Dissociating between object affordances and spatial compatibility effects using early response components

Perception and action are tightly linked: objects may be perceived not only in terms of visual features, but also in terms of possibilities for action. Previous studies showed that when a centrally located object has a salient graspable feature (e.g., a handle), it facilitates motor responses corresponding with the feature's position. However, such so-called affordance effects have been criticized as resulting from spatial compatibility effects, due to the visual asymmetry created by the graspable feature, irrespective of any affordances. In order to dissociate between affordance and spatial compatibility effects, we asked participants to perform a simple reaction-time task to typically graspable and non-graspable objects with similar visual features (e.g., lollipop and stop sign). Responses were measured using either electromyography (EMG) on proximal arm muscles during reaching-like movements, or with finger key-presses. In both EMG and button press measurements, participants responded faster when the object was either presented in the same location as the responding hand, or was affordable, resulting in significant and independent spatial compatibility and affordance effects, but no interaction. Furthermore, while the spatial compatibility effect was present from the earliest stages of movement preparation and throughout the different stages of movement execution, the affordance effect was restricted to the early stages of movement execution. Finally, we tested a small group of unilateral arm amputees using EMG, and found residual spatial compatibility but no affordance, suggesting that spatial compatibility effects do not necessarily rely on individuals’ available affordances. Our results show dissociation between affordance and spatial compatibility effects, and suggest that rather than evoking the specific motor action most suitable for interaction with the viewed object, graspable objects prompt the motor system in a general, body-part independent fashio

Brain (re)organisation following amputation:implications for phantom limb pain

Following arm amputation the region that represented the missing hand in primary somatosensory cortex (S1) becomes deprived of its primary input, resulting in changed boundaries of the S1 body map. This remapping process has been termed ‘reorganisation’ and has been attributed to multiple mechanisms, including increased expression of previously masked inputs. In a maladaptive plasticity model, such reorganisation has been associated with phantom limb pain (PLP). Brain activity associated with phantom hand movements is also correlated with PLP, suggesting that preserved limb functional representation may serve as a complementary process. Here we review some of the most recent evidence for the potential drivers and consequences of brain (re)organisation following amputation, based on human neuroimaging. We emphasise other perceptual and behavioural factors consequential to arm amputation, such as non-painful phantom sensations, perceived limb ownership, intact hand compensatory behaviour or prosthesis use, which have also been related to both cortical changes and PLP. We also discuss new findings based on interventions designed to alter the brain representation of the phantom limb, including augmented/virtual reality applications and brain computer interfaces. These studies point to a close interaction of sensory changes and alterations in brain regions involved in body representation, pain processing and motor control. Finally, we review recent evidence based on methodological advances such as high field neuroimaging and multivariate techniques that provide new opportunities to interrogate somatosensory representations in the missing hand cortical territory. Collectively, this research highlights the need to consider potential contributions of additional brain mechanisms, beyond S1 remapping, and the dynamic interplay of contextual factors with brain changes for understanding and alleviating PLP

Peripersonal space: a multisensory interface for body-object interactions

Research in the last four decades has brought a considerable advance in our understanding of how the brain synthesizes information arising from different sensory modalities. Indeed, many cortical and subcortical areas, beyond those traditionally considered to be ‘associative,’ have been shown to be involved in multisensory interaction and integration (Ghazanfar and Schroeder 2006). Visuo-tactile interaction is of particular interest, because of the prominent role played by vision in guiding our actions and anticipating their tactile consequences in everyday life. In this chapter, we focus on the functional role that visuo-tactile processing may play in driving two types of body-object interactions: avoidance and approach. We will first review some basic features of visuo-tactile interactions, as revealed by electrophysiological studies in monkeys. These will prove to be relevant for interpreting the subsequent evidence arising from human studies. A crucial point that will be stressed is that these visuo-tactile mechanisms have not only sensory, but also motor-related activity that qualifies them as multisensory-motor interfaces. Evidence will then be presented for the existence of functionally homologous processing in the human brain, both from neuropsychological research in brain-damaged patients and in healthy participants. The final part of the chapter will focus on some recent studies in humans showing that the human motor system is provided with a multisensory interface that allows for continuous monitoring of the space near the body (i.e., peripersonal space). We further demonstrate that multisensory processing can be modulated on-line as a consequence of interacting with objects. This indicates that, far from being passive, the monitoring of peripersonal space is an active process subserving actions between our body and objects located in the space around us

Making sense of phantom limb pain

Phantom limb pain (PLP) impacts the majority of individuals who undergo limb amputation. The PLP experience is highly heterogenous in its quality, intensity, frequency and severity. This heterogeneity, combined with the low prevalence of amputation in the general population, has made it difficult to accumulate reliable data on PLP. Consequently, we lack consensus on PLP mechanisms, as well as effective treatment options. However, the wealth of new PLP research, over the past decade, provides a unique opportunity to re-evaluate some of the core assumptions underlying what we know about PLP and the rationale behind PLP treatments. The goal of this review is to help generate consensus in the field on how best to research PLP, from phenomenology to treatment. We highlight conceptual and methodological challenges in studying PLP, which have hindered progress on the topic and spawned disagreement in the field, and offer potential solutions to overcome these challenges. Our hope is that a constructive evaluation of the foundational knowledge underlying PLP research practices will enable more informed decisions when testing the efficacy of existing interventions and will guide the development of the next generation of PLP treatments

Lifelong learning of cognitive styles for physical problem-solving: The effect of embodied experience

‘Embodied cognition’ suggests that our bodily experiences broadly shape our cognitive capabilities. We study how embodied experience affects the abstract physical problem-solving styles people use in a virtual task where embodiment does not affect action capabilities. We compare how groups with different embodied experience – 25 children and 35 adults with congenital limb differences versus 45 children and 40 adults born with two hands – perform this task, and find that while there is no difference in overall competence, the groups use different cognitive styles to find solutions. People born with limb differences think more before acting but take fewer attempts to reach solutions. Conversely, development affects the particular actions children use, as well as their persistence with their current strategy. Our findings suggest that while development alters action choices and persistence, differences in embodied experience drive changes in the acquisition of cognitive styles for balancing acting with thinking

Normalisation of brain connectivity through compensatory behaviour, despite congenital hand absence

Previously we showed, using task-evoked fMRI, that compensatory intact hand usage after amputation facilitates remapping of limb representations in the cortical territory of the missing hand (Makin et al., 2013a). Here we show that compensatory arm usage in individuals born without a hand (one-handers) reflects functional connectivity of spontaneous brain activity in the cortical hand region. Compared with two-handed controls, one-handers showed reduced symmetry of hand region inter-hemispheric resting-state functional connectivity and corticospinal white matter microstructure. Nevertheless, those one-handers who more frequently use their residual (handless) arm for typically bimanual daily tasks also showed more symmetrical functional connectivity of the hand region, demonstrating that adaptive behaviour drives long-range brain organisation. We therefore suggest that compensatory arm usage maintains symmetrical sensorimotor functional connectivity in one-handers. Since variability in spontaneous functional connectivity in our study reflects ecological behaviour, we propose that inter-hemispheric symmetry, typically observed in resting sensorimotor networks, depends on coordinated motor behaviour in daily life

Network-level reorganisation of functional connectivity following arm amputation

AbstractOne of the most striking demonstrations of plasticity in the adult human brain follows peripheral injury, such as amputation. In the primary sensorimotor cortex, arm amputation results in massive local remapping of the missing hands' cortical territory. However, little is known about the consequences of sensorimotor deprivation on global brain organisation. Here, we used resting-state fMRI to identify large-scale reorganisation beyond the primary sensorimotor cortex in arm amputees, compared with two-handed controls. Specifically, we characterised changes in functional connectivity between the cortical territory of the missing hand in the primary sensorimotor cortex (‘missing hand cortex’) and two networks of interest: the sensorimotor network, which is typically strongly associated with the hand cortex, and the default mode network (DMN), which is normally dissociated from it. Functional connectivity values between the missing hand cortex and the sensorimotor network were reduced in amputees, and connectivity was weaker in individuals amputated for longer periods. Lower levels of functional coupling between the missing hand cortex and the sensorimotor network were also associated with emerged coupling of this cortex with the DMN. Our results demonstrate that plasticity following arm amputation is not restricted to local remapping occurring within the sensorimotor homunculus of the missing hand but rather produces a cascade of cortical reorganisation at a network-level scale. These findings may provide a new framework for understanding how local deprivation following amputation could elicit complex perceptual experiences of phantom sensations, such as phantom pain

Perceptually relevant remapping of human somatotopy in 24 hours

Experience-dependent reorganisation of functional maps in the cerebral cortex is well described in the primary sensory cortices. However, there is relatively little evidence for such cortical reorganisation over the short-term. Using human somatosensory cortex as a model, we investigated the effects of a 24 hr gluing manipulation in which the right index and right middle fingers (digits 2 and 3) were adjoined with surgical glue. Somatotopic representations, assessed with two 7 tesla fMRI protocols, revealed rapid off-target reorganisation in the non-manipulated fingers following gluing, with the representation of the ring finger (digit 4) shifted towards the little finger (digit 5) and away from the middle finger (digit 3). These shifts were also evident in two behavioural tasks conducted in an independent cohort, showing reduced sensitivity for discriminating the temporal order of stimuli to the ring and little fingers, and increased substitution errors across this pair on a speeded reaction time task

Obtaining and maintaining cortical hand representation as evidenced from acquired and congenital handlessness

© Lukinova et al. A key question in neuroscience is how cortical organisation relates to experience. Previously we showed that amputees experiencing highly vivid phantom sensations maintain cortical representation of their missing hand (Kikkert et al., 2016). Here, we examined the role of sensory hand experience on persistent hand representation by studying individuals with acquired and congenital hand loss. We used representational similarity analysis in primary somatosensory and motor cortex during missing and intact hand movements. We found that key aspects of acquired amputees’ missing hand representation persisted, despite varying vividness of phantom sensations. In contrast, missing hand representation of congenital one-handers, who do not experience phantom sensations, was significantly reduced. Across acquired amputees, individuals’ reported motor control over their phantom hand positively correlated with the extent to which their somatosensory hand representation was normally organised. We conclude that once cortical organisation is formed, it is remarkably persistent, despite long-term attenuation of peripheral signals

Adaptable Categorization of Hands and Tools in Prosthesis Users.

Some theories propose that tools become incorporated into the neural representation of the hands (a process known as tool embodiment; Maravita & Iriki, 2004). Others suggest that conceptual body representation is rigid and that experience with one’s own body is insufficient for adapting bodily cognition, as shown in individuals born without hands (Vannuscorps & Caramazza, 2016) and in amputees with persistent phantom hand representation (Kikkert et al., 2016). How sharp is the conceptual boundary between hands and tools? This question is particularly relevant for individuals who have lost one hand and use prosthetic hands as tools to supplement their missing hand function. Although both congenital one-handers (i.e., amelia patients) and one-handed amputees are encouraged to use prostheses, the former show a greater tendency than the latter to use prosthetic hands in daily tasks (Jang et al., 2011). One-handers have a fully functional remaining hand (allowing them to use handheld tools, etc.), which makes them less likely to show semantic distortions in hand and tool representation. However, their bodies and their interactions with their environment are fundamentally altered by their disability (Makin et al., 2013; Makin, Wilf, Schwartz, & Zohary, 2010). To determine how real-world experience shapes conceptual categorization of hands, tools, and prostheses, we recruited one-handers with congenital or acquired unilateral hand loss to take part in a study involving a priming task. We predicted that one-handers, particularly congenital one-handers, would show more conceptual blurring between hands and tools than control participants would, as a result of less experience with a hand and more reliance on prostheses (which are essentially tools) for typical hand functions. We further predicted that individual differences in prosthesis usage would be reflected in implicit categorization of hands, manual tools, and prostheses