Activity in ventral premotor cortex is modulated by vision of own hand in action

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.

Functional Properties of Parietal Hand Manipulation–related Neurons and Mirror Neurons Responding to Vision of Own Hand Action

“…This may be an important process for identification of self-body action. The system also leads to generalization of matching between actions and viewing actions executed by other individuals (Fadiga et al, 2013;Raos et al, 2006). The idea is congruent with our results that mirror neurons are found in AIP where hand-type neurons are found.…”

“…We hypothesize that these neurons are capable of monitoring ongoing hand movement by comparing the corollary discharge (predicted sensory feedback) with the actual visual feedback. Notably, the activity of premotor neurons is modulated by transient visual feedback during grasping actions (Fadiga et al, 2013), demonstrating that a subset of premotor neurons is sensitive to the observation of oneʼs own grasping. Fadiga et al suggested that this modulation is due to an effect along the parietal-frontal pathway.…”

Finger pressure adjustments to various object configurations during precision grip in humans and monkeys

“…Hand movements during the task were recorded by a 3D-motion optical analyzer (Qualisys Motion Capture System; Qualisys, Charlotte, USA) and were synchronized by using the TTL signal of pad release. Setup and procedure were similar to those described by a previous work (Fadiga et al, 2013). Three small adhesive infraredreflective spheres (diameter 3.0 mm, weight 40 mg) were placed over three anatomical landmarks: the wrist (head of the ulna) and the last interphalangeal joint of thumb and index finger.…”

“…The motion analysis software reconstructed the 3D coordinates of the markers in space and time, enabling off-line reconstruction of the movement of each marker. Movements were recorded at a sampling rate of 200 Hz, a value considered more than appropriate for the biological motion of primates (Saleh et al, 2012;Fadiga et al, 2013). Using TTL signals from the pad (at the release) and from the handle (at touch), we analyzed wrist velocity and grip aperture, i.e., the distance between the two markers placed on the fingers.…”

An fMRI Compatible Touchscreen to Measure Hand Kinematics during a Complex Drawing Task

“…Due to the restricted environment of functional Magnetic Resonance Imaging (fMRI), most studies investigating kinematics have used simple hand movements (e.g. [3,4]) or the mere observation of movements (e.g. [5,6]) to study the neural correlates of motor control.…”