The evolutionary neuroscience of tool making

The appearance of the first intentionally modified stone tools over 2.5 million years ago marked a watershed in human evolutionary history, expanding the human adaptive niche and initiating a trend of technological elaboration that continues to the present day. However, the cognitive foundations of this behavioral revolution remain controversial, as do its implications for the nature and evolution of modern human technological abilities. Here we shed new light on the neural and evolutionary foundations of human tool making skill by presenting functional brain imaging data from six inexperienced subjects learning to make stone tools of the kind found in the earliest archaeological record. Functional imaging of this complex, naturalistic task was accomplished through positron emission tomography with the slowly decaying radiological tracer (18)flouro-2-deoxyglucose. Results show that simple stone tool making is supported by a mosaic of primitive and derived parietofrontal perceptual-motor systems, including recently identified human specializations for representation of the central visual field and perception of three-dimensional form from motion. In the naive tool makers reported here, no activation was observed in prefrontal executive cortices associated with strategic action planning or in inferior parietal cortex thought to play a role in the representation of everyday tool use skills. We conclude that uniquely human capacities for sensorimotor adaptation and affordance perception, rather than abstract conceptualization and planning, were central factors in the initial stages of human technological evolution. The appearance of the first intentionally modified stone tools over 2.5 million years ago marked a watershed in human evolutionary history, expanding the human adaptive niche and initiating a trend of technological elaboration that continues to the present day. However, the cognitive foundations of this behavioral revolution remain controversial, as do its implications for the nature and evolution of modern human technological abilities. Here we shed new light on the neural and evolutionary foundations of human tool making skill by presenting functional brain imaging data from six inexperienced subjects learning to make stone tools of the kind found in the earliest archaeological record. Functional imaging of this complex, naturalistic task was accomplished through positron emission tomography with the slowly decaying radiological tracer (18)flouro-2-deoxyglucose. Results show that simple stone tool making is supported by a mosaic of primitive and derived parietofrontal perceptual-motor systems, including recently identified human specializations for representation of the central visual field and perception of three-dimensional form from motion. In the naive tool makers reported here, no activation was observed in prefrontal executive cortices associated with strategic action planning or in inferior parietal cortex thought to play a role in the representation of everyday tool use skills. We conclude that uniquely human capacities for sensorimotor adaptation and affordance perception, rather than abstract conceptualization and planning, were central factors in the initial stages of human technological evolution

Editorial: Perceiving and Acting in the real world: from neural activity to behavior

The interaction between perception and action represents one of the pillars of human evolutionary success. Our interactions with the surrounding world involve a variety of behaviors, almost always including movements of the eyes and hands. Such actions rely on neural mechanisms that must process an enormous amount of information in order to generate appropriate motor commands. Yet, compared to the great advancements in the field of perception for cognition, the neural underpinnings of how we control our movements, as well as the interactions between perception and motor control, remain elusive. With this research topic we provide a framework for: 1) the perception of real objects and shapes using visual and haptic information, 2) the reference frames for action and perception, and 3) how perceived target properties are translated into goal-directed actions and object manipulation. The studies in this special issue employ a variety of methodologies that include behavioural kinematics, neuroimaging, transcranial magnetic stimulation and patient cases. Here we provide a brief summary and commentary on the articles included in this research topic

A validated set of tool pictures with matched objects and non-objects for laterality research

Neuropsychological and neuroimaging research has established that knowledge related to tool use and tool recognition is lateralized to the left cerebral hemisphere. Recently, behavioural studies with the visual half-field technique have confirmed the lateralization. A limitation of this research was that different sets of stimuli had to be used for the comparison of tools to other objects and objects to non-objects. Therefore, we developed a new set of stimuli containing matched triplets of tools, other objects and non-objects. With the new stimulus set, we successfully replicated the findings of no visual field advantage for objects in an object recognition task combined with a significant right visual field advantage for tools in a tool recognition task. The set of stimuli is available as supplemental data to this article

Brainstem circuits involved in skilled forelimb movements

Movement is the main output of the nervous system as well as the fundamental form of interaction animals have with their environment. Due to its function and scope, movement has to be characterized by both stability and flexibility. Such apparently conflicting attributes are reflected in the complex organization of the motor system, composed of a vast network of widely distributed circuits interacting with each other to generate an appropriate motor output. Different neuronal structures, located throughout the brain, are responsible for producing a broad spectrum of actions, ranging from simple locomotion to complex goal directed movements such as reaching for food or playing a musical instrument. The brainstem is one of such structures, holding considerable importance in the generation of the motor output, but also largely unexplored, due to its less-than-accessible anatomic location, functional intricacies and the lack of appropriate techniques to investigate its complexity. Despite recent advances, a deeper understanding of the role of brainstem neuronal circuits in skilled movements is still missing. In this dissertation, we investigated the involvement of the lateral rostral medulla (LatRM) in the construction of skilled forelimb behaviors. The focus of my work was centered on elucidating the anatomical and functional relationships between LatRM and the caudal brainstem, and specifically on the interactions with the medullary reticular formation, considering both its ventral (MdV) and dorsal subdivisions (MdD). In summary, we reveal the existence of anatomically segregated subpopulations of neurons in the lower brainstem which encode different aspects of skilled forelimb movements. Moreover, we show that LatRM neurons are necessary for the correct execution of skilled motor programs and their activation produces complex coordinated actions. All this evidence suggests that LatRM may be a key orchestrator for skilled movements by functioning as integration center for upstream signals as well as coordinator by selecting the appropriate effectors in the lower medulla and the spinal cord

Investigating the Declarative and Procedural Memory Processes Underlying Acquisition of Tool-Related Knowledge and Skills

It has been proposed that the acquisition of tool-related knowledge and skills (e.g., attributes of a tool, how it is used, how it is grasped) relies on a complex set of memory processes. However, the precise memory representations of different aspects of tool knowledge are still unclear. It has also been argued that some aspects may require an interaction between the declarative and procedural memory systems. However, the nature of this interaction between both memory systems in relation to tool-related knowledge is not well understood. A series of three experiments was carried out in the current dissertation to systematically investigate the role of declarative and procedural memory in mediating complex tool knowledge and skills. In Experiment 1 participants with Parkinson’s disease (PD) showed unimpaired memory for tool attributes and tool grasping relative to controls. In addition, participants with PD showed intact motor skill learning and skilled tool use within sessions, but failed to retain proficiency of these skills after a 3-week delay. In Experiment 2, declarative encoding processes were interrupted in healthy adults by dividing attention during training. Findings showed that dividing attention during training was detrimental for subsequent memory for tool attributes as well as accurate demonstration of tool use and tool grasping. However, dividing attention did not interfere with motor skill learning. In Experiment 3, motor procedural learning among healthy adults was disrupted by limiting access to performance-based feedback during training. Results showed that recall of tool attributes and tool grasping were intact, but limited feedback was detrimental for motor skill learning and skilled tool use. Taken together, the results suggest that memory for tool attributes and tool grasping primarily relies on declarative memory which is associated with the medial temporal lobes. In contrast, findings suggest that motor skill acquisition related to complex tools is primarily supported by striatal-dependent procedural memory. Thus, these results represent a dissociation between declarative and procedural aspects of tool knowledge and skills. Findings from the current studies also provide new insights into the interaction between declarative and procedural memory. The results suggest that skilled tool use requires a cooperative interaction of both systems. The evidence also suggests that the pattern of interaction between memory systems may vary, depending on the learning context

Perception meets action: fMRI and behavioural investigations of human tool use

Tool use is essential and culturally universal to human life, common to hunter-gatherer and modern advanced societies alike. Although the neuroscience of simpler visuomotor behaviors like reaching and grasping have been studied extensively, relatively little is known about the brain mechanisms underlying learned tool use. With learned tool use, stored knowledge of object function and use supervene requirements for action programming based on physical object properties. Contemporary models of tool use based primarily on evidence from the study of brain damaged individuals implicate a set of specialized brain areas underlying the planning and control of learned actions with objects, distinct from areas devoted to more basic aspects of visuomotor control. The findings from the current thesis build on these existing theoretical models and provide new insights into the neural and behavioural mechanisms of learned tool use. In Project 1, I used fMRI to visualize brain activity in response to viewing tool use grasping. Grasping actions typical of how tools are normally grasped during use were found to preferentially activate occipitotemporal areas, including areas specialized for visual object recognition. The findings revealed sensitivity within this network to learned contextual associations tied to stored knowledge of tool-specific actions. The effects were seen to arise implicitly, in the absence of concurrent effects in visuomotor areas of parietofrontal cortex. These findings were taken to reflect the tuning of higher-order visual areas of occipitotemporal cortex to learned statistical regularities of the visual world, including the way in which tools are typically seen to be grasped and used. These areas are likely to represent an important source of inputs to visuomotor areas as to learned conceptual knowledge of tool use. In Project 2, behavioural priming and the kinematics of real tool use grasping was explored. Behavioural priming provides an index into the planning stages of actions. Participants grasped tools to either move them, grasp-to-move (GTM), or to demonstrate their common use, grasp-to-use (GTU), and grasping actions were preceded by a visual preview (prime) of either the same (congruent) or different (incongruent) tool as that which was then acted with. Behavioural priming was revealed as a reaction time advantage for congruent trial types, thought to reflect the triggering of learned use-based motor plans by the viewing of tools at prime events. The findings from two separate experiments revealed differential sensitivity to priming according to task and task setting. When GTU and GTM tasks were presented separately, priming was specific to the GTU task. In contrast, when GTU and GTM tasks were presented in the same block of trials, in a mixed task setting, priming was evident for both tasks. Together the findings indicate the importance of both task and task setting in shaping effects of action priming, likely driven by differences in the allocation of attentional resources. Differences in attention to particular object features, in this case tool identity, modulate affordances driven by those features which in turn determines priming. Beyond the physical properties of objects, knowledge and intention of use provide a mechanism for which affordances and the priming of actions may operate. Project 3 comprised a neuroimaging variant of the behavioural priming paradigm used in Project 2, with tools and tool use actions specially tailored for the fMRI environment. Preceding tool use with a visual preview of the tool to be used gave rise to reliable neural priming, measured as reduced BOLD activity. Neural priming of tool use was taken to reflect increased metabolic efficiency in the retrieval and implementation of stored tool use plans. To demonstrate specificity of priming for familiar tool use, a control task was used whereby actions with tools were determined not by tool identity but by arbitrarily learned associations with handle color. The findings revealed specificity for familiar tool-use priming in four distinct parietofrontal areas, including left inferior parietal cortex previously implicated in the storage of learned tool use plans. Specificity of priming for tool-action and not color-action associations provides compelling evidence for tool-use-experience-dependent plasticity within parietofrontal areas

Action execution, action perception and 'mirror' neurones

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How the brain grasps tools: fMRI & motion-capture investigations

Humans’ ability to learn about and use tools is considered a defining feature of our species, with most related neuroimaging investigations involving proxy 2D picture viewing tasks. Using a novel tool grasping paradigm across three experiments, participants grasped 3D-printed tools (e.g., a knife) in ways that were considered to be typical (i.e., by the handle) or atypical (i.e., by the blade) for subsequent use. As a control, participants also performed grasps in corresponding directions on a series of 3D-printed non-tool objects, matched for properties including elongation and object size. Project 1 paired a powerful fMRI block-design with visual localiser Region of Interest (ROI) and searchlight Multivoxel Pattern Analysis (MVPA) approaches. Most remarkably, ROI MVPA revealed that hand-selective, but not anatomically overlapping tool-selective, areas of the left Lateral Occipital Temporal Cortex and Intraparietal Sulcus represented the typicality of tool grasping. Searchlight MVPA found similar evidence within left anterior temporal cortex as well as right parietal and temporal areas. Project 2 measured hand kinematics using motion-capture during a highly similar procedure, finding hallmark grip scaling effects despite the unnatural task demands. Further, slower movements were observed when grasping tools, relative to non-tools, with grip scaling also being poorer for atypical tool, compared to non-tool, grasping. Project 3 used a slow-event related fMRI design to investigate whether representations of typicality were detectable during motor planning, but MVPA was largely unsuccessful, presumably due to a lack of statistical power. Taken together, the representations of typicality identified within areas of the ventral and dorsal, but not ventro-dorsal, pathways have implications for specific predictions made by leading theories about the neural regions supporting human tool-use, including dual visual stream theory and the two-action systems model