The macaque lateral grasping network: A neural substrate for generating purposeful hand actions

Borra, Elena; Gerbella, Marzio; Rozzi, Stefano; Luppino, Giuseppe

doi:10.1016/j.neubiorev.2017.01.017

Cited by 102 publications

(78 citation statements)

References 406 publications

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“…Other anatomical studies showed that the parietal and premotor mirror areas share numerous other anatomical connections that may extend the functional properties of this neural mechanism beyond the classically described functions (Rizzolatti et al, 2014; Bonini, 2015; Borra et al, 2017). Among these connections, in particular, area F5 is anatomically connected with other cortical motor regions such as F1, F2vr (ventrorostral) and F6 which also are endowed with mirror properties or with properties related to self-other behaviors (Cisek and Kalaska, 2004; Kraskov et al, 2009; Yoshida et al, 2011).…”

Section: Introductionmentioning

confidence: 88%

Two different mirror neuron networks: The sensorimotor (hand) and limbic (face) pathways

et al. 2017

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The vast majority of functional studies investigating mirror neurons (MNs) explored their properties in relation to hand actions, and very few investigated how MNs responding to mouth actions or communicative gestures. From an anatomical point of view, hand and mouth MNs were recorded in two partially overlapping sectors of the ventral precentral cortex of the macaque monkey: hand MNs were located more dorsally (area F5), mouth MNs more ventrally, extending over the border between the premotor (F5) and the opercular region (DO and PrCO). Despite this anatomical segregation, there is a general assumption that a same neuroanatomical network, having a main source of visual information deriving from the parietal cortex, supports both hand and mouth MNs. In the current review, we challenge this perspective and describe the connectivity pattern of mouth MNs sector, comparing it with the hand MNs sector of F5. The mouth and hand MNs sectors share part of their connectivity pattern, but each also has distinct and specific connections. In particular, the mouth MNs F5/opercular region is connected with premotor, parietal areas mostly related to the somatosensory and motor representation of the face/mouth (area F4, the region between areas F3 and F6, areas PF and SII) and with area PrCO, involved in processing gustatory and somatosensory intraoral input. Unlike hand MNs, mouth MNs do not receive their visual input from parietal regions. Information related to face/communicative behaviors could come from the ventrolateral prefrontal cortex (areas 12 and 46). Further strong connections derive from limbic structures involved in encoding emotional facial expressions and motivational/reward processing. These brain structures include the anterior cingulate cortex, the anterior and mid-dorsal insula, orbitofrontal cortex and the basolateral amygdala. These anatomical data are in agreement with neurophysiological evidence showing that in the mouth MNs F5/opercular region there are neurons responding to facial communicative gestures and also neurons firing during the production of vocalizations. The mirror mechanism is therefore composed and supported by at least two different anatomical pathways: one is concerned with sensorimotor transformation in relation to reaching and hand grasping within the traditional parietal-premotor circuits; the second one is linked to the mouth/face motor control and is connected with limbic structures, involved in communication/emotions and reward processing. This new view of the mirror mechanism provides a new theoretical account to explain different patterns of brain activation in neuroimaging studies and has also important implications for our comprehension of the developmental factors and evolutionary processes involved in mirror neurons origins and functions.

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Section: Introductionmentioning

confidence: 88%

Two different mirror neuron networks: The sensorimotor (hand) and limbic (face) pathways

et al. 2017

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“…1) is formed by parietal area PFG (entry point), AIP, and SII, by premotor area F5a, prefrontal areas 46 ventrocaudal, and part of area 12. The LGS is regarded as a privileged network to encodes purposeful hand actions (for dedicated reviews, see Borra et al, 2017;Borra and Luppino, 2018). Recent studies suggest that it can be recruited by inputs from area F6 (Lanzilotto et al, 2016).…”

Section: The Lateral Grasping System (Lgs)mentioning

confidence: 99%

Corticocortical Systems Underlying High-Order Motor Control

Battaglia-Mayer

Caminiti

2019

J. Neurosci.

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Cortical networks are characterized by the origin, destination, and reciprocity of their connections, as well as by the diameter, conduction velocity, and synaptic efficacy of their axons. The network formed by parietal and frontal areas lies at the core of cognitive-motor control because the outflow of parietofrontal signaling is conveyed to the subcortical centers and spinal cord through different parallel pathways, whose orchestration determines, not only when and how movements will be generated, but also the nature of forthcoming actions. Despite intensive studies over the last 50 years, the role of corticocortical connections in motor control and the principles whereby selected cortical networks are recruited by different task demands remain elusive. Furthermore, the synaptic integration of different cortical signals, their modulation by transthalamic loops, and the effects of conduction delays remain challenging questions that must be tackled to understand the dynamical aspects of parietofrontal operations. In this article, we evaluate results from nonhuman primate and selected rodent experiments to offer a viewpoint on how corticocortical systems contribute to learning and producing skilled actions. Addressing this subject is not only of scientific interest but also essential for interpreting the devastating consequences for motor control of lesions at different nodes of this integrated circuit. In humans, the study of corticocortical motor networks is currently based on MRI-related methods, such as resting-state connectivity and diffusion tract-tracing, which both need to be contrasted with histological studies in nonhuman primates.

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“…A considerable body of work has indicated that cooperative interplay of both hemispheres is required for movement, and further that each hemisphere is responsible for different aspects of motor programming for complex actions (Sainburg et al 2002). When considering grasping and hand-object manipulation, fronto-parietal connections are essential in providing the motor program with visual and somatosensory information required to achieve adequate hand shaping and control in both monkeys and humans (Borra et al 2017;Turella & Lingnau 2014). Three parallel branches of the superior longitudinal fasciculus convey sensorimotor transformations between frontal and parietal regions, each of which has different patterns of structural asymmetry (Thiebaut de Schotten et al 2011).…”

Section: Discussionmentioning

confidence: 99%

“…Skilled manual action requires sensorimotor transformations to coordinate adequate muscle synergies to perform finger movements. Sensorimotor integration mainly requiring visual and somatic information, is mediated by a widespread fronto-parietal circuit (Turella & Lingnau, 2014), which has been well studied in macaques (Borra et al 2017) but only partially in humans (Binkofski et al 1999). Notably, neurons tuned to eye and hand movements in monkey fronto-parietal regions code primarily for the contralateral limb, but also for the ipsilateral limb (Cisek et al 2 003).…”

Section: Introductionmentioning

confidence: 99%

The effect of left fronto-parietal resections on hand selection: a lesion-tractography study

Howells

Puglisi

Leonetti

et al. 2019

Preprint

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Strong right-hand preference on the population level is a uniquely human feature, although the neural basis for this is still not clearly defined. Recent behavioural and neuroimaging literature suggests that hand preference may be related to the orchestrated function and size of fronto-parietal white matter tracts bilaterally. Lesions to these tracts induced during tumour resection may provide an opportunity to test this hypothesis. In the present study, a cohort of seventeen neurosurgical patients with left hemisphere brain tumours were recruited to investigate whether resection of certain white matter tracts affects the choice of hand selected for the execution of a goal-directed task (assembly of jigsaw puzzles). Patients performed the puzzles, but also tests for basic motor ability, selective attention and visuo-constructional ability, preoperatively and one month after surgery. Diffusion tractography of fronto-parietal tracts (the superior longitudinal fasciculus) and the corticospinal tract were performed, to evaluate whether resection of tracts was significantly associated with changes in hand selection. A complementary atlas-based disconnectome analysis was also conducted. Results showed a shift in hand selection despite the absence of any motor or cognitive deficits, which was significantly associated with patients with frontal and parietal resections, compared with those with resections in other lobes. In particular, this effect was significantly associated with the resection of dorsal fronto-parietal white matter connections, but not with the ventral fronto-parietal tract. Dorsal white matter pathways contribute bilaterally, with specific lateralised competencies, to control of goaldirected hand movements. We show that unilateral lesions, by unbalancing the cooperation of the two hemispheres, can alter the choice of hand selected to accomplish movements.

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The macaque lateral grasping network: A neural substrate for generating purposeful hand actions

Cited by 102 publications

References 406 publications

Two different mirror neuron networks: The sensorimotor (hand) and limbic (face) pathways

Two different mirror neuron networks: The sensorimotor (hand) and limbic (face) pathways

Corticocortical Systems Underlying High-Order Motor Control

The effect of left fronto-parietal resections on hand selection: a lesion-tractography study

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