1. Hemispheric Asymmetries in Nonhuman Animal Perception

- Original:

Hauser, M.D., and K. Andersson. 1994. Left Hemisphere Dominance for Processing Vocalizations in Adult, but Not Infant, Rhesus Monkeys: Field Experiments. Proceedings of the National Academy of Sciences 91: 3946-3948.

ABSTRACT In humans, the left hemisphere of the brain is dominant for processing language. To assess the evolutionary origins of this neuropsychological mechanism, playback experiments were conducted on a large population of free-ranging rhesus monkeys (Macaca mulatta). Playbacks provided an equal opportunity to orient the right or left ear toward the speaker. Results revealed that 61 of 80 adult rhesus favored the right ear (left hemisphere) when vocalizations from their own repertoire were heard but favored the left ear when listening to heterospecific vocalizations. In contrast, infants less than a year old showed no perceptual asymmetry for conspecific or heterospecific calls. Thus, like humans, adult rhesus monkeys also evidence left hemisphere dominance for processing species-specific vocalizations. The emergence of such asymmetry, however, may depend on both differential maturation of the two hemispheres and experience with the species-typical vocal repertoire.

- Replications:

Ghazanfar, A.A., D. Smith-Rohrberg, M.D. Hauser. 2001. The Role of Temporal Cues in Rhesus Monkey Vocal Recognition: Orienting Asymmetries to Reversed Calls. Brain, Behavior and Evolution 58: 163-172.

Böye, M., O. Güntürkün, and J. Vauclair. 2005. Right Ear Advantage for Conspecific Calls in Adults and Subadults, but Not Infants, California Sea Lions (Zalophus californianus): Hemispheric Specialization for Communication? European Journal of Neuroscience 21: 1727-1732.

Siniscalchi M., A. Quaranta, and L.J. Rogers. 2008. Hemispheric Specialization in Dogs for Processing Different Acoustic Stimuli. PLoS ONE 3(10): e3349. doi:10.1371/journal.pone.0003349

Marzoli, D., and L. Tommasi. 2010. Side Biases in Humans (Homo sapiens): Three Ecological Studies on Hemispheric Asymmetries. Naturwissenchaften 96: 1099-1106.

2. Hemispheric Asymmetries in Production of Facial Expressions/Vocalizations

- Original:

Hauser, M.D. 1993. Right Hemisphere Dominance for the Production of Facial Expression in Monkeys. Science 261: 475–477.

ABSTRACT In humans, the left side of the face (right hemisphere of the brain) is dominant in emotional expression. In rhesus monkeys, the left side of the face begins to display facial expression earlier than the right side and is more expressive. Humans perceive rhesus chimeras created by pairing the left half of the face with its mirrorreversed duplicate as more expressive than chimeras created by right-right pairings. That the right hemisphere determines facial expression, and the left hemisphere processes species-typical vocal signals, suggests that human and nonhuman primates exhibit the same pattern of brain asymmetry for communication.

- Replications:

Hook-Costigan, M.A., and L.J. Rogers. 1998. Lateralized Use of the Mouth in Production of Vocalizations by Marmosets. Neuropsychologia 36: 1265-1273.

Hauser, M.D., and K. Akre. 2001. Asymmetries in the Timing of Facial and Vocal Expressions by Rhesus Monkeys: Implications for Hemispheric Specialization. Animal Behaviour 61: 391–400.

Fernández-Carriba, S., A. Loeches, A. Morcillo, and W.D. Hopkins. 2002. Asymmetry in Facial Expression of Emotions by Chimpanzees. Neuropsychologia 40: 1523–1533.

Wallez, C., and J. Vauclair. 2011. Right Hemisphere Dominance for Emotion Processing in Baboons. Brain and Cognition 75: 164-169

3. Language

- Original:

Ramus, F., M.D. Hauser, C.T. Miller, D. Morris, and J. Mehler. 2000. Language Discrimination by Human Newborns and Cotton-Top Tamarin Monkeys. Science 288: 349-351

ABSTRACT Humans, but no other animal, make meaningful use of spoken language. What is unclear, however, is whether this capacity depends on a unique constellation of perceptual and neurobiological mechanisms or whether a subset of such mechanisms is shared with other organisms. To explore this problem, parallel experiments were conducted on human newborns and cotton-top tamarin monkeys to assess their ability to discriminate unfamiliar languages. A habituation-dishabituation procedure was used to show that human newborns and tamarins can discriminate sentences from Dutch and Japanese but not if the sentences are played backward. Moreover, the cues for discrimination are not present in backward speech. This suggests that the human newborns’ tuning to certain properties of speech relies on general processes of the primate auditory system.

- Corroborations (same/different species, same/different method, same/different computation):

Hauser, M.D., E.L. Newport, and R.N. Aslin. 2001. Segmentation of the Speech Stream in a Nonhuman Primate: Statistical Learning in Cotton-Top Tamarins. Cognition 78: B53-B64.

Toro, J.M., J.B., Trobalon, and N. Sebastian-Galles. 2003. The Use of Prosodic Cues in Language Discrimination Tasks by Rats. Animal Cognition 6: 131-136.

Fitch, W.T., and M.D. Hauser. 2004. Computational Constraints on Syntactic Processing in a Nonhuman Primate. Science 303: 377-380.

Newport, E.L., M.D. Hauser, G. Spaepen, and R.N. Aslin. 2004. Learning at a Distance II. Statistical Learning of Non-Adjacent Dependencies in a Nonhuman Primate. Cognitive Psychology 49: 85-117.

Toro, J.M., and J.B. Trobalon. 2005. Statistical Computations Over a Speech Stream in a Rodent. Perception and Psychophysics 67: 867-875.

Toro, J.M., J.B. Trobalon, and N. Sebastian-Galles. 2005. Effects of Backward Speech and Speaker Variability in Language Discrimination by Rats. Journal of Experimental Psychology: Animal Behavior Processes 31: 95-100.

Tincoff, R., M.D. Hauser, F. Tsao, G. Spaepen, F. Ramus, and J. Mehler. 2005. Language Discrimination Based on Rhythmic Cues: Further Experiments on Cotton-Top Tamarins. Developmental Science 8: 26-35.

Watanabe, S., E. Yamamoto, and M. Uozumi. 2006. Language Discrimination by Java Sparrows. Behavioural Processes 73: 114-116.

Murphy, R.A., E. Mondraógn, and V.A. Murphy. 2008. Rule Learning by Rats. Science 319: 1849-1851.

Endress, A.D., D. Cahill, S. Block, J. Watumull, and M.D. Hauser. 2009. Evidence of an Evolutionary Precursor to Human Language Affixation in a Non-Human Primate. Biology Letters 5: 749-751.

Hauser, M.D., and D. Glynn. 2009. Can Free-Ranging Rhesus Monkeys (Macaca mulatta) Extract Artificially Created Rules Comprised of Natural Vocalizations? Journal of Comparative Psychology 123: 161-167.

Endress, A.D., S. Cardan, E. Versace, and M.D. Hauser. 2010. The Apes’ Edge: Spontaneous Positional Learning in Chimpanzees and Humans. Animal Cognition 13: 483-495.

Abe, K., and D. Watanabe. 2011. Songbirds Possess the Spontaneous Ability to Discriminate Syntactic Rules. Nature Neuroscience. doi: 10.1038/nn.2869

4. Rational Action

- Original:

Wood, J.N., D.D. Glynn, B.C. Phillips, and M.D. Hauser. 2007. The Perception of Rational, Goal-Directed Action in Nonhuman Primates. Science 317: 1402-1405.

ABSTRACT Humans are capable of making inferences about other individuals’ intentions and goals by evaluating their actions in relation to the constraints imposed by the environment. This capacity enables humans to go beyond the surface appearance of behavior to draw inferences about an individual’s mental states. Presently unclear is whether this capacity is uniquely human or is shared with other animals. We show that cotton-top tamarins, rhesus macaques, and chimpanzees all make spontaneous inferences about a human experimenter’s goal by attending to the environmental constraints that guide rational action. These findings rule out simple associative accounts of action perception and show that our capacity to infer rational, goal-directed action likely arose at least as far back as the New World monkeys, some 40 million years ago.

- Replications:

Buttelmann, D., M. Carpenter, J. Call, and M. Tomasello. 2007. Enculturated Chimpanzees Imitate Rationally. Developmental Science 10: F31-F38.

Range, F., Z. Viranyi, and L. Huber. 2007. Selective Imitation in Domestic Dogs. Current Biology 17: 1-5.

Buttelmann, D., M. Carpenter, J. Call, and M. Tomasello. 2008. Rational Tool Use and Tool Choice in Human Infants and Great Apes. Child Development 79: 609-626.

Rochat, M., E. Serra, L. Fadiga, and V. Gallese. 2008. The Evolution of Social Cognition: Goal Familiarity Shapes Monkeys’ Action Understanding. Current Biology 18: 227-232.

Hauser, M.D., and J.N. Wood. 2011. Replication of ‘Rhesus Monkeys Correctly Read the Goal-Relevant Gestures of a Human Agent.’ Proceedings of the Royal Society B 278: 158-159.

Wood, J.N., and M.D. Hauser. 2011. Replication of ‘The Perception of Rational, Goal-Directed Action in Nonhuman Primates.’ Science 332: 537.

5. Object File Number Processing

- Original:

Hauser, M.D., S. Carey, and L.B. Hauser. 2000. Spontaneous Number Representation in Semi-Free-Ranging Rhesus Monkeys. Proceedings of the Royal Society 267: 829-833.

ABSTRACT Previous research has shown that animals possess considerable numerical abilities. However, this work was based on experiments involving extensive training, a small number of captive subjects and relatively artificial testing procedures. We present the results of experiments on over 200 semi-free-ranging rhesus monkeys using a task which involves no training and mimics a natural foraging problem. The subjects observed two experimenters place pieces of apple, one at a time, into each of two opaque containers. The experimenters then walked away so that the subjects could approach. The monkeys chose the container with the greater number of apple slices when the comparisons were one versus two, two versus three, three versus four and three versus five slices. They failed at four versus five, four versus six, four versus eight and three versus eight slices. Controls established that it was the representation of number which underlay their successful choices rather than the amount of time spent placing apple pieces into the box or the volume of apple placed in the box. The failures at values greater than three slices stand in striking contrast to other animal studies where training was involved and in which far superior numerical abilities were demonstrated. The range of success achieved by rhesus monkeys in this spontaneous number task matches the range achieved by human infants and corresponds to the range encoded in the syntax of natural languages.

- Replications:

Feigenson, L., S. Carey, and M.D. Hauser. 2002. The Representations Underlying Infants’ Choice of More: Object Files Versus Analog Magnitudes. Psychological Science 13: 150-156.

Uller C., R. Jaeger, G. Guidry, and C. Martin. 2003. Salamanders (Plethodon cinereus) Go for More: Rudiments of Number in a Species of Basal Vertebrate. Animal Cognition 6: 105-112.

Ward C., and B.B. Smuts. 2007. Quantity-Based Judgments in the Domestic Dog (Canis lupus familiaris). Animal Cognition 10: 71-80.

Agrillo C., M. Dadda, G. Serena, and A. Bisazza. 2008. Do Fish Count? Spontaneous Discrimination of Quantity in Female Mosquitofish. Animal Cognition 11: 495–503.

Barner, D., J.N. Wood, M.D. Hauser, and S. Carey. 2008. Evidence for a Non-Linguistic Distinction Between Singular and Plural Sets in Rhesus Monkeys. Cognition 107: 603-622.

Wood, J.N., M.D. Hauser, D. Glynn, and D. Barner. 2008. Free-Ranging Rhesus Monkeys Spontaneously Individuate and Enumerate Small Numbers of Non-Solid Portions. Cognition 106: 207-221.

Dadda, M., L. Piffer, C. Agrillo, and A. Bisazza, 2009. Spontaneous Number Representation in Mosquitofish. Cognition 112: 343-348.

Uller C., and J. Lewis. 2009. Horses (Equus caballus) Select the Greater of Two Quantities in Small Numerical Contrasts. Animal Cognition 12: 733-738.

Bisazza A., L. Piffer, G. Serena, and C. Agrillo. 2010. Ontogeny of Numerical Abilities in Fish. PLoS ONE 5(11): e15516. doi:10.1371/journal.pone.0015516

Gómez-Laplaza L.M., and R. Gerlai. 2011. Spontaneous Discrimination of Small Quantities: Shoaling Preferences in Angelfish (Pterophyllum scalare). Animal Cognition: doi:10.1007/s10071-011-0392-7

6. Tool Use

- Original:

Hauser, M.D. 1997. Artifactual Kinds and Functional Design Features: What a Primate Understands without Language. Cognition 64: 285-308.

ABSTRACT Of several domains of knowledge, humans appear to be born with an innately structured
representational system for making sense of objects, what properties individuate them, how they move in space, and what causes them to move from one location to another. They also appear to make simple conceptual cuts between artifactual kinds and living kinds. The basis for this distinction seems to be a combination of crucial functional properties, together with a teleological (i.e., historical/intentional) stance, one that asks ‘What was this object designed for?’. Although non-human primates also appear to have considerable understanding of objects, and often use objects as tools, it is not clear whether they draw a distinction between artifactual and living kinds, and if so, what factors guide this distinction. As a step in addressing this problem, I present experiments on a small New World monkey, the cotton-top tamarin (Saguinus oedipus), designed to reveal their understanding of the functional properties of tools using a procedure associated with minimal training. Specifically, the experiments explored whether tamarins distinguish between relevant and irrelevant properties of a tool, and further, understand that some features can be transformed with little cost to functionality. The first experiment was a means-end task and 4 involved using a cane-like object (a tool) to access a piece of food. In this experiment, there were always two choices: either the food was immediately accessible because it was located on the inside of the cane’s hook or less readily accessible because it was located on the outside of the hook. Most of the tamarins reached criterion on this task within a few sessions, consistently picking the cane with the most accessible food. Subsequent experiments (2-4) involved property changes (i.e., its color, texture, size and shape) that had either significant or relatively insignificant effects on the tool's function. In general, the tamarins appeared tolerant of all property transformations as evidenced by the fact that they selected each object at least once. However, clear preferences also emerged suggesting that some properties had a more significant impact on the tool’s functionality. Thus, in head-to-head competitions, tools with color or texture changes were selectively preferred over tools with shape or size changes. This makes sense color and texture do not effect the tool's function, whereas shape and size do. The final experiments involved both novel and familiar objects that, based on their current configuration, could readily be used as tools, in contrast with objects that required considerable manipulation to convert into a tool. Consistently, the tamarins preferred possible over convertible tools, and when two convertible tools were presented at the same time, they preferred the tool that required the fewest changes to the required motor response. Results suggest that the tamarins distinguish between relevant and irrelevant properties of a tool and this distinction is based on functionality, on having good design. This ability is especially surprising given the fact that tamarins do not naturally use tools, and infrequently come into contact with artifacts. Results are discussed in light of current theories concerning the representational foundations of natural kinds, and in particular, artifactual kinds.

- Replications:

Santos L.R., N. Mahajan, and J.L. Barnes. 2005. How Prosimian Primates Represent Tools: Experiments with Two Lemur Species (Eulemur fulvus and Lemur catta). Journal of Comparative Psychology 119: 394-403.

Spaulding B., and M.D. Hauser. 2005. What Experience is Required for Acquiring Tool Competence? Experiments with Two Callitrichids. Animal Behavior 70: 517-526.

Santos L.R., H.M. Pearson, G.M. Spaepen, F. Tsao, and M.D. Hauser. 2006. Probing the Limits of Tool Competence: Experiments with Two Non-Tool-Using Species (Cercopithecus aethiops and Saguinus oedipus). Animal Cognition 9: 94-109.

Okanoya K., N. Tokimoto, N. Kumazawa, S. Hihara, and A. Iriki. 2008. Tool-Use Training in a Species of Rodent: The Emergence of an Optimal Motor Strategy and Functional Understanding. PLoS ONE 26: e1860.

7. Folk Physics and the Looking Time, Expectancy Violation Method

Hauser’s lab was the first to apply the looking time, expectancy violation method—originally designed for work on human infants—to nonhuman animals. The replications apply the same method sometimes for the same content domain (e.g., number, folk physics) on a variety of different species.

- Originals:

- The first to apply the method: Hauser, M.D., P. MacNeilage, and M. Ware. 1996. Numerical Representations in Primates. Proceedings of the National Academy of Sciences 93: 1514-1517.

ABSTRACT Research has demonstrated that human infants and nonhuman primates have a rudimentary numerical system that enables them to count objects or events. More recently, however, studies using a preferential looking paradigm have suggested that preverbal human infants are capable of simple arithmetical operations, such as adding and subtracting a small number of visually presented objects. These findings implicate a relatively sophisticated representational system in the absence of language. To explore the evolutionary origins of this capacity, we present data from an experiment with wild rhesus monkeys (Macaca mulatta) that methodologically mirrors those conducted on human infants. Results suggest that rhesus monkeys detect additive and subtractive changes in the number of objects present in their visual field. Given the methodological and empirical similarities, it appears that nonhuman primates such as rhesus monkeys may also have access to arithmetical representations, although alternative explanations must be considered for both primate species.

- Hauser, M.D. 1998. Expectations About Object Motion and Destination: Experiments with a Nonhuman Primate. Developmental Science 1: 31-38. 5

ABSTRACT Human infants have considerable understanding of why objects move and what causes them to take one trajectory over another. Here, we explore the possibility that this capacity is shared with other nonhumans and present results from preferential looking time tests with a New World monkey, the cotton-top tamarin. Experiments examined whether individuals form different expectations about an object’s potential capacity to change locations. Test objects were: 1) self-propelled, moving, animate; 2) self-propelled, moving, inanimate; 3) non-self-propelled, moving due to an external agent, inanimate; 4) non-self-propelled, motionless, inanimate. When category 1 objects, either a live mouse or frog, emerged from behind an occluder in a novel location, this did not affect looking time; subjects appeared to expect such changes. In contrast, when the other objects emerged in a novel location following occlusion from view, subjects looked longer than when the object emerged in the location seen prior to occlusion; such locational changes were apparently not expected. Some feature other than self-propelled motion accounts for the tamarins’ looking time responses and at least one candidate feature is whether the object is animate or inanimate.

- Replications:

Santos, L.R., and M.D. Hauser, M.D. 1999. How Monkeys See the Eyes: Cotton-Top Tamarins’ Reaction to Changes in Visual Attention and Action. Animal Cognition 2: 131-139.

Munakata, Y., L. Santos, R. O’Reilly, M.D. Hauser, and E.S. Spelke. 2001. Visual Representation in the Wild: How Rhesus Monkeys Parse Objects. Journal of Cognitive Neuroscience 13: 44-58.

Uller, C., M.D. Hauser, and S. Carey. 2001. Spontaneous Representation of Number in Cotton-Top Tamarins. Journal of Comparative Psychology 115: 248-257.

Santos, L.R., and M.D. Hauser. 2002. A Nonhuman Primate’s Understanding of Solidity: Dissociations Between Seeing and Acting. Developmental Science 5: F1-F7.

Santos, L.R., G. Sulkowski, G.M. Spaepen, and M.D. Hauser. 2002. Object Individuation Using Property/Kind Information in Rhesus Macaques (Macaca mulatta). Cognition 83: 241-264.

Hauser, M.D., and S. Carey. 2003. Spontaneous Representations of Small Numbers of Objects by Rhesus Macaques: Examinations of Content and Format. Cognitive Psychology 47: 367-401.

Santos, L.R., C.T. Miller, and M.D. Hauser. 2003. Representing Tools: How Two Nonhuman Primate Species Distinguish Between the Functionally Relevant and Irrelevant Features of Tools. Animal Cognition 6: 269-281.

Cacchione, T., and H. Krist. 2004. Recognizing Impossible Object Relations: Intuitions About Support in Chimpanzees (Pan troglodytes). Journal of Comparative Psychology 118: 140-148.

Bird, C. D., and N.J. Emery. 2010. Rooks Perceive Support Relations Similar to Six-Month-Old Babies. Proceedings of the Royal Society B 277: 147-151.

Murai, C., M. Tanaka, and M. Sakagami. 2011. Physical Intuitions About Support Relations in Monkeys (Macaca fuscata) and Apes (Pan troglodytes). Journal of Comparative Psychology 125: 216-226.