A Review : Psychophysiology of Tool Use in Non-Human Primates

Behavioral and Brain Sciences, 2012

The cortical representation of concepts varies according to the information critical for their development. Living categories, being mainly based upon visual information, are bilaterally represented in the rostral parts of the ventral stream of visual processing; whereas tools, being mainly based upon action data, are unilaterally represented in a left-sided fronto-parietal network. The unilateral representation of tools results from involvement in actions of the right side of the body.

2014

Tool use requires the manipulation of an object in the environment to achieve a goal, and the ability to relate one object to another. In the present experiments, I investigated tool use acquisition, and the relationship between tool use and self-control, in lion-tailed macaques (Macaca silenus). First, I examined three lion-tailed macaques' abilities to manipulate a tool by presenting a rake-shaped tool resting on a platform, with a food reward placed outside of the rake head. This experiment measured the monkeys' abilities to manipulate a rake-shaped tool, and investigated how the monkeys learned the tool-using skill. Two monkeys learned to successfully manipulate the tool to obtain the reward, while the other did not. In the second experiment, I investigated tool use in relation to self-control, by presenting a modified token-exchange task. In a trial, I presented one monkey that successfully learned to use the tool with a choice between a medium-value reward, and a rake tool that could be used to obtain a higher-value reward. If the monkey chose the tool over the food, I pushed a platform with a high-value food resting on it up to the caging that could be retrieved using the tool. The monkey began choosing the tool over the apple piece significantly more often than chance in his seventh 20-trial session. My results indicated that this monkey was capable of self-control using this novel design, as he chose the tool to retrieve the high-value reward over the lowvalue reward, even when there was a delay of up to 10 s between choosing the tool and retrieving the reward. This study was one of the first that investigated tool use acquisition and response inhibition in lion-tailed macaques. Performance of the two successful liontailed macaques on the tool acquisition task may reflect phylogenetic differences, in that vii they performed similar to another Old World monkey species (Macaca fuscata), but outperformed marmosets (Callithrix jacchus), a New World monkey species. Their capacity for self-control on this task was similar to that seen in both Old and New World monkey species.

Brain, 2009

Misuse of tools and objects by patients with left brain damage is generally recognized as a manifestation of apraxia, caused by parietal lobe damage. The use of tools and objects can, however, be subdivided in several components. The purpose of our study was to find out which of these are dependent on parietal lobe function. Thirty-eight patients with left brain damage and aphasia were examined using tests to assess the retrieval of functional knowledge from semantic memory (Functional Associations), mechanical problem solving (Novel Tools) and use of everyday tools and objects (Common Tools). Voxel-wise analysis of magnetic resonance images revealed two regions where lesions had a significant impact on the test results. One extended rostrally from the central region and ventrally through the middle frontal cortex to the dorsal margin of the inferior frontal gyrus. The other reached dorsally and caudally from the supramarginal gyrus, through the inferior, to superior parietal lobe. Whereas the frontal lesions had an adverse influence on all experimental tests as well as on the subtests of the Aachen Aphasia test, parietal lesions impaired Novel and Common Tools, but did not have an adverse effect on the Functional Associates. An association between Functional Associations and temporal lesions became apparent when patients with only a selective deficit in the test were considered, but did not show up in the whole group analysis. The parietal influence was as strong for the selection as for the use of either novel or common tools, although choice of appropriate manual configuration and movements was more important for use than for selection. We conclude that the contribution of the parietal lobe to tool use concerns general principles of tool use rather than knowledge about the prototypical use of common tools and objects, and the comprehension of mechanical interactions of the tool with other tools, recipients or material rather than the selection of grip formation and manual movements.

Behavioral and Brain Sciences, 1989

Spontaneous tool use and sensorimotor intelligence in Cebus were observed to determine whether tool use is discovered fortuitously and learned by trial-and-error or, rather, whether advanced sensorimotor abilities (experimentation and insight) are critical in its ontogeny and evolution. During 62 hours of observing three captive groups of cebus monkeys, totaling 12 animals, 38 series and 66 acts of spontaneous tool use were recorded. Nine monkeys (75%) used tools; 14 different kinds of tool use were observed. Of seven captive spider monkeys observed for 21 hours, none used tools. Comparative observations of sensorimotor intelligence were made using Piaget's model. The sensorimotor basis of tool use by the Cebus was also analyzed. Cebus monkeys showed all six levels of sensorimotor intelligence, whereas the spider monkeys showed only the first four stages. Besides these correlations between tool use and advanced sensorimotor ability, 37 of the 38 tool-use series and 65 of 66 individual acts involved Stage 5 and 6 sensorimotor mechanisms (i.e., tertiary circular reactions and insight); only one series involved Stage 3 fortuitous discovery and Stage 4 coordinations. This study and a literature survey suggest that strong tool-using propensity among primates is based on advanced sensorimotor ability rather than fortuitous discovery.

PLoS ONE, 2012

Sequential tool use is defined as using a tool to obtain another non-food object which subsequently itself will serve as a tool to act upon a further (sub)goal. Previous studies have shown that birds and great apes succeed in such tasks. However, the inclusion of a training phase for each of the sequential steps and the low cost associated with retrieving the longest tools limits the scope of the conclusions. The goal of the experiments presented here was, first to replicate a previous study on sequential tool use conducted on New Caledonian crows and, second, extend this work by increasing the cost of retrieving a tool in order to test tool selectivity of apes. In Experiment 1, we presented chimpanzees, orangutans and bonobos with an out-of-reach reward, two tools that were available but too short to reach the food and four out-of-reach tools differing in functionality. Similar to crows, apes spontaneously used up to 3 tools in sequence to get the reward and also showed a strong preference for the longest out-of reach tool independently of the distance of the food. In Experiment 2, we increased the cost of reaching for the longest out-of reach tool. Now apes used up to 5 tools in sequence to get the reward and became more selective in their choice of the longest tool as the costs of its retrieval increased. The findings of the studies presented here contribute to the growing body of comparative research on tool use.

Animal Cognition, 2012

We examined whether eight capuchins and eight chimpanzees were able to retrieve a reward placed inside a tube, of varying length, by selecting the correct stick from different sets of three sticks differing in length (functional feature) and handle (non-functional feature). Moreover, to investigate whether seeing the stick inside the tube (visual feedback) improves performance, half of the subjects were tested with a transparent apparatus and the other half with an opaque apparatus. Phase 1 included (a) Training 1 in which each stick had a different handle and (b) Transfer 1 in which the handles were switched among sticks, so that the functional tool had the same length but a different handle than before. The seven chimpanzees and one capuchin that passed Transfer 1 received Transfer 2. The other subjects received (a) Training 2, which used the same sticks from Phase 1 with handles switched in every trial, and (b) Transfer 2 in which the tube was longer, all sticks had the same new handle, and the formerly longest tool became intermediate in length. Eight chimpanzees and three capuchins passed Transfer 2. Results showed that (1) chimpanzees applied relational structures in tool using tasks more quickly than capuchins and (2) capuchins required more varied experience to attend to the functional feature of the tool. Interestingly, visual feedback did not improve performance in either species.

Le développement d'un comportement orienté vers des objets est comparé chez trois groupes de primates: singes capucins, chimpanzées ei humains, èn se référant s.pé^cialement au rôle du contexte-social dans lhcquisition de I'empioi d,outils. une différence importante entre des primates humains ét non humainr .it l" àegre auquet les objets en talt que tels deviénnent un centre des interactions sociales] de teiles interactions par la médiation d'objets sont une particularité d'humains. Chei ceux-ci le développement^ d'outils chez lés enfants --par exemple, comment uiili*". un" :Sl:t:._ e,1 ragitite par l'intervention d'adûrtes entrâînés, er probabrement par I rmrtatlon. Jusqu'lcl aucune preuve n'existe témoignant de la présènce de I'un ou de I'autre de ces mécanismes de -technique socia--le chez leô capucins, mais les chim-panzées, notament ceux qui habitent-un milieu riche et complêxe, sémblent être capables de tels actes. Les influences sociales sur I'acquisition ae I'utilisation d'outils sont étroitement apparentées aux capacités mentales (ihéories cognitives), et encore une tois la littérature parle d'une progression : singes capucini-chimpanzées_ humains. Manipulatiol d'obje_t, utilisation d'outils, développement, modélisation sociale, primate non humain, homme.

eLife, 2013

Sophisticated tool use is a defining characteristic of the primate species but how is it supported by the brain, particularly the human brain? Here we show, using functional MRI and pattern classification methods, that tool use is subserved by multiple distributed action-centred neural representations that are both shared with and distinct from those of the hand. In areas of frontoparietal cortex we found a common representation for planned hand-and tool-related actions. In contrast, in parietal and occipitotemporal regions implicated in hand actions and body perception we found that coding remained selectively linked to upcoming actions of the hand whereas in parietal and occipitotemporal regions implicated in tool-related processing the coding remained selectively linked to upcoming actions of the tool. The highly specialized and hierarchical nature of this coding suggests that hand-and tool-related actions are represented separately at earlier levels of sensorimotor processing before becoming integrated in frontoparietal cortex.

Journal of Experimental Psychology: Animal Learning and Cognition, 2014

Nonhuman primates perform poorly in trap tasks, a benchmark test of causal knowledge in nonhuman animals. However, recent evidence suggests that when the confound of tool-use is avoided, great apes' performance improves dramatically. In the present study, we examined the cognitive underpinnings of tool-use that contribute to apes' poor performance in trap tasks. We presented chimpanzees (Pan troglodytes), bonobos (Pan paniscus), and orangutans (Pongo abelii) with different versions of a maze-like, multilevel trap task. We manipulated whether the apes had to use their fingers or a stick to negotiate a reward through the maze. Furthermore, we varied whether the apes got visual information about the functionality of the traps (i.e. blockage of free passage) or only arbitrary color stimuli indicating the location of the traps. We found that apes in the finger-maze task outperformed apes in the tool-use-maze task (and partially planned their moves multiple steps ahead) and (2) tool-using apes failed to learn to avoid the traps and performed similar to apes that did not get functional information about the traps. Follow-up experiments with apes that already had learnt to avoid the traps showed that tool-use or the color cues per se did not pose a problem for experienced apes. These results suggest that simultaneously monitoring two spatial relations (tool-reward and reward-surface of the apparatus) might overstrain apes' cognitive system. Thus, trap tasks involving tool-use might constitute a dual task loading on the same cognitive resources; a candidate for these shared resources is the attentional system.

Tool use research has suffered from a lack of consistent theoretical frameworks. There is a plethora of tool use definitions and the most widespread ones are so inclusive that the behaviors that fall under them arguably do not have much in common. The situation is aggravated by the prevalence of anecdotes, which have played an undue role in the literature. In order to provide a more rigorous foundation for research and to advance our understanding of the interrelation between tool use and cognition, we suggest the adoption of Fragaszy and Mangalam's (2018) tooling framework, which is characterized by the creation of a body-plus-object system that manages a mechanical interface between tool and surface. Tooling is limited to a narrower suite of behaviors than tool use, which might facilitate its neurocognitive investigation. Indeed, evidence in the literature indicates that tooling has distinct neurocognitive underpinnings not shared by other activities typically classified as tool use, at least in primates. In order to understand the extent of tooling incidences in previous research, we systematically surveyed the comprehensive tool use catalog by Shumaker et al. (2011). We identified 201 tool use submodes, of which only 81 could be classified as tooling, and the majority of the tool use examples across species were poorly supported by evidence. Furthermore, tooling appears to be phylogenetically