The two visual systems hypothesis suggests processing of visual information into two distinct routes in the brain: a dorsal stream for the control of actions and a ventral stream for the identification of objects. Recently, increasing evidence has shown that the dorsal and ventral streams are not strictly independent, but do interact with each other. In this paper, we argue that the interactions between dorsal and ventral streams are important for controlling complex object-oriented hand movements, especially skilled grasp. Anatomical studies have reported the existence of direct connections between dorsal and ventral stream areas. These physiological interconnections appear to be gradually more active as the precision demands of the grasp become higher. It is hypothesised that the dorsal stream needs to retrieve detailed information about object identity, stored in ventral stream areas, when the object properties require complex fine-tuning of the grasp. In turn, the ventral stream might receive up to date grasp-related information from dorsal stream areas to refine the object internal representation. Future research will provide direct evidence for which specific areas of the two streams interact, the timing of their interactions and in which behavioural context they occur.

When lifting an object, the brain uses visual cues and an internal object representation to predict its weight and scale fingertip forces accordingly. Once available, tactile information is rapidly integrated to update the weight prediction and refine the internal object representation. If visual cues cannot be used to predict weight, force planning relies on implicit knowledge acquired from recent lifting experience, termed sensorimotor memory. Here, we investigated whether perception of weight is similarly biased according to previous lifting experience and how this is related to force scaling. Participants grasped and lifted series of light or heavy objects in a semi-randomized order and estimated their weights. As expected, we found that forces were scaled based on previous lifts (sensorimotor memory) and these effects increased depending on the length of recent lifting experience. Importantly, perceptual weight estimates were also influenced by the preceding lift, resulting in lower estimations after a heavy lift compared to a light one. In addition, weight estimations were negatively correlated with the magnitude of planned force parameters. This perceptual bias was only found if the current lift was light, but not heavy since the magnitude of sensorimotor memory effects had, according to Weber’s law, relatively less impact on heavy compared to light objects. A control experiment tested the importance of active lifting in mediating these perceptual changes and showed that when weights are passively applied on the hand, no effect of previous sensory experience is found on perception. These results highlight how fast learning of novel object lifting dynamics can shape weight perception and demonstrate a tight link between action planning and perception control. If predictive force scaling and actual object weight do not match, the online motor corrections, rapidly implemented to downscale forces, will also downscale weight estimation in a proportional manner.

Transcranial magnetic stimulation studies have highlighted that corticospinal excitability is increased during observation of object lifting, an effect termed "motor resonance." This facilitation is driven by movement features indicative of object weight, such as object size or observed movement kinematics. Here, we investigated in 35 humans (23 females) how motor resonance is altered when the observer's weight expectations, based on visual information, do not match the actual object weight as revealed by the observed movement kinematics. Our results highlight that motor resonance is not robustly driven by object weight but easily masked by a suppressive mechanism reflecting the correctness of weight expectations. Subsequently, we investigated in 24 humans (14 females) whether this suppressive mechanism was driven by higher-order cortical areas. For this, we induced "virtual lesions" to either the posterior superior temporal sulcus (pSTS) or dorsolateral prefrontal cortex (DLPFC) before having participants perform the task. Importantly, virtual lesion of pSTS eradicated this suppressive mechanism and restored object weight-driven motor resonance. In addition, DLPFC virtual lesion eradicated any modulation of motor resonance. This indicates that motor resonance is heavily mediated by top-down inputs from both pSTS and DLPFC. Together, these findings shed new light on the theorized cortical network driving motor resonance. That is, our findings highlight that motor resonance is not only driven by the putative human mirror neuron network consisting of the primary motor and premotor cortices as well as the anterior intraparietal sulcus, but also by top-down input from pSTS and DLPFC.

Skillful object lifting relies on scaling fingertip forces according to the object's weight. When no visual cues about weight are available, force planning relies on recent lifting experience. Recently, we showed that previously lifted objects also affect weight estimation, as objects are perceived to be lighter when lifted after heavy objects compared to after light ones. Here, we investigated the underlying neural mechanisms mediating these effects. We asked participants to lift objects and estimate their weight. Simultaneously, we applied transcranial magnetic stimulation (TMS) during the dynamic loading or static holding phase. Two subject groups received TMS over either the anterior intraparietal sulcus (aIPS) or lateral occipital area (LO), known to be important nodes in object grasping and perception. We hypothesized that TMS over aIPS and LO during object lifting would alter force scaling and weight perception. Contrary to our hypothesis, we did not find effects of aIPS or LO stimulation on force planning or weight estimation caused by previous lifting experience. However, we found that TMS over both areas increased grip forces, but only when applied during dynamic loading, and decreased weight estimation, but only when applied during static holding, suggesting time-specific effects. Interestingly, our results also indicate that TMS over LO, but not aIPS, affected load force scaling specifically for heavy objects, which further indicates that load and grip forces might be controlled differently. These findings provide new insights on the interactions between brain networks mediating action and perception during object manipulation.