Luigi Tamè

Spatial coding of touch at the fingers: Insights from double simultaneous stimulation within and between hands

We studied the effect of tactile double simultaneous stimulation (DSS) within and between hands to examine spatial coding of touch at the fingers. Participants performed a go/no-go task to detect a tactile stimulus delivered to one target finger (e.g., right index), stimulated alone or with a concurrent non-target finger, either on the same hand (e.g., right middle finger) or on the other hand (e.g., left index finger=homologous; left middle finger=non-homologous). Across blocks we also changed the unseen hands posture (both hands palm down, or one hand rotated palm-up). When both hands were palm-down DSS interference effects emerged both within and between hands, but only when the non-homologous finger served as non-target. This suggests a clear segregation between the fingers of each hand, regardless of finger side. By contrast, when one hand was palm-up interference effects emerged only within hand, whereas between hands DSS interference was considerably reduced or absent. Thus, between hands interference was clearly affected by changes in hands posture. Taken together, these findings provide behavioral evidence in humans for multiple spatial coding of touch during tactile DSS at the fingers. In particular, they confirm the existence of representational stages of touch that distinguish between body-regions more than body-sides. Moreover, they show that the availability of tactile stimulation side becomes prominent when postural update is required.

Microsaccades distinguish between global and local visual processing

Much is known about the functional mechanisms involved in visual search. Yet, the fundamental question of whether the visual system can perform different types of visual analysis at different spatial resolutions still remains unsettled. In the visual-attention literature, the distinction between different spatial scales of visual processing corresponds to the distinction between distributed and focused attention. Some authors have argued that singleton detection can be performed in distributed attention, whereas others suggest that even such a simple visual operation involves focused attention. Here we showed that microsaccades were spatially biased during singleton discrimination but not during singleton detection. The results provide support to the hypothesis that some coarse visual analysis can be performed in a distributed attention mode.

The contribution of primary and secondary somatosensory cortices to the representation of body parts and body sides: An fmri adaptation study

Although the somatosensory homunculus is a classically used description of the way somatosensory inputs are processed in the brain, the actual contributions of primary (SI) and secondary (SII) somatosensory cortices to the spatial coding of touch remain poorly understood. We studied adaptation of the fMRI BOLD response in the somatosensory cortex by delivering pairs of vibrotactile stimuli to the finger tips of the index and middle fingers. The first stimulus (adaptor) was delivered either to the index or to the middle finger of the right or left hand, and the second stimulus (test) was always administered to the left index finger. The overall BOLD response evoked by the stimulation was primarily contralateral in SI and was more bilateral in SII. However, our fMRI adaptation approach also revealed that both somatosensory cortices were sensitive to ipsilateral as well as to contralateral inputs. SI and SII adapted more after subsequent stimulation of homologous as compared with nonhomologous fingers, showing a distinction between different fingers. Most importantly, for both somatosensory cortices, this finger-specific adaptation occurred irrespective of whether the tactile stimulus was delivered to the same or to different hands. This result implies integration of contralateral and ipsilateral somatosensory inputs in SI as well as in SII. Our findings suggest that SI is more than a simple relay for sensory information and that both SI and SII contribute to the spatial coding of touch by discriminating between body parts (fingers) and by integrating the somatosensory input from the two sides of the body (hands).

Early Integration of Bilateral Touch in the Primary Somatosensory Cortex

Animal, as well as behavioural and neuroimaging studies in humans have documented integration of bilateral tactile information at the level of primary somatosensory cortex (SI). However, it is still debated whether integration in SI occurs early or late during tactile processing, and whether it is somatotopically organized. To address both the spatial and temporal aspects of bilateral tactile processing we used magnetoencephalography in a tactile repetition‐suppression paradigm. We examined somatosensory evoked‐responses produced by probe stimuli preceded by an adaptor, as a function of the relative position of adaptor and probe (probe always at the left index finger; adaptor at the index or middle finger of the left or right hand) and as a function of the delay between adaptor and probe (0, 25, or 125 ms). Percentage of response‐amplitude suppression was computed by comparing paired (adaptor + probe) with single stimulations of adaptor and probe. Results show that response suppression varies differentially in SI and SII as a function of both spatial and temporal features of the stimuli. Remarkably, repetition suppression of SI activity emerged early in time, regardless of whether the adaptor stimulus was presented on the same and the opposite body side with respect to the probe. These novel findings support the notion of an early and somatotopically organized inter‐hemispheric integration of tactile information in SI. Hum Brain Mapp 36:1506–1523, 2015.

Bilateral representations of touch in the primary somatosensory cortex

ABSTRACT According to current textbook knowledge, the primary somatosensory cortex (SI) supports unilateral tactile representations, whereas structures beyond SI, in particular the secondary somatosensory cortex (SII), support bilateral tactile representations. However, dexterous and well-coordinated bimanual motor tasks require early integration of bilateral tactile information. Sequential processing, first of unilateral and subsequently of bilateral sensory information, might not be sufficient to accomplish these tasks. This view of sequential processing in the somatosensory system might therefore be questioned, at least for demanding bimanual tasks. Evidence from the last 15 years is forcing a revision of this textbook notion. Studies in animals and humans indicate that SI is more than a simple relay for unilateral sensory information and, together with SII, contributes to the integration of somatosensory inputs from both sides of the body. Here, we review a series of recent works from our own and other laboratories in favour of interactions between tactile stimuli on the two sides of the body at early stages of processing. We focus on tactile processing, although a similar logic may also apply to other aspects of somatosensation. We begin by describing the basic anatomy and physiology of interhemispheric transfer, drawing on neurophysiological studies in animals and behavioural studies in humans that showed tactile interactions between body sides, both in healthy and in brain-damaged individuals. Then we describe the neural substrates of bilateral interactions in somatosensation as revealed by neurophysiological work in animals and neuroimaging studies in humans (i.e., functional magnetic resonance imaging, magnetoencephalography, and transcranial magnetic stimulation). Finally, we conclude with considerations on the dilemma of how efficiently integrating bilateral sensory information at early processing stages can coexist with more lateralized representations of somatosensory input, in the context of motor control.

Multimodal contributions to body representation

Our body is a unique entity by which we interact with the external world. Consequently, the way we represent our body has profound implications in the way we process and locate sensations and in turn perform appropriate actions. The body can be the subject, but also the object of our experience, providing information from sensations on the body surface and viscera, but also knowledge of the body as a physical object. However, the extent to which different senses contribute to constructing the rich and unified body representations we all experience remains unclear. In this review, we aim to bring together recent research showing important roles for several different sensory modalities in constructing body representations. At the same time, we hope to generate new ideas of how and at which level the senses contribute to generate the different levels of body representations and how they interact. We will present an overview of some of the most recent neuropsychological evidence about multisensory control of pain, and the way that visual, auditory, vestibular and tactile systems contribute to the creation of coherent representations of the body. We will focus particularly on some of the topics discussed in the symposium on Multimodal Contributions to Body Representation held on the 15th International Multisensory Research Forum (2015, Pisa, Italy).

Vision of the body and the differentiation of perceived body side in touch.

Although tactile representations of the two body sides are initially segregated into opposite hemispheres of the brain, behavioural interactions between body sides exist and can be revealed under conditions of tactile double simultaneous stimulation (DSS) at the hands. Here we examined to what extent vision can affect body side segregation in touch. To this aim, we changed hand-related visual input while participants performed a go/no-go task to detect a tactile stimulus delivered to one target finger (e.g., right index), stimulated alone or with a concurrent non-target finger either on the same hand (e.g., right middle finger) or on the other hand (e.g., left index finger=homologous; left middle finger=non-homologous). Across experiments, the two hands were visible or occluded from view (Experiment 1), images of the two hands were either merged using a morphing technique (Experiment 2), or were shown in a compatible vs incompatible position with respect to the actual posture (Experiment 3). Overall, the results showed reliable interference effects of DSS, as compared to target-only stimulation. This interference varied as a function of which non-target finger was stimulated, and emerged both within and between hands. These results imply that the competition between tactile events is not clearly segregated across body sides. Crucially, non-informative vision of the hand affected overall tactile performance only when a visual/proprioceptive conflict was present, while neither congruent nor morphed hand vision affected tactile DSS interference. This suggests that DSS operates at a tactile processing stage in which interactions between body sides can occur regardless of the available visual input from the body.

Top down influence on visuo-tactile interaction modulates neural oscillatory responses

Multisensory integration involves bottom-up as well as top-down processes. We investigated the influences of top-down control on the neural responses to multisensory stimulation using EEG recording and time-frequency analyses. Participants were stimulated at the index or thumb of the left hand, using tactile vibrators mounted on a foam cube. Simultaneously they received a visual distractor from a light emitting diode adjacent to the active vibrator (spatially congruent trial) or adjacent to the inactive vibrator (spatially incongruent trial). The task was to respond to the elevation of the tactile stimulus (upper or lower), while ignoring the simultaneous visual distractor. To manipulate top-down control on this multisensory stimulation, the proportion of spatially congruent (vs. incongruent) trials was changed across blocks. Our results reveal that the behavioral cost of responding to incongruent than congruent trials (i.e., the crossmodal congruency effect) was modulated by the proportion of congruent trials. Most importantly, the EEG gamma band response and the gamma-theta coupling were also affected by this modulation of top-down control, whereas the late theta band response related to the congruency effect was not. These findings suggest that gamma band response is more than a marker of multisensory binding, being also sensitive to the correspondence between expected and actual multisensory stimulation. By contrast, theta band response was affected by congruency but appears to be largely immune to stimulation expectancy.

Neural Correlates of Finger Gnosis

Neuropsychological studies have described patients with a selective impairment of finger identification in association with posterior parietal lesions. However, evidence of the role of these areas in finger gnosis from studies of the healthy human brain is still scarce. Here we used functional magnetic resonance imaging to identify the brain network engaged in a novel finger gnosis task, the intermanual in-between task (IIBT), in healthy participants. Several brain regions exhibited a stronger blood oxygenation level-dependent (BOLD) response in IIBT than in a control task that did not explicitly rely on finger gnosis but used identical stimuli and motor responses as the IIBT. The IIBT involved stronger signal in the left inferior parietal lobule (IPL), bilateral precuneus (PCN), bilateral premotor cortex, and left inferior frontal gyrus. In all regions, stimulation of nonhomologous fingers of the two hands elicited higher BOLD signal than stimulation of homologous fingers. Only in the left anteromedial IPL (a-mIPL) and left PCN did signal strength decrease parametrically from nonhomology, through partial homology, to total homology with stimulation delivered synchronously to the two hands. With asynchronous stimulation, the signal was stronger in the left a-mIPL than in any other region, possibly indicating retention of task-relevant information. We suggest that the left PCN may contribute a supporting visuospatial representation via its functional connection to the right PCN. The a-mIPL may instead provide the core substrate of an explicit bilateral body structure representation for the fingers that when disrupted can produce the typical symptoms of finger agnosia.

Within, but not between hands interactions in vibrotactile detection thresholds reflect somatosensory receptive field organization.

Detection of a tactile stimulus on one finger is impaired when a concurrent stimulus (masker) is presented on an additional finger of the same or the opposite hand. This phenomenon is known to be finger-specific at the within-hand level. However, whether this specificity is also maintained at the between hand level is not known. In four experiments, we addressed this issue by combining a Bayesian adaptive staircase procedure quick estimation of threshold (QUEST) with a two-interval forced choice (2IFC) design in order to establish threshold for detecting 200 ms, 100 Hz sinusoidal vibrations applied to the index or little fingertip of either hand (targets). We systematically varied the masker finger (index, middle, ring, or little finger of either hand), while controlling the spatial location of the target and masker stimuli. Detection thresholds varied consistently as a function of the masker finger when the latter was on the same hand (Experiments 1 and 2), but not when on different hands (Experiments 3 and 4). Within the hand, detection thresholds increased for masker fingers closest to the target finger (i.e., middle > ring when the target was index). Between the hands, detection thresholds were higher only when the masker was present on any finger as compared to when the target was presented in isolation. The within hand effect of masker finger is consistent with the segregation of different fingers at the early stages of somatosensory processing, from the periphery to the primary somatosensory cortex (SI). We propose that detection is finger-specific and reflects the organization of somatosensory receptive fields in SI within, but not between the hands.