Tamar R. Makin

Is That Near My Hand? Multisensory Representation of Peripersonal Space in Human Intraparietal Sulcus

Our ability to interact with the immediate surroundings depends not only on an adequate representation of external space but also on our ability to represent the location of objects with respect to our own body and especially to our hands. Indeed, electrophysiological studies in monkeys revealed multimodal neurons with spatially corresponding tactile and visual receptive fields in a number of brain areas, suggesting a representation of visual peripersonal space with respect to the body. In this functional magnetic resonance imaging study, we localized areas in human intraparietal sulcus (IPS) and lateral occipital complex (LOC) that represent nearby visual space with respect to the hands (perihand space), by contrasting the response to a ball moving near-to versus far-from the hands. Furthermore, by independently manipulating sensory information about the hand, in the visual (using a dummy hand) and proprioceptive domains (by changing the unseen hand position), we determined the sensory contributions to the representation of hand-centered space. In the posterior IPS, the visual contribution was dominant, overriding proprioceptive information. Surprisingly, regions within LOC also displayed visually dominant, hand-related activation. In contrast, the anterior IPS was characterized by a proprioceptive representation of the hand, as well as showing tactile hand-specific activation, suggesting a homology with monkey parietal hand-centered areas. We therefore suggest that, whereas cortical regions within the posterior IPS and LOC represent hand-centered space in a predominantly visual manner, the anterior IPS uses multisensory information in representing perihand space.

Topographic Representation of the Human Body in the Occipitotemporal Cortex

Large-scale topographic representations of the body have long been established in the somatosensory and motor cortices. Using functional imaging, we identified a topographically organized body part map within the occipitotemporal cortex (OTC), with distinct clusters of voxels showing clear preference for different visually presented body parts. This representation was consistent both across hemispheres and participants. Using converging methods, the preference for specific body parts was demonstrated to be robust and did not merely reflect shape differences between the categories. Finally, execution of (unseen) movements with different body parts resulted in a limited topographic representation of the limbs and trunk, which partially overlapped with the visual body part map. This motor-driven activation in the OTC could not be explained solely by visual or motor imagery of the body parts. This suggests that visual and motor-related information converge within the OTC in a body part specific manner.

Phantom pain is associated with preserved structure and function in the former hand area

Phantom pain after arm amputation is widely believed to arise from maladaptive cortical reorganization, triggered by loss of sensory input. We instead propose that chronic phantom pain experience drives plasticity by maintaining local cortical representations and disrupting inter-regional connectivity. Here we show that, while loss of sensory input is generally characterized by structural and functional degeneration in the deprived sensorimotor cortex, the experience of persistent pain is associated with preserved structure and functional organization in the former hand area. Furthermore, consistent with the isolated nature of phantom experience, phantom pain is associated with reduced inter-regional functional connectivity in the primary sensorimotor cortex. We therefore propose that contrary to the maladaptive model, cortical plasticity associated with phantom pain is driven by powerful and long-lasting subjective sensory experience, such as triggered by nociceptive or top–down inputs. Our results prompt a revisiting of the link between phantom pain and brain organization.

Coding of Visual Space during Motor Preparation: Approaching Objects Rapidly Modulate Corticospinal Excitability in Hand-Centered Coordinates

Defensive behaviors, such as withdrawing your hand to avoid potentially harmful approaching objects, rely on rapid sensorimotor transformations between visual and motor coordinates. We examined the reference frame for coding visual information about objects approaching the hand during motor preparation. Subjects performed a simple visuomanual task while a task-irrelevant distractor ball rapidly approached a location either near to or far from their hand. After the distractor ball appearance, single pulses of transcranial magnetic stimulation were delivered over the subjects primary motor cortex, eliciting motor evoked potentials (MEPs) in their responding hand. MEP amplitude was reduced when the ball approached near the responding hand, both when the hand was on the left and the right of the midline. Strikingly, this suppression occurred very early, at 70–80 ms after ball appearance, and was not modified by visual fixation location. Furthermore, it was selective for approaching balls, since static visual distractors did not modulate MEP amplitude. Together with additional behavioral measurements, we provide converging evidence for automatic hand-centered coding of visual space in the human brain.

Reassessing cortical reorganization in the primary sensorimotor cortex following arm amputation

The brain’s ability to reorganise itself is key to our recovery from injuries, but the subsequent mismatch between old and new organisation may lead to pain. Makin et al. argue against this ‘maladaptive plasticity’ theory by showing that phantom pain in upper limb amputees is independent of cortical remapping.

Children’s Responses to the Rubber-Hand Illusion Reveal Dissociable Pathways in Body Representation

The bodily self is constructed from multisensory information. However, little is known of the relation between multisensory development and the emerging sense of self. We investigated this question by measuring the strength of the rubber-hand illusion in young children (4 to 9 years old) and adults. Intermanual pointing showed that children were as sensitive as adults to visual-tactile synchrony cues for hand position, which indicates that a visual-tactile pathway to the bodily self matures by at least 4 years of age. However, regardless of synchrony cues, children’s perceived hand position was closer to the rubber hand than adults’ perceived hand position was. This indicates a second, later-maturing process based on visual-proprioceptive information. Furthermore, explicit feelings of embodiment were related only to the visual-tactile process. These findings demonstrate two dissociable processes underlying body representation in early life, and they call into question current models of body representation and ownership in adulthood.

Deprivation-related and use-dependent plasticity go hand in hand

Arm-amputation involves two powerful drivers for brain plasticity—sensory deprivation and altered use. However, research has largely focused on sensory deprivation and maladaptive change. Here we show that adaptive patterns of limb usage after amputation drive cortical plasticity. We report that individuals with congenital or acquired limb-absence vary in whether they preferentially use their intact hand or residual arm in daily activities. Using fMRI, we show that the deprived sensorimotor cortex is employed by whichever limb individuals are over-using. Individuals from either group that rely more on their intact hands (and report less frequent residual arm usage) showed increased intact hand representation in the deprived cortex, and increased white matter fractional anisotropy underlying the deprived cortex, irrespective of the age at which deprivation occurred. Our results demonstrate how experience-driven plasticity in the human brain can transcend boundaries that have been thought to limit reorganisation after sensory deprivation in adults. DOI: http://dx.doi.org/10.7554/eLife.01273.001

Amputees “Neglect” the Space Near Their Missing Hand

The space within reach of our hands is the medium for reaching, grasping, and avoidance movements. Accordingly, visual information in this action space is organized in hand-centered coordinates (Graziano, Yap, & Gross, 1994; Makin, Holmes, Brozzoli, Rossetti, & Farne, 2009; Makin, Holmes, & Zohary, 2007), generating a common frame of reference for perception and action (Fogassi & Luppino, 2005; Graziano, 1999). We hypothesized that amputation of the hand, producing an asymmetry in action space, would cause permanent distortions in visuospatial perception. We hypothesized further that this visual distortion would be limited to near space, because hand actions are not possible in far space. We report here that amputation of a hand is indeed associated with a mild visual neglect of the amputated side: Participants with an amputated hand favored their intact side when comparing distances in a landmarkposition judgment task. Importantly, this bias was absent when the targets were placed in far space. Our results thus demonstrate that the possibility for action within near space shapes the actor’s spatial perception.

Unmasking Latent Inhibitory Connections in Human Cortex to Reveal Dormant Cortical Memories

Summary Balance of cortical excitation and inhibition (EI) is thought to be disrupted in several neuropsychiatric conditions, yet it is not clear how it is maintained in the healthy human brain. When EI balance is disturbed during learning and memory in animal models, it can be restabilized via formation of inhibitory replicas of newly formed excitatory connections. Here we assess evidence for such selective inhibitory rebalancing in humans. Using fMRI repetition suppression we measure newly formed cortical associations in the human brain. We show that expression of these associations reduces over time despite persistence in behavior, consistent with inhibitory rebalancing. To test this, we modulated excitation/inhibition balance with transcranial direct current stimulation (tDCS). Using ultra-high-field (7T) MRI and spectroscopy, we show that reducing GABA allows cortical associations to be re-expressed. This suggests that in humans associative memories are stored in balanced excitatory-inhibitory ensembles that lie dormant unless latent inhibitory connections are unmasked. Video Abstract

Revealing the neural fingerprints of a missing hand

The hand area of the primary somatosensory cortex contains detailed finger topography, thought to be shaped and maintained by daily life experience. Here we utilise phantom sensations and ultra high-field neuroimaging to uncover preserved, though latent, representation of amputees’ missing hand. We show that representation of the missing hand’s individual fingers persists in the primary somatosensory cortex even decades after arm amputation. By demonstrating stable topography despite amputation, our finding questions the extent to which continued sensory input is necessary to maintain organisation in sensory cortex, thereby reopening the question what happens to a cortical territory once its main input is lost. The discovery of persistent digit topography of amputees’ missing hand could be exploited for the development of intuitive and fine-grained control of neuroprosthetics, requiring neural signals of individual digits. DOI: http://dx.doi.org/10.7554/eLife.15292.001