BackgroundWe physically interact with external stimuli when they occur within a limited space immediately surrounding the body, i.e., Peripersonal Space (PPS). In the primate brain, specific fronto-parietal areas are responsible for the multisensory representation of PPS, by integrating tactile, visual and auditory information occurring on and near the body. Dynamic stimuli are particularly relevant for PPS representation, as they might refer to potential harms approaching the body. However, behavioural tasks for studying PPS representation with moving stimuli are lacking. Here we propose a new dynamic audio-tactile interaction task in order to assess the extension of PPS in a more functionally and ecologically valid condition.Methodology/Principal FindingsParticipants vocally responded to a tactile stimulus administered at the hand at different delays from the onset of task-irrelevant dynamic sounds which gave the impression of a sound source either approaching or receding from the subject’s hand. Results showed that a moving auditory stimulus speeded up the processing of a tactile stimulus at the hand as long as it was perceived at a limited distance from the hand, that is within the boundaries of PPS representation. The audio-tactile interaction effect was stronger when sounds were approaching compared to when sounds were receding.Conclusion/SignificanceThis study provides a new method to dynamically assess PPS representation: The function describing the relationship between tactile processing and the position of sounds in space can be used to estimate the location of PPS boundaries, along a spatial continuum between far and near space, in a valuable and ecologically significant way.
Interaction with objects in the environment typically requires integrating information concerning the object location with the position and size of body parts. The former information is coded in a multisensory representation of the space around the body, a representation of peripersonal space (PPS), whereas the latter is enabled by an online, constantly updated, action-orientated multisensory representation of the body (BR). Using a tool to act upon relatively distant objects extends PPS representation. This effect has been interpreted as indicating that tools can be incorporated into BR. However, empirical data showing that tool-use simultaneously affects PPS representation and BR are lacking. To study this issue, we assessed the extent of PPS representation by means of an audio-tactile interaction task and BR by means of a tactile distance perception task and a body-landmarks localisation task, before and after using a 1-m-long tool to reach far objects. Tool-use extended the representation of PPS along the tool axis and concurrently shaped BR; after tool-use, subjects perceived their forearm narrower and longer compared to before tool-use, a shape more similar to the one of the tool. Tool-use was necessary to induce these effects, since a pointing task did not affect PPS and BR. These results show that a brief training with a tool induces plastic changes both to the perceived dimensions of the body part acting upon the tool and to the space around it, suggesting a strong overlap between peripersonal space and body representation.
Dedicated neural systems represent the space surrounding the body, termed Peripersonal space (PPS), by integrating visual or auditory stimuli occurring near the body with somatosensory information. As a behavioral proxy to PPS, we measured participants’ reaction time to tactile stimulation while task-irrelevant auditory or visual stimuli were presented at different distances from their body. In 7 experiments we delineated the critical distance at which auditory or visual stimuli boosted tactile processing on the hand, face, and trunk as a proxy of the PPS extension. Three main findings were obtained. First, the size of PPS varied according to the stimulated body part, being progressively bigger for the hand, then face, and largest for the trunk. Second, while approaching stimuli always modulated tactile processing in a space-dependent manner, receding stimuli did so only for the hand. Finally, the extension of PPS around the hand and the face varied according to their relative positioning and stimuli congruency, whereas the trunk PPS was constant. These results suggest that at least three body-part specific PPS representations exist, differing in extension and directional tuning. These distinct PPS representations, however, are not fully independent from each other, but referenced to the common reference frame of the trunk.
The space around the body, i.e., peripersonal space (PPS), is conceived as a multisensory-motor interface between body and environment. PPS is represented by frontoparietal neurons integrating tactile, visual, and auditory stimuli occurring near the body. PPS is plastic, because it extends by using a tool to reach far objects. Although interactions with others occur within PPS, little is known about how social environment modulates it. Here, we show that presence and interaction with others shape PPS representation. Participants performed a tactile detection task on their face while concurrent task-irrelevant sounds approached toward or receded from their face. Because a sound affects touch when occurring within PPS, we calculated the critical distance where sounds speeded up tactile reaction time as a proxy of PPS boundaries. Experiment 1 shows that PPS boundaries shrink when subjects face another individual, as compared to a mannequin, placed in far space. Experiment 2 and 3 show that, after playing an economic game with another person, PPS boundaries between self and other merge, but only if the other behaved cooperatively. These results reveal that PPS representation is sensitive to social modulation, showing a link between low-level sensorimotor processing and high-level social cognition.
Little is known about whether and how multimodal representations of the body (BRs) and of the space around the body (Peripersonal Space, PPS) adapt to amputation and prosthesis implantation. In order to investigate this issue, we tested BR in a group of upper limb amputees by means of a tactile distance perception task and PPS by means of an audio-tactile interaction task. Subjects performed the tasks with stimulation either on the healthy limb or the stump of the amputated limb, while wearing or not wearing their prosthesis. When patients performed the tasks on the amputated limb, without the prosthesis, the perception of arm length shrank, with a concurrent shift of PPS boundaries towards the stump. Conversely, wearing the prosthesis increased the perceived length of the stump and extended the PPS boundaries so as to include the prosthetic hand, such that the prosthesis partially replaced the missing limb.
A network of brain regions including the ventral premotor cortex (vPMc) and the posterior parietal cortex (PPc) is consistently recruited during processing of multisensory stimuli within peripersonal space (PPS). However, to date, information on the causal role of these fronto-parietal areas in multisensory PPS representation is lacking. Using low-frequency repetitive TMS (rTMS; 1 Hz), we induced transient virtual lesions to the left vPMc, PPc, and visual cortex (V1, control site) and tested whether rTMS affected audio-tactile interaction in the PPS around the hand. Subjects performed a timed response task to a tactile stimulus on their right (contralateral to rTMS) hand while concurrent task-irrelevant sounds were presented either close to the hand or 1 m far from the hand. When no rTMS was delivered, a sound close to the hand reduced RT-to-tactile targets as compared with when a far sound was presented. This space-dependent, auditory modulation of tactile perception was specific to a hand-centered reference frame. Such a specific form of multisensory interaction near the hand can be taken as a behavioral hallmark of PPS representation. Crucially, virtual lesions to vPMc and PPc, but not to V1, eliminated the speeding effect due to near sounds, showing a disruption of audio-tactile interactions around the hand. These findings indicate that multisensory interaction around the hand depends on the functions of vPMc and PPc, thus pointing to the necessity of this human fronto-parietal network in multisensory representation of PPS.
Stimuli from different sensory modalities occurring on or close to the body are integrated in a multisensory representation of the space surrounding the body, i.e., peripersonal space (PPS). PPS dynamically modifies depending on experience, e.g., it extends after using a tool to reach far objects. However, the neural mechanism underlying PPS plasticity after tool use is largely unknown. Here we use a combined computational-behavioral approach to propose and test a possible mechanism accounting for PPS extension. We first present a neural network model simulating audio-tactile representation in the PPS around one hand. Simulation experiments showed that our model reproduced the main property of PPS neurons, i.e., selective multisensory response for stimuli occurring close to the hand. We used the neural network model to simulate the effects of a tool-use training. In terms of sensory inputs, tool use was conceptualized as a concurrent tactile stimulation from the hand, due to holding the tool, and an auditory stimulation from the far space, due to tool-mediated action. Results showed that after exposure to those inputs, PPS neurons responded also to multisensory stimuli far from the hand. The model thus suggests that synchronous pairing of tactile hand stimulation and auditory stimulation from the far space is sufficient to extend PPS, such as after tool-use. Such prediction was confirmed by a behavioral experiment, where we used an audio-tactile interaction paradigm to measure the boundaries of PPS representation. We found that PPS extended after synchronous tactile-hand stimulation and auditory-far stimulation in a group of healthy volunteers. Control experiments both in simulation and behavioral settings showed that the same amount of tactile and auditory inputs administered out of synchrony did not change PPS representation. We conclude by proposing a simple, biological-plausible model to explain plasticity in PPS representation after tool-use, which is supported by computational and behavioral data.
Neuroprosthetics research in amputee patients aims at developing new prostheses that move and feel like real limbs. Targeted muscle and sensory reinnervation (TMSR) is such an approach and consists of rerouting motor and sensory nerves from the residual limb towards intact muscles and skin regions. Movement of the myoelectric prosthesis is enabled via decoded electromyography activity from reinnervated muscles and touch sensation on the missing limb is enabled by stimulation of the reinnervated skin areas. Here we ask whether and how motor control and redirected somatosensory stimulation provided via TMSR affected the maps of the upper limb in primary motor (M1) and primary somatosensory (S1) cortex, as well as their functional connections. To this aim, we tested three TMSR patients and investigated the extent, strength, and topographical organization of the missing limb and several control body regions in M1 and S1 at ultra high-field (7 T) functional magnetic resonance imaging. Additionally, we analysed the functional connectivity between M1 and S1 and of both these regions with fronto-parietal regions, known to be important for multisensory upper limb processing. These data were compared with those of control amputee patients (n = 6) and healthy controls (n = 12). We found that M1 maps of the amputated limb in TMSR patients were similar in terms of extent, strength, and topography to healthy controls and different from non-TMSR patients. S1 maps of TMSR patients were also more similar to normal conditions in terms of topographical organization and extent, as compared to non-targeted muscle and sensory reinnervation patients, but weaker in activation strength compared to healthy controls. Functional connectivity in TMSR patients between upper limb maps in M1 and S1 was comparable with healthy controls, while being reduced in non-TMSR patients. However, connectivity was reduced between S1 and fronto-parietal regions, in both the TMSR and non-TMSR patients with respect to healthy controls. This was associated with the absence of a well-established multisensory effect (visual enhancement of touch) in TMSR patients. Collectively, these results show how M1 and S1 process signals related to movement and touch are enabled by targeted muscle and sensory reinnervation. Moreover, they suggest that TMSR may counteract maladaptive cortical plasticity typically found after limb loss, in M1, partially in S1, and in their mutual connectivity. The lack of multisensory interaction in the present data suggests that further engineering advances are necessary (e.g. the integration of somatosensory feedback into current prostheses) to enable prostheses that move and feel as real limbs.
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