Functional Brain Mapping of Monkey Tool Use

doi:10.1006/nimg.2001.0878

NeuroImage

Volume 14, Issue 4, October 2001, Pages 853-861

https://doi.org/10.1006/nimg.2001.0878 Get rights and content

Abstract

When using a tool, we can perceive a psychological association between the tool and the body parts—the tool is incorporated into our “body-image.” During tool use, visual response properties of bimodal (tactile and visual) neurons in the intraparietal area of the monkey's cerebral cortex were modified to include the hand-held tool. Visual properties of the monkey intraparietal neurons may represent the body-image in the brain. We explored tool use-induced activation within the intraparietal area and elsewhere in alert monkey brain using positron emission tomography (PET). Tool use-related activities compared with the control condition (simple-stick manipulation) revealed a significant increase in cerebral blood flow in the corresponding intraparietal region, basal ganglia, presupplementary motor area, premotor cortex, and cerebellum. These tool use-specific areas may participate in maintaining and updating the body-image for the precise guidance of a hand-held rake onto a distant reward.

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The body in the world: tools and somato-centric maps in the primate brain
2023, Cognitive Archaeology, Body Cognition, and the Evolution of Visuospatial Perception
Throughout their evolutionary process, primates acquired biological traits suited for object and tool manipulation. The vertical rotation of the body axis, first in sitting and later in standing and walking, promoted forelimb specialization for precise manual tasks. This verticalization was accompanied by a dissociation of body, hand, and head axes that complexified spatial processing. Tool usage by early hominids coincided with a massive increase in brain size and the emergence of neural structures dedicated to sensorimotor and cognitive processing of complex visually guided actions. Actual tool use triggers specific mechanisms by which the brain undergoes structural and functional changes, leading to the incorporation of the tool in the body representation. This process modifies the representation of the reachable/peripersonal space, expanding it beyond the limits of the body. As tools became more elaborate, social skills became essential for cultural transmission of tool manufacture and use. Observing oneself and others manipulating a tool enabled a convergence of egocentric and allocentric representations and paved the way for further mechanisms allowing the agent to situate itself in a social world.
Brain intrinsic connection patterns underlying tool processing in human adults are present in neonates and not in macaques
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Tool understanding and use are supported by a dedicated left-lateralized, intrinsically connected network in the human adult brain. To examine this network's phylogenetic and ontogenetic origins, we compared resting-state functional connectivity (rsFC) among regions subserving tool processing in human adults to rsFC among homologous regions in human neonates and macaque monkeys (adolescent and mature). These homologous regions formed an intrinsic network in human neonates, but not in macaques. Network topological patterns were highly similar between human adults and neonates, and significantly less so between humans and macaques. The premotor-parietal rsFC had most significant contribution to the formation of the neonatal tool network. These results suggest that an intrinsic brain network potentially supporting tool processing exists in the human brain prior to individual tool use experiences, and that the premotor-parietal functional connection in particular offers a brain basis for complex tool behaviors specific to humans.
The macaque ventral intraparietal area has expanded into three homologue human parietal areas
2022, Progress in Neurobiology
The macaque ventral intraparietal area (VIP) in the fundus of the intraparietal sulcus has been implicated in a diverse range of sensorimotor and cognitive functions such as motion processing, multisensory integration, processing of head peripersonal space, defensive behavior, and numerosity coding. Here, we exhaustively review macaque VIP function, cytoarchitectonics, and anatomical connectivity and integrate it with human studies that have attempted to identify a potential human VIP homologue. We show that human VIP research has consistently identified three, rather than one, bilateral parietal areas that each appear to subsume some, but not all, of the macaque area’s functionality. Available evidence suggests that this human “VIP complex” has evolved as an expansion of the macaque area, but that some precursory specialization within macaque VIP has been previously overlooked. The three human areas are dominated, roughly, by coding the head or self in the environment, visual heading direction, and the peripersonal environment around the head, respectively. A unifying functional principle may be best described as prediction in space and time, linking VIP to state estimation as a key parietal sensorimotor function. VIP’s expansive differentiation of head and self-related processing may have been key in the emergence of human bodily self-consciousness.
Development of a control task for clarifying the neural mechanisms underlying tool-use behavior in rats (Rattus norvegicus)
2019, MethodsX
Many studies on non-human animals have attempted to investigate the neural mechanisms underlying tool-use behavior. However, previous studies showed considerable non-tool-use-specific differences between tool-use and control tasks. The purpose of the present study was to develop a control training task for studies that investigate the neural mechanisms behind tool-use in rodents. Eight rats were subjected to control tasks which excluded tool-use-specific factors and consisted of training for hook-pulling and hook-choice tasks, as well as tool-choice tests which included tool-use specific factors and were similar to those in a previous study on rats. With the exception of one rat, the results of the hook-choice training showed that the previous study and the present study had similar difficulty levels. In the tool-choice tests of the present study, rats did not choose the functional tools over the non-functional tools when there was no contradiction between their appearance and functionality, which contrasted with the previous study on which this study was based on. These results suggest that the training task that excludes tool-use-specific factors can be appropriately utilized as a control task for studies investigating the neural mechanisms behind tool-use in animals and, potentially, in humans.
- •
  Hook-choice training without tool-use-specific factors can be performed as a control task.
- •
  Prior tool-use training improved rats’ performance in experimental tests.
- •
  Control task for rodents allows investigation of the neural mechanisms of tool-use.
Getting a handle on virtual tools: An examination of the neuronal activity associated with virtual tool use
2018, Neuropsychologia
Tool use is associated with three visual streams—dorso-dorsal, ventro-dorsal, and ventral visual streams. These streams are involved in processing online motor planning, action semantics, and tool semantics features, respectively. Little is known about the way in which the brain represents virtual tools. To directly assess this question, a virtual tool paradigm was created that provided the ability to manipulate tool components in isolation of one another. During functional magnetic resonance imaging (fMRI), adult participants performed a series of virtual tool manipulation tasks in which vision and movement kinematics of the tool were manipulated. Reaction time and hand movement direction were monitored while the tasks were performed. Functional imaging revealed that activity within all three visual streams was present, in a similar pattern to what would be expected with physical tool use. However, a previously unreported network of right-hemisphere activity was found including right inferior parietal lobule, middle and superior temporal gyri and supramarginal gyrus – regions well known to be associated with tool processing within the left hemisphere. These results provide evidence that both virtual and physical tools are processed within the same brain regions, though virtual tools recruit bilateral tool processing regions to a greater extent than physical tools.
The parietal lobe and tool use
2018, Handbook of Clinical Neurology
The ability to craft and use tools is a crucial skill of human beings, distinguishing humans from all other species. Humans show a unique capacity to create novel, technologically advanced devices and represent physical causality using tools. In the present chapter we review the effect of tool use in changing body–space multisensory integration and body representation and the fundamental contribution of the parietal lobe to the neural underpinnings of tool use. In the final section we briefly introduce the effect of parietal brain damage on tool use.
At the beginning of 20th century, a crucial role for the left parietal lobe for a proper control of gestures, including the pantomimed and actual use of tools, was already clear. Actual available evidence supports a critical role of the parietal lobe for both the lower-level multisensory integration of somatosensory and visual input necessary for the interactions between body, tools, and external objects, and for the representation of the mechanical and conceptual dynamics of tool use. Parietal regions, rather than merely representing the prototypical use of a tool, would be critical to understand the general mechanical interactions of the tool with the environment.
The increase of knowledge about such brain mechanisms is of utmost relevance in the present times, characterized by the development of more and more sophisticated technological tools, such as functional prostheses, robotic interfaces, and virtual-reality devices.

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¹: To whom correspondence and reprint requests should be addressed at Division of Advanced Technology for Medical Imaging, National Institute of Radiological Sciences, 4-9-1, Anagawa, Inageku, Chiba-shi 263-8555, Japan. Fax: +81-43-253-0396. E-mail: [email protected].

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Regular ArticleFunctional Brain Mapping of Monkey Tool Use

Abstract

Trends Neurosci.

Behav. Brain Res.

Neuron

Curr. Opin. Neurobiol.

NeuroImage

Behav. Brain Res.

Neurosci. Lett.

Neurosci. Res.

Reorganization of activity in the supplementary motor area associated with motor learning and functional recovery

Exp. Brain Res.

Parallel organization of functionally segregated circuits linking basal ganglia and cortex

Annu. Rev. Neurosci.

Multimodal representation of space in the posterior parietal cortex and its use in planning movements

Annu. Rev. Neurosci.

Functional anatomic studies of memory retrieval for auditory words and visual pictures

J. Neurosci.

Ventral intraparietal area of the macaque: Anatomic location and visual response properties

J. Neurophysiol.

Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: A dual tracer study

J. Comp. Neurol.

Mapping motor representations with positron emission tomography

Nature

Cortical areas and the selection of movement: A study with positron emission tomography

Exp. Brain Res.

Spatial invariance of visual receptive fields in parietal cortex neurons

Nature

The origin of corticospinal projections from the premotor areas in the frontal lobe

J. Neurosci.

Coding of peripersonal space in inferior premotor cortex (area F4)

J. Neurophysiol.

Statistical parametric maps in functional imaging: A general linear approach

Hum. Brain Mapp.

Inferotemporal neurons distinguish and retain behaviorally relevant features of visual stimuli

Science

Cognitive planning deficit in patients with cerebellar atrophy

Neurology

Coding the location of the arm by sight

Science

Coding of visual space by premotor neurons

Science

Sensory disturbance from cerebral lesions

Brain

Activation of human presupplementary motor area in learning of sequential procedures: A functional MRI study

J. Neurophysiol.

Disturbances of visual orientation

Brit. J. Ophthal.

Regular Article
Functional Brain Mapping of Monkey Tool Use