A major achievement of primates evolution is skilled hand action, that depends on the direct cortico-motoneural system, as well as on the expansion of the parietal lobe. The first is responsible for encoding the dynamic force necessary to grasp and manipulate objects, the second to shape the hand configuration to the physical and geometrical properties of objects. Therefore, the parieto-frontal interplay lays at the core of primates manipulative skills. To characterize the temporal aspects of this recurrent mechanism, we will record neural activity simultaneously from both parietal and premotor cortex of monkeys, while these exert directional hand forces on an isometric joy-stick, so as to move a visual cursor from a central location to different visual targets on a screen. To determine which action parameter is encoded by premotor and parietal neurons, during neural recording, monkeys will be exposed to a new force condition, that will oblige them to change the force output necessary to successfully bring the cursor to the target. This task perturbation will also allow to determine if and how the new learned association between force exerted and visual cursor's motion is encoded by neural activity. Finally, during a 'wash-out' session, the perturbation will be removed, so as to determine whether a memory of the new learned association will remain in neural activity, at the service of predictive control of force during future hand actions. This study is inspired by the consequence of parietal and frontal lesions manipulative skills in humans, that predict that both region participate to the distributed control of hand action, although with different role. It is our hypothesis that while both areas encode force variation over time, premotor cortex has a prominent role in encoding static hand force as well. Parietal cortex can serve as a memory reservoir of the hand dynamics required for object manipulations spanning over time.
The novelty of this study is both conceptual and methodological. On the conceptual side, the assumption that old assumption (Hamel-Paquet et al. 2006) that parietal cortex encodes action kinematics and not dynamics clashes with the most recent achievements on the anatomical organization of the parieto-frontal network (Caminiti et al. 2017), with a case report about the clinical consequence of parietal lesions in patients (Ferrari-Toniolo et al. 2014), as well as with a pilot physiological study of the representation of hand force during tool use (Ferrari-Toniolo et al. 2015).
From the methodological point of view, neural activity, in form the of single-unit firing frequency and local field potentials (LFP), has never been recorded simultaneously from parietal and frontal areas during object manipulation requiring the specification of different types of hand force and their change over time, as well as under unexpected perturbation of the force field.
If the project will be successful, the advancement of knowledge will refer to i) the predictive power of the statistic of connectivity, that is of computational neuroanatomy on cortical representation of visuomotor functions within the distributed parieto-frontal network; ii) the relevance of pathological behavior in inspiring animal models of cortical syndrome after brain lesion; iii) the accuracy of animal models in restoring a 'positive image' of the collapse of cortical function after lesion; iv) the possibility of inspiring new, physiologically-driven, rehabilitation protocols in patients suffering from frontal and parietal lesions, to be 'personalized' for both categories. Relevant to this issue is that all information combined for skilled hand action on objects can have multiple access node and outflow pathways, in other words can be encoded within a redundant network that represents a potential substrate for vicariation and recovery of function dependent on functional and/or anatomical plasticity. This is more than just an hypothesis, if only ones considers that it has been claimed that intensive object manipulation and use induce some changes in the structure and connectivity of parietal areas (Hihara et al., 2006; Quallo et al., 2009). If confirmed in a quantitative fashion at global network level, this will opens a new perspective for scientifically-founded rehabilitation procedures in apraxic patients suffering from parietal lesions.
References
Hamel-Paquet C, Sergio L, Kalaska J J. Neurophysiol. 95:3353-3370, 2006.
Caminiti R, Borra E, Visco-Comandini F, Battaglia-Mayer A, Averbeck B, Luppino G. eNeuro 4(1) e0306-16.2017
Ferrari-Toniolo S, O Papazachariadis, F Visco-Comandini, M Salvati, A D'Elia, F Di Berardino, R Caminiti, A Battaglia-Mayer. Neuropsychologia 63:59-7, 2014.
Ferrari-Toniolo S, F Visco-Comandini, O Papazachariadis, R Caminiti, A Battaglia-Mayer. J Neurosci 35: 10899¿10910, 2015.
Hihara S, Notoya T, Tanaka M, Ichinose S, Ojima H, Obayashi S, Fujii N, Iriki A. Neuropsychologia 44:2636-46, 2006
Quallo MM, Price CJ, Ueno K, Asamizuya T, Cheng K, Lemon RN, Iriki A. PNAS 106:18379-84