Lisa A. Heimbauer

Responses to the Assurance game in monkeys, apes, and humans using equivalent procedures

There is great interest in the evolution of economic behavior. In typical studies, species are asked to play one of a series of economic games, derived from game theory, and their responses are compared. The advantage of this approach is the relative level of consistency and control that emerges from the games themselves; however, in the typical experiment, procedures and conditions differ widely, particularly between humans and other species. Thus, in the current study, we investigated how three primate species, capuchin monkeys, chimpanzees, and humans, played the Assurance (or Stag Hunt) game using procedures that were, to the best of our ability, the same across species, particularly with respect to training and pretesting. Our goal was to determine what, if any, differences existed in the ways in which these species made decisions in this game. We hypothesized differences along phylogenetic lines, which we found. However, the species were more similar than might be expected. In particular, humans who played using “nonhuman primate-friendly” rules did not behave as is typical. Thus, we find evidence for similarity in decision-making processes across the order Primates. These results indicate that such comparative studies are possible and, moreover, that in any comparison rating species’ relative abilities, extreme care must be taken in ensuring that one species does not have an advantage over the others due to methodological procedures.

Capuchin monkeys ( Cebus apella ) use positive, but not negative, auditory cues to infer food location

Nonhuman primates appear to capitalize more effectively on visual cues than corresponding auditory versions. For example, studies of inferential reasoning have shown that monkeys and apes readily respond to seeing that food is present (“positive” cuing) or absent (“negative” cuing). Performance is markedly less effective with auditory cues, with many subjects failing to use this input. Extending recent work, we tested eight captive tufted capuchins (Cebus apella) in locating food using positive and negative cues in visual and auditory domains. The monkeys chose between two opaque cups to receive food contained in one of them. Cup contents were either shown or shaken, providing location cues from both cups, positive cues only from the baited cup, or negative cues from the empty cup. As in previous work, subjects readily used both positive and negative visual cues to secure reward. However, auditory outcomes were both similar to and different from those of earlier studies. Specifically, all subjects came to exploit positive auditory cues, but none responded to negative versions. The animals were also clearly different in visual versus auditory performance. Results indicate that a significant proportion of capuchins may be able to use positive auditory cues, with experience and learning likely playing a critical role. These findings raise the possibility that experience may be significant in visually based performance in this task as well, and highlight that coming to grips with evident differences between visual versus auditory processing may be important for understanding primate cognition more generally.

A Serial Reaction Time (SRT) task with symmetrical joystick responding for nonhuman primates

The serial reaction time (SRT) task is a simple procedure in which participants produce differentiated responses to each of a series of stimuli presented at varying locations. Learning about stimulus order is revealed through decreased latencies for structured versus randomized sequences. Although widely used with humans and well suited to nonhumans, this paradigm is little used in comparative research. In the present article, we describe an SRT procedure that uses colored circles as stimuli, a circular layout of locations, and symmetrical joystick deflections as responses. In two experiments, we showed that four rhesus macaques (Macaca mulatta) learned to track sequences up to eight items long, with three animals showing faster responding to repeating sequences than to randomized versions. After extended training, these participants also showed evidence of faster responding at all positions within repeating sequences. This method minimizes response effort, equates effort and travel distance across stimulus locations, and is applicable to any joystick-capable species.

Visual artificial grammar learning by rhesus macaques ( Macaca mulatta ): exploring the role of grammar complexity and sequence length

Humans and nonhuman primates can learn about the organization of stimuli in the environment using implicit sequential pattern learning capabilities. However, most previous artificial grammar learning studies with nonhuman primates have involved relatively simple grammars and short input sequences. The goal in the current experiments was to assess the learning capabilities of monkeys on an artificial grammar-learning task that was more complex than most others previously used with nonhumans. Three experiments were conducted using a joystick-based, symmetrical-response serial reaction time task in which two monkeys were exposed to grammar-generated sequences at sequence lengths of four in Experiment 1, six in Experiment 2, and eight in Experiment 3. Over time, the monkeys came to respond faster to the sequences generated from the artificial grammar compared to random versions. In a subsequent generalization phase, subjects generalized their knowledge to novel sequences, responding significantly faster to novel instances of sequences produced using the familiar grammar compared to those constructed using an unfamiliar grammar. These results reveal that rhesus monkeys can learn and generalize the statistical structure inherent in an artificial grammar that is as complex as some used with humans, for sequences up to eight items long. These findings are discussed in relation to whether or not rhesus macaques and other primate species possess implicit sequence learning abilities that are similar to those that humans draw upon to learn natural language grammar.

Evidence for cognitive restoration of time-reversed speech by a language-trained chimpanzee (Pan troglodytes)

Previously, we reported on the ability of Panzee, a language-trained chimpanzee, to identify sine-wave and noise-vocoded speech by attending to the amplitude and frequency modulations in the altered signals. Here, we report on her ability to perceive phoneme-length information in words reproduced in time-reversed form. While this manipulation preserves the amplitude of frequency components, it reverses the pattern of energy changes within each reversal window. Listeners easily recognize speech at reversal windows up to 100-ms length, but at longer reversal lengths unintelligibility begins to occur (Saberi and Perrott, 1999). The theoretical interpretation is that individual phonetic segments range from 50 to 100 ms (Crystal and House, 1988), and reversal-windows less than 100 ms provide for restoration of phoneme perception. Hypothesizing that Panzee also perceives speech based on phonemic segments, we tested her and humans with words in eight reversal forms ranging from 25 to 200 ms. Results revealed tim...

A chimpanzee responds best to sine-wave speech with formant tones 1 and 2 present

A seminal study by Remez and colleagues [R. E. Remez, et al., Science, 212, 947–949 (1981)] demonstrated that listeners were more successful in identifying sine-wave speech when the first two (T12) or all three formant tones (T123) were present than when either were absent (forms T13 and T23). To determine whether a language-trained chimpanzee (Panzee) with the ability to recognize English words in sine-wave form [L. A. Heimbauer, et al., Curr. Biol., doi:10.1016/j.cub.2011.06.007 (2011)] would respond similarly, she and 13 humans were tested with words synthesized in the four forms used by Remez et al. Indeed, for each species, perception of speech was significantly better when the first and second tones were both present. Panzees performance suggests that she is attending to the same spectro-temporal features of sine-wave speech that are critical to humans. The outcomes further indicate that basic capabilities involved in speech perception could have been present in latent form in the common ancestor o...

A chimpanzee (Pan troglodytes) recognizes spoken words synthesized as sine‐wave speech.

The human ability to understand speech in the absence of traditional acoustic cues to phonetic content has been argued to be evidence of specialized processing. To determine whether this capability is unique to humans, perception of sine‐wave speech was examined in a 23‐year‐old, language‐trained chimpanzee named Panzee. This animal was reared from infancy by human caregivers in a speech‐rich environment and identifies more than 125 spoken words using graphical symbols (lexigrams). Test trials presented one of 48 familiar words via computer in either natural or sine‐wave form, with Panzee choosing a corresponding lexigram from among four alternatives. Her performance on sine‐wave words was well above chance levels, in spite of receiving no reward or any other feedback when responding to these sounds. The chimpanzee also showed above‐chance accuracy on trials that cumulatively represented the first instances of hearing words in sine‐wave form. While she was less accurate with sine‐wave words than with natural versions, human listeners hearing the same stimuli were less accurate as well. Panzee’s performance indicates that experience with spoken language and general auditory‐processing mechanisms alone can be sufficient for perceiving even highly impoverished synthetic speech.

Perception of voiced‐only and noise‐vocoded speech by a language‐trained chimpanzee (Pan troglodytes).

The ability of human listeners to understand speech even in altered or synthetic forms is argued to be evidence of uniquely human processing abilities. However, extensive early experience with speech may also contribute to this capability. To investigate this issue two experiments were designed to test the ability of Panzee, a 22‐year‐old language‐trained chimpanzee, to recognize words in synthetic form. Like a human child, she was reared from infancy by human caregivers who routinely spoke to her. She communicates with humans by identifying words using graphical symbols (lexigrams). Experimental training and testing were conducted with two different sets of 24 familiar words presented one‐per‐trial in natural, voiced‐only, or noise‐vocoded forms, with Panzee choosing one of four lexigrams presented on a computer monitor. Experiment 1 showed equivalent performance with words heard in natural form versus voiced‐only versions, resynthesized from only voiced components of a word. Noise‐vocoded words presente...

Transmission fidelity in rhesus monkey (Macaca mulatta) “coos” and “screams”.

In animal communication, studies of environmental acoustics examine issues such as habitat‐specific propagation effects on vocalizations and likely impact on psychologically significant aspects (e.g., localizability and identifiability). The current work compared transmission fidelity in harmonically structured “coos” versus noisy “screams” produced by female rhesus monkeys (Macaca mulatta). Calls were broadcast in a temperate, mixed forest using a loudspeaker (Genelec 1029A) positioned either 0.5 m or 1.0 m above the ground, and re‐recorded using two microphones (Sennheiser MKH106T) and a digital audio deck (TAS‐CAM DA‐P1). The “near” microphone remained at a constant distance of 2.5 m from the loudspeaker, while the “far” microphone was positioned at 10, 20, 30, 40, or 50 m. Eight different coos and eight different screams were played four times each at every distance, with cross‐correlation values calculated for each pair of near‐ and far‐microphone recordings. Results included that correlations decrea...

Speech perception in a language‐trained chimpanzee (Pan troglodytes).

After decades of research, the question of whether humans perceive spoken language using a specialized “speech mode” remains unresolved. Studies in nonhumans suggest that animals perceive phonemic contrasts much as humans do, but involve subjects trained for thousands of trials on single discriminations. This work reports initial speech perception results from Panzee, a chimpanzee (Pan troglodytes) reared by humans speaking to her as they would to a child and also training her to use graphical wordlike “lexigrams.” Panzee comprehends approximately 126 spoken words, documented through a procedure in which a digitally presented spoken word is matched to one of four lexigrams presented on a monitor. First experiments have compared performance with natural digitized versions of 24 spoken words to synthetic LPC‐based replicas and to whispered versions. Using a different subset of eight test words within each of three 96‐trial sessions showed comparable mean performance for natural (83.3%), synthesized (82.5%),...