010, Gómez-Laplaza and Gerlai, 2012, Piffer et al., 2011, Stancher et al., 2013), amphibians (e.g. Krusche et al., 2010, Uller et al., 2003), non-human primates (e.g. Beran, 2008, Brannon and Terrace, 1998, Hanus and Call, 2007), and other mammals (e.g. Jaakkola et al., 2005, Uller and Lewis, 2009, Vonk and Beran, 2012, Ward and Smuts, 2007).

Other research shows that animals can learn to respond to arbitrary stimuli in prescribed ordinal sequences and represent the abstract ordinal position of each item (e.g. monkeys: Chen et al., 1997, Terrace, 2005, Terrace et al., 2003; domestic chicks: Rugani, Regolin et al., 2007). Pigeons show more limited ability to encode ordinal positions of arbitrary items in a sequence (Scarf and Colombo, 2010, Terrace, 1993, Terrace et al., 1996). Rats (Davis and Bradford, 1986, Suzuki and Kobayashi, 2000), bees (Dacke & Srinivasan, 2008), and chicks (Rugani, Regolin et al., 2007) moving through space can learn to select a target landmark based on how many identical landmarks they have already passed. Only one previous study tested the ability of a non-human primate to respond selectively to a particular ordinal position in a sequence. Using the Wisconsin General Test Apparatus, Ruby trained a single rhesus monkey to select the third block from the left in a formboard from three, four, five, six, or seven identical blocks in a row (Ruby, 1984). However, in that study the food reward was always placed in the hole under the correct block, leaving open the possibility that the monkey used odor cues. Spacing between the blocks was also held constant throughout the experiment, so the monkey may have relied on spatial position rather than ordinal position.

We developed a set of touch-screen tasks for rhesus macaques that parallel the experiments Rugani and colleagues conducted with birds (Rugani, Regolin et al., 2007, Rugani, Kelly et al., 2010, Rugani, Vallortigara et al., 2011). By using a touch-screen, we avoided experimenter cuing and odor cuing, and gained precise control over the appearance and spatial placement of stimuli. First we trained monkeys to select the fourth item from the bottom in a vertical array of five identical items presented on a touch-screen. We then tested their ability to identify the fourth position over changes in the appearance, location, and spacing of the stimuli. Next we rotated the array ninety degrees into a horizontal line to assess whether monkeys map number to space in a preferred direction. If monkeys do not have a spatially oriented mental number line, they should respond to the fourth position from the left and fourth position from the right with equal likelihood. If macaques do have a spatially oriented mental number line, they should preferentially select the fourth position from the left, suggesting a left-to-right orientation, or the fourth position from the right, suggesting a right-to-left orientation, but not both.

Section snippets

Subjects

Four adult male rhesus macaques served as subjects (Macaca mulatta, mean age = 9.8 years, range = 7–15 years). Monkeys were housed singly (n = 3) or in pairs (n = 1) in a vivarium, and those housed in pairs were separated for testing. All animals had participated in previous touch-screen tasks unrelated to the present study. Fresh fruit and Purina monkey chow were provided daily. The monkeys’ water consumption was restricted for unrelated experiments.

Apparatus

A 15-inch touch-sensitive computer monitor (Elo

Ordinal position testing

On average subjects required 16 training sessions (range = 13–19) before moving to the test sessions. During training and every testing condition, subjects always completed the full number of trials constituting each session. One-tailed exact binomial tests were used to determine whether each position was selected above the 20% chance expectation. Here we report data on all subjects together; individual subjects’ accuracy and binomial test p-values are shown in Supplementary Tables S1–S14.

Discussion

We investigated whether rhesus monkeys, like humans, map number to space. To test this question, we first trained monkeys to select a specific ordinal position in a vertical array of homogeneous items. All four monkeys rapidly learned to identify the fourth oval from the bottom of a five-oval vertical array. They maintained high performance when the color or shape of the stimuli was altered, indicating that their responses did not depend upon the particular appearance of the array elements.

Acknowledgements

We thank Monica Carlson and all members of Elizabeth Brannon’s and Michael Platt’s labs for assistance with data collection and helpful discussions of this study. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship Program under Grant No. 1106401 to C.B.D., and NIH Grant R01-EY-019303 and the James McDonnell Scholar Award to E.M.B.

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