Dual systems for all: Higher-order, role-based relational reasoning as a uniquely derived feature of human cognition.

Hoerl and McCormack demonstrate that although animals possess a sophisticated temporal updating system, there is no evidence that they also possess a temporal reasoning system. This important case study is directly related to the broader claim that although animals are manifestly capable of first-order (perceptually-based) relational reasoning, they lack the capacity for higher-order, role-based relational reasoning. We argue this distinction applies to all domains of cognition.

Meta-analytic techniques reveal that corvid causal reasoning in the Aesop's Fable paradigm is driven by trial-and-error learning.

The classic Aesop's fable, Crow and the Pitcher, has inspired a major line of research in comparative cognition. Over the past several years, five articles (over 32 experiments) have examined the ability of corvids (e.g., rooks, crows, and jays) to complete lab-based analogs of this fable, by requiring them to drop stones and other objects into tubes of water to retrieve a floating worm (Bird and Emery in Curr Biol 19:1-5, 2009b; Cheke et al. in Anim Cogn 14:441-455, 2011; Jelbert et al. in PLoS One 3:e92895, 2014; Logan et al. in PLoS One 7:e103049, 2014; Taylor et al. in Gray R D 12:e26887, 2011). These researchers have stressed the unique potential of this paradigm for understanding causal reasoning in corvids. Ghirlanda and Lind (Anim Behav 123:239-247, 2017) re-evaluated trial-level data from these studies and concluded that initial preferences for functional objects, combined with trial-and-error learning, may account for subjects' performance on key variants of the paradigm. In the present paper, we use meta-analytic techniques to provide more precise information about the rate and mode of learning that occurs within and across tasks. Within tasks, subjects learned from successful (but not unsuccessful) actions, indicating that higher-order reasoning about phenomena such as mass, volume, and displacement is unlikely to be involved. Furthermore, subjects did not transfer information learned in one task to subsequent tasks, suggesting that corvids do not engage with these tasks as variants of the same problem (i.e., how to generate water displacement to retrieve a floating worm). Our methodological analysis and empirical findings raise the question: Can Aesop's fable studies distinguish between trial-and-error learning and/or higher-order causal reasoning? We conclude they cannot.

The relationship between joint attention and theory of mind in neurotypical adults.

Joint attention (JA) is hypothesized to have a close relationship with developing theory of mind (ToM) capabilities. We tested the co-occurrence of ToM and JA in social interactions between adults with no reported history of psychiatric illness or neurodevelopmental disorders. Participants engaged in an experimental task that encouraged nonverbal communication, including JA, and also ToM activity. We adapted an in-lab variant of experience sampling methods (Bryant et al., 2013) to measure ToM during JA based on participants' subjective reports of their thoughts while performing the task. This experiment successfully elicited instances of JA in 17/20 dyads. We compared participants' thought contents during episodes of JA and non-JA. Our results suggest that, in adults, JA and ToM may occur independently.

Constraints on the exploitation of the functional properties of objects in expert tool-using chimpanzees (Pan troglodytes).

Many species exploit immediately apparent dimensions of objects during tool use and manufacture and operate over internal perceptual representations of objects (they move and reorient objects in space, have rules of operation to deform or modify objects, etc). Humans, however, actively test for functionally relevant object properties before such operations begin, even when no previous percepts of a particular object's qualities in the domain have been established. We hypothesize that such prospective diagnostic interventions are a human specialization of cognitive function that has been entirely overlooked in the neuropsychological literature. We presented chimpanzees with visually identical rakes: one was functional for retrieving a food reward; the other was non-functional (its base was spring-loaded). Initially, they learned that only the functional tool could retrieve a distant reward. In test 1, we explored if they would manually test for the rakes' rigidity during tool selection, but before using it. We found no evidence of such behavior. In test 2, we obliged the apes to deform the non-functional tool's base before using it, in order to evaluate whether this would cause them to switch rakes. It did not. Tests 3-6 attempted to focus the apes' attention on the functionally relevant property (rigidity). Although one ape eventually learned to abandon the non-functional rake before using it, she still did not attempt to test the rakes for rigidity prior to use. While these results underscore the ability of chimpanzees to use novel tools, at the same time they point toward a fundamental (and heretofore unexplored) difference in causal reasoning between humans and apes. We propose that this behavioral difference reflects a human specialization in how object properties are represented, which could have contributed significantly to the evolution of our technological culture. We discuss developing a new line of evolutionarily motivated neuropsychological research on action disorders.

Brief Report: Theory of Mind, Relational Reasoning, and Social Responsiveness in Children With and Without Autism: Demonstration of Feasibility for a Larger-Scale Study.

Understanding the underpinnings of social responsiveness and theory of mind (ToM) will enhance our knowledge of autism spectrum disorder (ASD). We hypothesize that higher-order relational reasoning (higher-order RR: reasoning necessitating integration of relationships among multiple variables) is necessary but not sufficient for ToM, and that social responsiveness varies independently of higher-order RR. A pilot experiment tested these hypotheses in n = 17 children, 3-14, with and without ASD. No child failing 2nd-order RR passed a false belief ToM test. Contrary to prediction, Social Responsiveness Scale scores did correlate with 2nd-order RR performance, likely due to sample characteristics. It is feasible to translate this comparative cognition-inspired line of inquiry for full-scale studies of ToM, higher-order RR, and social responsiveness in ASD.

Brief Report: Chimpanzee Social Responsiveness Scale (CSRS) Detects Individual Variation in Social Responsiveness for Captive Chimpanzees.

Comparative studies of social responsiveness, a core impairment in autism spectrum disorder (ASD), will enhance our understanding of typical and atypical social behavior. We previously reported a quantitative, cross-species (human-chimpanzee) social responsiveness measure, which included the development of the Chimpanzee Social Responsiveness Scale (CSRS). Here, we augment our prior CSRS sample with 25 zoo chimpanzees at three sites: combined N = 54. The CSRS demonstrated strong interrater reliability, and low-ranked chimpanzees, on average, displayed higher CSRS scores. The CSRS continues to discriminate variation in chimpanzee social responsiveness, and the association of higher scores with lower chimpanzee social standing has implications for the relationship between autistic traits and human social status. Continued comparative investigations of social responsiveness will enhance our understanding of underlying impairments in ASD, improve early diagnosis, and inform future therapies.

Theory of Mind experience sampling in typical adults.

We explored the frequency with which typical adults make Theory of Mind (ToM) attributions, and under what circumstances these attributions occur. We used an experience sampling method to query 30 typical adults about their everyday thoughts. Participants carried a Personal Data Assistant (PDA) that prompted them to categorize their thoughts as Action, Mental State, or Miscellaneous at approximately 30 pseudo-random times during a continuous 10-h period. Additionally, participants noted the direction of their thought (self versus other) and degree of socializing (with people versus alone) at the time of inquiry. We were interested in the relative frequency of ToM (mental state attributions) and how prominent they were in immediate social exchanges. Analyses of multiple choice answers suggest that typical adults: (1) spend more time thinking about actions than mental states and miscellaneous things, (2) exhibit a higher degree of own- versus other-directed thought when alone, and (3) make mental state attributions more frequently when not interacting (offline) than while interacting with others (online). A significant 3-way interaction between thought type, direction of thought, and socializing emerged because action but not mental state thoughts about others occurred more frequently when participants were interacting with people versus when alone; whereas there was an increase in the frequency of both action and mental state attributions about the self when participants were alone as opposed to socializing. A secondary analysis of coded free text responses supports findings 1-3. The results of this study help to create a more naturalistic picture of ToM use in everyday life and the method shows promise for future study of typical and atypical thought processes.

Impaired eye region search accuracy in children with autistic spectrum disorders.

To explore mechanisms underlying reduced fixation of eyes in autism, children with autistic spectrum disorders (ASD) and typically developing children were tested in five visual search experiments: simple color feature; color-shape conjunction; face in non-face objects; mouth region; and eye region. No group differences were found for reaction time profile shapes in any of the five experiments, suggesting intact basic search mechanics in children with ASD. Contrary to early reports in the literature, but consistent with other more recent findings, we observed no superiority for conjunction search in children with ASD. Importantly, children with ASD did show reduced accuracy for eye region search (p = .005), suggesting that eyes contribute less to high-level face representations in ASD or that there is an eye region-specific disruption to attentional processes engaged by search in ASD.

So, are we the massively lucky species?

We are in vehement agreement with most of Vaesen's key claims. But Vaesen fails to consider or rebut the possibility that there are deep causal dependencies among the various cognitive traits he identifies as uniquely human. We argue that "higher-order relational reasoning" is one such linchpin trait in the evolution of human tool use, social intelligence, language, and culture.

Comparative investigations of manual action representations: evidence that chimpanzees represent the costs of potential future actions involving tools.

The ability to adjust one's ongoing actions in the anticipation of forthcoming task demands is considered as strong evidence for the existence of internal action representations. Studies of action selection in tool use reveal that the behaviours that we choose in the present moment differ depending on what we intend to do next. Further, they point to a specialized role for mechanisms within the human cerebellum and dominant left cerebral hemisphere in representing the likely sensory costs of intended future actions. Recently, the question of whether similar mechanisms exist in other primates has received growing, but still limited, attention. Here, we present data that bear on this issue from a species that is a natural user of tools, our nearest living relative, the chimpanzee. In experiment 1, a subset of chimpanzees showed a non-significant tendency for their grip preferences to be affected by anticipation of the demands associated with bringing a tool's baited end to their mouths. In experiment 2, chimpanzees' initial grip preferences were consistently affected by anticipation of the forthcoming movements in a task that involves using a tool to extract a food reward. The partial discrepancy between the results of these two studies is attributed to the ability to accurately represent differences between the motor costs associated with executing the two response alternatives available within each task. These findings suggest that chimpanzees are capable of accurately representing the costs of intended future actions, and using those predictions to select movements in the present even in the context of externally directed tool use.

Initial description of a quantitative, cross-species (chimpanzee-human) social responsiveness measure.

OBJECTIVE: Comparative studies of social responsiveness, an ability that is impaired in autism spectrum disorders, can inform our understanding of both autism and the cognitive architecture of social behavior. Because there is no existing quantitative measure of social responsiveness in chimpanzees, we generated a quantitative, cross-species (human-chimpanzee) social responsiveness measure. METHOD: We translated the Social Responsiveness Scale (SRS), an instrument that quantifies human social responsiveness, into an analogous instrument for chimpanzees. We then retranslated this "Chimpanzee SRS" into a human "Cross-Species SRS" (XSRS). We evaluated three groups of chimpanzees (n = 29) with the Chimpanzee SRS and typical and human children with autism spectrum disorder (ASD; n = 20) with the XSRS. RESULTS: The Chimpanzee SRS demonstrated strong interrater reliability at the three sites (ranges for individual ICCs: 0.534 to 0.866; mean ICCs: 0.851 to 0.970). As has been observed in human beings, exploratory principal components analysis of Chimpanzee SRS scores supports a single factor underlying chimpanzee social responsiveness. Human subjects' XSRS scores were fully concordant with their SRS scores (r = 0.976, p = .001) and distinguished appropriately between typical and ASD subjects. One chimpanzee known for inappropriate social behavior displayed a significantly higher score than all other chimpanzees at its site, demonstrating the scale's ability to detect impaired social responsiveness in chimpanzees. CONCLUSION: Our initial cross-species social responsiveness scale proved reliable and discriminated differences in social responsiveness across (in a relative sense) and within (in a more objectively quantifiable manner) human beings and chimpanzees.

Carryover effect of joint attention to repeated events in chimpanzees and young children.

Gaze following is a fundamental component of triadic social interaction which includes events and an object shared with other individuals and is found in both human and nonhuman primates. Most previous work has focused only on the immediate reaction after following another's gaze. In contrast, this study investigated whether gaze following is retained after the observation of the other's gaze shift, whether this retainment differs between species and age groups, and whether the retainment depends on the nature of the preceding events. In the social condition, subjects (1- and 2-year-old human children and chimpanzees) witnessed an experimenter who looked and pointed in the direction of a target lamp. In the physical condition, the target lamp blinked but the experimenter did not provide any cues. After a brief delay, we presented the same stimulus again without any cues. All subjects looked again to the target location after experiencing the social condition and thus showed a carryover effect. However, only 2-year-olds showed a carryover effect in the physical condition; 1-year-olds and chimpanzees did not. Additionally, only human children showed spontaneous interactive actions such as pointing. Our results suggest that the difference between the two age groups and chimpanzees is conceptual and not only quantitative.

Chimpanzees' context-dependent tool use provides evidence for separable representations of hand and tool even during active use within peripersonal space.

Considerable attention has been devoted to behaviors in which tools are used to perform actions in extrapersonal space by extending the reach. Evidence suggests that these behaviors result in an expansion of the body schema and peripersonal space. However, humans often use tools to perform tasks within peripersonal space that cannot be accomplished with the hands. In some of these instances (e.g., cooking), a tool is used as a substitute for the hand in order to pursue actions that would otherwise be hazardous. These behaviors suggest that even during the active use of tools, we maintain non-isomorphic representations that distinguish between our hands and handheld tools. Understanding whether such representations are a human specialization is of potentially great relevance to understand the evolutionary history of technological behaviors including the controlled use of fire. We tested six captive adult chimpanzees to determine whether they would elect to use a tool, rather than their hands, when acting in potentially hazardous vs. nonhazardous circumstances located within reach. Their behavior suggests that, like humans, chimpanzees represent the distinction between the hand vs. tool even during active use. We discuss the implications of this evidence for our understanding of tool use and its evolution.

Darwin's mistake: explaining the discontinuity between human and nonhuman minds.

Over the last quarter century, the dominant tendency in comparative cognitive psychology has been to emphasize the similarities between human and nonhuman minds and to downplay the differences as "one of degree and not of kind" (Darwin 1871). In the present target article, we argue that Darwin was mistaken: the profound biological continuity between human and nonhuman animals masks an equally profound discontinuity between human and nonhuman minds. To wit, there is a significant discontinuity in the degree to which human and nonhuman animals are able to approximate the higher-order, systematic, relational capabilities of a physical symbol system (PSS) (Newell 1980). We show that this symbolic-relational discontinuity pervades nearly every domain of cognition and runs much deeper than even the spectacular scaffolding provided by language or culture alone can explain. We propose a representational-level specification as to where human and nonhuman animals' abilities to approximate a PSS are similar and where they differ. We conclude by suggesting that recent symbolic-connectionist models of cognition shed new light on the mechanisms that underlie the gap between human and nonhuman minds.

Chimpanzees do not take advantage of very low cost opportunities to deliver food to unrelated group members.

We conducted experiments on two populations of chimpanzees, Pan troglodytes, to determine whether they would take advantage of opportunities to provide food rewards to familiar group members at little cost to themselves. In both of the experiments described here, chimpanzees were able to deliver identical rewards to themselves and to other members of their social groups. We compared the chimpanzees' behaviour when they were paired with another chimpanzee and when they were alone. If chimpanzees are motivated to provide benefits to others, they are expected to consistently deliver rewards to others and to distinguish between the partner-present and partner-absent conditions. Results from both experiments indicate that our subjects were largely indifferent to the benefits they could provide to others. They were less likely to provide rewards to potential recipients as the experiment progressed, and all but one of the 18 subjects were as likely to deliver rewards to an empty enclosure as to an enclosure housing another chimpanzee. These results, in conjunction with similar results obtained in previous experiments, suggest that chimpanzees are not motivated by prosocial sentiments to provide food rewards to other group members.

On the lack of evidence that non-human animals possess anything remotely resembling a 'theory of mind'.

After decades of effort by some of our brightest human and non-human minds, there is still little consensus on whether or not non-human animals understand anything about the unobservable mental states of other animals or even what it would mean for a non-verbal animal to understand the concept of a 'mental state'. In the present paper, we confront four related and contentious questions head-on: (i) What exactly would it mean for a non-verbal organism to have an 'understanding' or a 'representation' of another animal's mental state? (ii) What should (and should not) count as compelling empirical evidence that a non-verbal cognitive agent has a system for understanding or forming representations about mental states in a functionally adaptive manner? (iii) Why have the kind of experimental protocols that are currently in vogue failed to produce compelling evidence that non-human animals possess anything even remotely resembling a theory of mind? (iv) What kind of experiments could, at least in principle, provide compelling evidence for such a system in a non-verbal organism?

Causal cognition in human and nonhuman animals: a comparative, critical review.

In this article, we review some of the most provocative experimental results to have emerged from comparative labs in the past few years, starting with research focusing on contingency learning and finishing with experiments exploring nonhuman animals' understanding of causal-logical relations. Although the theoretical explanation for these results is often inchoate, a clear pattern nevertheless emerges. The comparative evidence does not fit comfortably into either the traditional associationist or inferential alternatives that have dominated comparative debate for many decades now. Indeed, the similarities and differences between human and nonhuman causal cognition seem to be much more multifarious than these dichotomous alternatives allow.

Differences in How 12- and 24-Month-Olds Interpret the Gaze of Adults.

This study examined the hypothesis that toddlers interpret an adult's head turn as evidence that the adult was looking at something, whereas younger infants interpret gaze based on an expectancy that an interesting object will be present on the side to which the adult has turned. Infants of 12 months and toddlers of 24 months were first shown that an adult head turn to the side predicted the activation of a remote-controlled toy on that side of the room. After this connection had been demonstrated, participants were assigned to 2 conditions. In the head turn condition the toys were removed but the adult continued to produce head turns to the side. In the toy condition the adult stopped turning but the toys continued to be activated when the participant turned toward them. Results showed that, compared to 12-month-olds, 24-month-olds were more likely to continue to turn to the side when the adult continued to turn even though there was no longer anything of interest to see. In contrast, compared to 24-month-olds, 12-month-olds were, if anything, more likely to continue to turn to the side in the condition in which the adult stopped turning. The latter result was replicated in a condition in which the activation of the toy was not contingent on the child's own head turn. These results imply that the meaning of gaze following may change significantly over the 2nd year of life. For 12-month-olds, gaze is a useful predictor of where interesting sights may occur. In contrast, for 24-month-olds, gaze may be a signal that the adult is looking at something.

Chimpanzees are indifferent to the welfare of unrelated group members.

Humans are an unusually prosocial species-we vote, give blood, recycle, give tithes and punish violators of social norms. Experimental evidence indicates that people willingly incur costs to help strangers in anonymous one-shot interactions, and that altruistic behaviour is motivated, at least in part, by empathy and concern for the welfare of others (hereafter referred to as other-regarding preferences). In contrast, cooperative behaviour in non-human primates is mainly limited to kin and reciprocating partners, and is virtually never extended to unfamiliar individuals. Here we present experimental tests of the existence of other-regarding preferences in non-human primates, and show that chimpanzees (Pan troglodytes) do not take advantage of opportunities to deliver benefits to familiar individuals at no material cost to themselves, suggesting that chimpanzee behaviour is not motivated by other-regarding preferences. Chimpanzees are among the primates most likely to demonstrate prosocial behaviours. They participate in a variety of collective activities, including territorial patrols, coalitionary aggression, cooperative hunting, food sharing and joint mate guarding. Consolation of victims of aggression and anecdotal accounts of solicitous treatment of injured individuals suggest that chimpanzees may feel empathy. Chimpanzees sometimes reject exchanges in which they receive less valuable rewards than others, which may be one element of a 'sense of fairness', but there is no evidence that they are averse to interactions in which they benefit more than others.