Abstract
Parietal and premotor cortices of the macaque monkey contain distinct populations of neurons which, in addition to their motor discharge, are also activated by visual stimulation. Among these visuomotor neurons, a population of grasping neurons located in the anterior intraparietal area (AIP) shows discharge modulation when the own hand is visible during object grasping. Given the dense connections between AIP and inferior frontal regions, we aimed at investigating whether two hand-related frontal areas, ventral premotor area F5 and primary motor cortex (area F1), contain neurons with similar properties. Two macaques were involved in a grasping task executed in various light/dark conditions in which the to-be-grasped object was kept visible by a dim retro-illumination. Approximately 62% of F5 and 55% of F1 motor neurons showed light/dark modulations. To better isolate the effect of hand-related visual input, we introduced two further conditions characterized by kinematic features similar to the dark condition. The scene was briefly illuminated (i) during hand preshaping (pre-touch flash, PT-flash) and (ii) at hand-object contact (touch flash, T-flash). Approximately 48% of F5 and 44% of F1 motor neurons showed a flash-related modulation. Considering flash-modulated neurons in the two flash conditions, ∼40% from F5 and ∼52% from F1 showed stronger activity in PT- than T-flash (PT-flash-dominant), whereas ∼60% from F5 and ∼48% from F1 showed stronger activity in T- than PT-flash (T-flash-dominant). Furthermore, F5, but not F1, flash-dominant neurons were characterized by a higher peak and mean discharge in the preferred flash condition as compared to light and dark conditions. Still considering F5, the distribution of the time of peak discharge was similar in light and preferred flash conditions. This study shows that the frontal cortex contains neurons, previously classified as motor neurons, which are sensitive to the observation of meaningful phases of the own grasping action. We conclude by discussing the possible functional role of these populations.
Highlights
Primates distinguish themselves from other species by a highly evolved grasping and manipulative capacity (MacNeilage, 1990; Sartori et al, 2012; Wells & Turnquist, 2001)
In addition to the traditional light vs dark approach, we added two main modifications: (i) we investigated the effect of instantaneous visual presentation of the acting hand at different grasping phases, ensuring that arm/hand kinematics were not modified with respect to the dark condition, and (ii) the to-be-grasped object was always kept visible by a dim retro-illumination in order to reduce to a minimum the kinematic differences between light and dark
Kruskal-Wallis test performed on grip size values (Fig. 2C) revealed that maximal grip aperture decreased (p = 0.019) in light condition compared to dark, PT- and T-flash conditions
Summary
Primates distinguish themselves from other species by a highly evolved grasping and manipulative capacity (MacNeilage, 1990; Sartori et al, 2012; Wells & Turnquist, 2001). Area F5, which receives a relevant parietal input from area AIP (Rizzolatti & Luppino, 2001), would transform object representations into grasping motor commands further elaborated in the primary motor cortex (area F1; Fogassi et al, 2001). Consistent with their strong anatomical connections (Matelli, Luppino & Rizzolatti, 1985), parietal and ventral premotor areas share neuronal populations with similar visuomotor properties. It has been suggested that these classes of neurons take part in processes of action-observation matching and sensorimotor transformation for grasping (Fadiga et al, 2000; Rizzolatti & Fadiga, 1998)
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