RESUMEN
Mammals use glabrous (hairless) skin of their hands and feet to navigate and manipulate their environment. Cortical maps of the body surface across species contain disproportionately large numbers of neurons dedicated to glabrous skin sensation, in part reflecting a higher density of mechanoreceptors that innervate these skin regions. Here, we find that disproportionate representation of glabrous skin emerges over postnatal development at the first synapse between peripheral mechanoreceptors and their central targets in the brainstem. Mechanoreceptor synapses undergo developmental refinement that depends on proximity of their terminals to glabrous skin, such that those innervating glabrous skin make synaptic connections that expand their central representation. In mice incapable of sensing gentle touch, mechanoreceptors innervating glabrous skin still make more powerful synapses in the brainstem. We propose that the skin region a mechanoreceptor innervates controls the developmental refinement of its central synapses to shape the representation of touch in the brain.
Asunto(s)
Tronco Encefálico/metabolismo , Mecanorreceptores/metabolismo , Sinapsis/metabolismo , Percepción del Tacto/fisiología , Potenciales de Acción/fisiología , Animales , Animales Recién Nacidos , Axones/metabolismo , Canales Iónicos/metabolismo , Ratones Noqueados , Neuronas/metabolismo , Imagen Óptica , Optogenética , Piel/inervaciónRESUMEN
Paralyzed muscles can be reanimated following spinal cord injury (SCI) using a brain-computer interface (BCI) to enhance motor function alone. Importantly, the sense of touch is a key component of motor function. Here, we demonstrate that a human participant with a clinically complete SCI can use a BCI to simultaneously reanimate both motor function and the sense of touch, leveraging residual touch signaling from his own hand. In the primary motor cortex (M1), residual subperceptual hand touch signals are simultaneously demultiplexed from ongoing efferent motor intention, enabling intracortically controlled closed-loop sensory feedback. Using the closed-loop demultiplexing BCI almost fully restored the ability to detect object touch and significantly improved several sensorimotor functions. Afferent grip-intensity levels are also decoded from M1, enabling grip reanimation regulated by touch signaling. These results demonstrate that subperceptual neural signals can be decoded from the cortex and transformed into conscious perception, significantly augmenting function.
Asunto(s)
Retroalimentación Sensorial/fisiología , Percepción del Tacto/fisiología , Tacto/fisiología , Adulto , Interfaces Cerebro-Computador/psicología , Mano/fisiopatología , Fuerza de la Mano/fisiología , Humanos , Masculino , Corteza Motora/fisiología , Movimiento/fisiología , Traumatismos de la Médula Espinal/fisiopatologíaRESUMEN
Advances in our understanding of brain function, along with the development of neural interfaces that allow for the monitoring and activation of neurons, have paved the way for brain-machine interfaces (BMIs), which harness neural signals to reanimate the limbs via electrical activation of the muscles or to control extracorporeal devices, thereby bypassing the muscles and senses altogether. BMIs consist of reading out motor intent from the neuronal responses monitored in motor regions of the brain and executing intended movements with bionic limbs, reanimated limbs, or exoskeletons. BMIs also allow for the restoration of the sense of touch by electrically activating neurons in somatosensory regions of the brain, thereby evoking vivid tactile sensations and conveying feedback about object interactions. In this review, we discuss the neural mechanisms of motor control and somatosensation in able-bodied individuals and describe approaches to use neuronal responses as control signals for movement restoration and to activate residual sensory pathways to restore touch. Although the focus of the review is on intracortical approaches, we also describe alternative signal sources for control and noninvasive strategies for sensory restoration.
Asunto(s)
Biónica , Interfaces Cerebro-Computador , Retroalimentación Sensorial/fisiología , Mano/fisiología , Movimiento/fisiología , Animales , Encéfalo/fisiología , Humanos , Percepción del Tacto/fisiologíaRESUMEN
Temperature is a fundamental sensory modality separate from touch, with dedicated receptor channels and primary afferent neurons for cool and warm1-3. Unlike for other modalities, however, the cortical encoding of temperature remains unknown, with very few cortical neurons reported that respond to non-painful temperature, and the presence of a 'thermal cortex' is debated4-8. Here, using widefield and two-photon calcium imaging in the mouse forepaw system, we identify cortical neurons that respond to cooling and/or warming with distinct spatial and temporal response properties. We observed a representation of cool, but not warm, in the primary somatosensory cortex, but cool and warm in the posterior insular cortex (pIC). The representation of thermal information in pIC is robust and somatotopically arranged, and reversible manipulations show a profound impact on thermal perception. Despite being positioned along the same one-dimensional sensory axis, the encoding of cool and that of warm are distinct, both in highly and broadly tuned neurons. Together, our results show that pIC contains the primary cortical representation of skin temperature and may help explain how the thermal system generates sensations of cool and warm.
Asunto(s)
Corteza Insular , Neuronas , Temperatura Cutánea , Corteza Somatosensorial , Animales , Ratones , Frío , Neuronas/fisiología , Corteza Somatosensorial/citología , Corteza Somatosensorial/fisiología , Percepción del Tacto/fisiología , Calor , Temperatura Cutánea/fisiología , Análisis Espacio-Temporal , Corteza Insular/citología , Corteza Insular/fisiologíaRESUMEN
Affective touch-a slow, gentle, and pleasant form of touch-activates a different neural network than which is activated during discriminative touch in humans. Affective touch perception is enabled by specialized low-threshold mechanoreceptors in the skin with unmyelinated fibers called C tactile (CT) afferents. These CT afferents are conserved across mammalian species, including macaque monkeys. However, it is unknown whether the neural representation of affective touch is the same across species and whether affective touch's capacity to activate the hubs of the brain that compute socioaffective information requires conscious perception. Here, we used functional MRI to assess the preferential activation of neural hubs by slow (affective) vs. fast (discriminative) touch in anesthetized rhesus monkeys (Macaca mulatta). The insula, anterior cingulate cortex (ACC), amygdala, and secondary somatosensory cortex were all significantly more active during slow touch relative to fast touch, suggesting homologous activation of the interoceptive-allostatic network across primate species during affective touch. Further, we found that neural responses to affective vs. discriminative touch in the insula and ACC (the primary cortical hubs for interoceptive processing) changed significantly with age. Insula and ACC in younger animals differentiated between slow and fast touch, while activity was comparable between conditions for aged monkeys (equivalent to >70 y in humans). These results, together with prior studies establishing conserved peripheral nervous system mechanisms of affective touch transduction, suggest that neural responses to affective touch are evolutionarily conserved in monkeys, significantly impacted in old age, and do not necessitate conscious experience of touch.
Asunto(s)
Estado de Conciencia , Macaca mulatta , Imagen por Resonancia Magnética , Percepción del Tacto , Animales , Estado de Conciencia/fisiología , Percepción del Tacto/fisiología , Masculino , Tacto/fisiología , Evolución Biológica , Corteza Somatosensorial/fisiología , Encéfalo/fisiología , Envejecimiento/fisiología , Femenino , Giro del Cíngulo/fisiologíaRESUMEN
The hand endows us with unparalleled precision and versatility in our interactions with objects, from mundane activities such as grasping to extraordinary ones such as virtuoso pianism. The complex anatomy of the human hand combined with expansive and specialized neuronal control circuits allows a wide range of precise manual behaviours. To support these behaviours, an exquisite sensory apparatus, spanning the modalities of touch and proprioception, conveys detailed and timely information about our interactions with objects and about the objects themselves. The study of manual dexterity provides a unique lens into the sensorimotor mechanisms that endow the nervous system with the ability to flexibly generate complex behaviour.
Asunto(s)
Mano/anatomía & histología , Mano/fisiología , Destreza Motora/fisiología , Humanos , Propiocepción/fisiología , Percepción del Tacto/fisiologíaRESUMEN
We can sense an object's shape by vision or touch. Previous studies suggested that the inferolateral occipitotemporal cortex (ILOTC) implements supramodal shape representations as it responds more to seeing or touching objects than shapeless textures. However, such activation in the anterior portion of the ventral visual pathway could be due to the conceptual representation of an object or visual imagery triggered by touching an object. We addressed these possibilities by directly comparing shape and conceptual representations of objects in early blind (who lack visual experience/imagery) and sighted participants. We found that bilateral ILOTC in both groups showed stronger activation during a shape verification task than during a conceptual verification task made on the names of the same manmade objects. Moreover, the distributed activity in the ILOTC encoded shape similarity but not conceptual association among objects. Besides the ILOTC, we also found shape representation in both groups' bilateral ventral premotor cortices and intraparietal sulcus (IPS), a frontoparietal circuit relating to object grasping and haptic processing. In contrast, the conceptual verification task activated both groups' left perisylvian brain network relating to language processing and, interestingly, the cuneus in early blind participants only. The ILOTC had stronger functional connectivity to the frontoparietal circuit than to the left perisylvian network, forming a modular structure specialized in shape representation. Our results conclusively support that the ILOTC selectively implements shape representation independently of visual experience, and this unique functionality likely comes from its privileged connection to the frontoparietal haptic circuit.
Asunto(s)
Corteza Cerebral , Percepción del Tacto , Humanos , Lóbulo Occipital , Percepción del Tacto/fisiología , Tacto/fisiología , Lóbulo Parietal/fisiología , Ceguera , Imagen por Resonancia Magnética/métodos , Mapeo EncefálicoRESUMEN
Adaptive behaviour crucially depends on flexible decision-making, which in mammals relies on the frontal cortex, specifically the orbitofrontal cortex (OFC)1-9. How OFC encodes decision variables and instructs sensory areas to guide adaptive behaviour are key open questions. Here we developed a reversal learning task for head-fixed mice, monitored the activity of neurons of the lateral OFC using two-photon calcium imaging and investigated how OFC dynamically interacts with primary somatosensory cortex (S1). Mice learned to discriminate 'go' from 'no-go' tactile stimuli10,11 and adapt their behaviour upon reversal of stimulus-reward contingency ('rule switch'). Imaging individual neurons longitudinally across all behavioural phases revealed a distinct engagement of S1 and lateral OFC, with S1 neural activity reflecting initial task learning, whereas lateral OFC neurons responded saliently and transiently to the rule switch. We identified direct long-range projections from lateral OFC to S1 that can feed this activity back to S1 as value prediction error. This top-down signal updated sensory representations in S1 by functionally remapping responses in a subpopulation of neurons that was sensitive to reward history. Functional remapping crucially depended on top-down feedback as chemogenetic silencing of lateral OFC neurons disrupted reversal learning, as well as plasticity in S1. The dynamic interaction of lateral OFC with sensory cortex thus implements computations critical for value prediction that are history dependent and error based, providing plasticity essential for flexible decision-making.
Asunto(s)
Plasticidad Neuronal/fisiología , Corteza Prefrontal/citología , Corteza Prefrontal/fisiología , Aprendizaje Inverso/fisiología , Corteza Somatosensorial/citología , Corteza Somatosensorial/fisiología , Percepción del Tacto/fisiología , Adaptación Psicológica , Animales , Mapeo Encefálico , Señalización del Calcio , Toma de Decisiones/fisiología , Discriminación en Psicología/fisiología , Masculino , Ratones , Estimulación Física , Células Receptoras Sensoriales/metabolismoRESUMEN
In the study of bodily awareness, the predictive coding theory has revealed that our brain continuously modulates sensory experiences to integrate them into a unitary body representation. Indeed, during multisensory illusions (e.g., the rubber hand illusion, RHI), the synchronous stroking of the participant's concealed hand and a fake visible one creates a visuotactile conflict, generating a prediction error. Within the predictive coding framework, through sensory processing modulation, prediction errors are solved, inducing participants to feel as if touches originated from the fake hand, thus ascribing the fake hand to their own body. Here, we aimed to address sensory processing modulation under multisensory conflict, by disentangling somatosensory and visual stimuli processing that are intrinsically associated during the illusion induction. To this aim, we designed two EEG experiments, in which somatosensory- (SEPs; Experiment 1; N = 18; F = 10) and visual-evoked potentials (VEPs; Experiment 2; N = 18; F = 9) were recorded in human males and females following the RHI. Our results show that, in both experiments, ERP amplitude is significantly modulated in the illusion as compared with both control and baseline conditions, with a modality-dependent diametrical pattern showing decreased SEP amplitude and increased VEP amplitude. Importantly, both somatosensory and visual modulations occur in long-latency time windows previously associated with tactile and visual awareness, thus explaining the illusion of perceiving touch at the sight location. In conclusion, we describe a diametrical modulation of somatosensory and visual processing as the neural mechanism that allows maintaining a stable body representation, by restoring visuotactile congruency under the occurrence of multisensory conflicts.
Asunto(s)
Electroencefalografía , Potenciales Evocados Somatosensoriales , Potenciales Evocados Visuales , Ilusiones , Percepción Visual , Humanos , Masculino , Femenino , Adulto , Percepción Visual/fisiología , Potenciales Evocados Somatosensoriales/fisiología , Adulto Joven , Ilusiones/fisiología , Potenciales Evocados Visuales/fisiología , Percepción del Tacto/fisiología , Estimulación Luminosa/métodos , Conflicto Psicológico , Corteza Somatosensorial/fisiología , Imagen CorporalRESUMEN
Millisecond-scale temporal spiking patterns encode sensory information in the periphery, but their role in the neocortex remains controversial. The sense of touch provides a window into temporal coding because tactile neurons often exhibit precise, repeatable, and informative temporal spiking patterns. In the somatosensory cortex (S1), responses to skin vibrations exhibit phase locking that faithfully carries information about vibratory frequency. However, the respective roles of spike timing and rate in frequency coding are confounded because vibratory frequency shapes both the timing and rates of responses. To disentangle the contributions of these two neural features, we measured S1 responses as rhesus macaques performed frequency discrimination tasks in which differences in frequency were accompanied by orthogonal variations in amplitude. We assessed the degree to which the strength and timing of responses could account for animal performance. First, we showed that animals can discriminate frequency, but their performance is biased by amplitude variations. Second, rate-based representations of frequency are susceptible to changes in amplitude but in ways that are inconsistent with the animals' behavioral biases, calling into question a rate-based neural code for frequency. In contrast, timing-based representations are highly informative about frequency but impervious to changes in amplitude, which is also inconsistent with the animals' behavior. We account for the animals' behavior with a model wherein frequency coding relies on a temporal code, but frequency judgments are biased by perceived magnitude. We conclude that information about vibratory frequency is not encoded in S1 firing rates but primarily in temporal patterning on millisecond timescales.
Asunto(s)
Macaca mulatta , Corteza Somatosensorial , Vibración , Animales , Corteza Somatosensorial/fisiología , Masculino , Potenciales de Acción/fisiología , Factores de Tiempo , Estimulación Física , Tacto/fisiología , Discriminación en Psicología/fisiología , Percepción del Tacto/fisiología , Neuronas/fisiología , Tiempo de Reacción/fisiología , FemeninoRESUMEN
The spatial coding of tactile information is functionally essential for touch-based shape perception and motor control. However, the spatiotemporal dynamics of how tactile information is remapped from the somatotopic reference frame in the primary somatosensory cortex to the spatiotopic reference frame remains unclear. This study investigated how hand position in space or posture influences cortical somatosensory processing. Twenty-two healthy subjects received electrical stimulation to the right thumb (D1) or little finger (D5) in three position conditions: palm down on right side of the body (baseline), hand crossing the body midline (effect of position), and palm up (effect of posture). Somatosensory-evoked potentials (SEPs) were recorded using electroencephalography. One early-, two mid-, and two late-latency neurophysiological components were identified for both fingers: P50, P1, N125, P200, and N250. D1 and D5 showed different cortical activation patterns: compared with baseline, the crossing condition showed significant clustering at P1 for D1, and at P50 and N125 for D5; the change in posture showed a significant cluster at N125 for D5. Clusters predominated at centro-parietal electrodes. These results suggest that tactile remapping of fingers after electrical stimulation occurs around 100-125 ms in the parietal cortex.
Asunto(s)
Percepción del Tacto , Tacto , Humanos , Tacto/fisiología , Dedos/fisiología , Percepción del Tacto/fisiología , Mano/fisiología , Electroencefalografía , Corteza SomatosensorialRESUMEN
The human body is represented in a topographic pattern in the primary somatosensory cortex (S1), and genital representation is displaced below the toe representation. However, the relationship between the representation of the genitals and toe in S1 remains unclear. In this study, tactile stimulation was applied to the big toe in healthy subjects to observe changes in tactile acuity in the unstimulated genital area, abdomen, and metacarpal dorsal. Then tactile stimulation was applied to the right abdomen and metacarpal dorsal to observe changes in tactile acuity in bilateral genitals. The results revealed that tactile stimulation of the big toe led to a reduction in the 2-point discrimination threshold (2PDT) not only in the stimulated big toe but also in the bilateral unstimulated genitals, whereas the bilateral abdomen and metacarpal dorsal threshold remained unchanged. On the other hand, tactile stimulation of the abdomen and metacarpal dorsal did not elicit 2-point discrimination threshold changes in the bilateral genitals. Cortical and subcortical mechanisms have been proposed to account for the findings. One explanation involves the intracortical interaction between 2 adjacent representations. Another possible explanation is that the information content of a specific body part is broadly distributed across the S1. Moreover, exploring the links between human behaviors and changes in the cerebral cortex is of significant importance.
Asunto(s)
Corteza Somatosensorial , Percepción del Tacto , Humanos , Corteza Somatosensorial/fisiología , Percepción del Tacto/fisiología , Tacto/fisiología , Corteza Cerebral , Dedos del PieRESUMEN
Fine sensory modalities play an essential role in perceiving the world. However, little is known about how the cortico-cortical distinguishes between dynamic and static tactile signals. This study investigated oscillatory connectivity during a tactile discrimination task of dynamic and static stimulation via electroencephalogram (EEG) recordings and the fast oscillatory networks across widespread cortical regions. While undergoing EEG recordings, the subject felt an electro-tactile presented by a 3-dot array. Each block consisted of 3 forms of stimulation: Spatio-temporal (dynamic), Spatial (static), and Control condition (lack of electrical stimulation). The average event-related potential for the Spatial and Spatio-temporal conditions exhibited statistically significant differences between 25 and 75, 81 and 121, 174 and 204 and 459 and 489 ms after stimulus onset. Based on those times, the sLORETA approach was used to reconstruct the inverse solutions of EEG. Source localization appeared superior parietal at around 25 to 75 ms, in the primary motor cortex at 81 to 121 ms, in the central prefrontal cortex at 174 to 204 and 459 to 489 ms. To better assess spectral brain functional connectivity, we selected frequency ranges with correspondingly significant differences: for static tactile stimulation, these are concentrated in the Theta, Alpha, and Gamma bands, whereas for dynamic stimulation, the relative energy change bands are focused on the Theta and Alpha bands. These nodes' functional connectivity analysis (phase lag index) showed 3 distinct distributed networks. A tactile information discrimination network linked the Occipital lobe, Prefrontal lobe, and Postcentral gyrus. A tactile feedback network linked the Prefrontal lobe, Postcentral gyrus, and Temporal lobe. A dominant motor feedforward loop network linked the Parietal cortex, Prefrontal lobe, Frontal lobe, and Parietal cortex. Processing dynamic and static tactile signals involves discriminating tactile information, motion planning, and cognitive decision processing.
Asunto(s)
Electroencefalografía , Percepción del Tacto , Humanos , Masculino , Femenino , Percepción del Tacto/fisiología , Adulto , Adulto Joven , Corteza Cerebral/fisiología , Discriminación en Psicología/fisiología , Tacto/fisiología , Vías Nerviosas/fisiología , Estimulación Física , Mapeo Encefálico , Potenciales Evocados/fisiologíaRESUMEN
Sense of touch is essential for our interactions with external objects and fine control of hand actions. Despite extensive research on human somatosensory processing, it is still elusive how involved brain regions interact as a dynamic network in processing tactile information. Few studies probed temporal dynamics of somatosensory information flow and reported inconsistent results. Here, we examined cortical somatosensory processing through magnetic source imaging and cortico-cortical coupling dynamics. We recorded magnetoencephalography signals from typically developing children during unilateral pneumatic stimulation. Neural activities underlying somatosensory evoked fields were mapped with dynamic statistical parametric mapping, assessed with spatiotemporal activation analysis, and modeled by Granger causality. Unilateral pneumatic stimulation evoked prominent and consistent activations in the contralateral primary and secondary somatosensory areas but weaker and less consistent activations in the ipsilateral primary and secondary somatosensory areas. Activations in the contralateral primary motor cortex and supramarginal gyrus were also consistently observed. Spatiotemporal activation and Granger causality analysis revealed initial serial information flow from contralateral primary to supramarginal gyrus, contralateral primary motor cortex, and contralateral secondary and later dynamic and parallel information flows between the consistently activated contralateral cortical areas. Our study reveals the spatiotemporal dynamics of cortical somatosensory processing in the normal developing brain.
Asunto(s)
Magnetoencefalografía , Corteza Somatosensorial , Humanos , Masculino , Corteza Somatosensorial/fisiología , Corteza Somatosensorial/crecimiento & desarrollo , Femenino , Niño , Potenciales Evocados Somatosensoriales/fisiología , Mapeo Encefálico , Percepción del Tacto/fisiología , Desarrollo Infantil/fisiología , Imagen por Resonancia Magnética , Red Nerviosa/fisiología , Estimulación Física , Corteza Motora/fisiología , Corteza Motora/crecimiento & desarrolloRESUMEN
Nonpainful tactile sensory stimuli are processed in the cortex, subcortex, and brainstem. Recent functional magnetic resonance imaging studies have highlighted the value of whole-brain, systems-level investigation for examining sensory processing. However, whole-brain functional magnetic resonance imaging studies are uncommon, in part due to challenges with signal to noise when studying the brainstem. Furthermore, differentiation of small sensory brainstem structures such as the cuneate and gracile nuclei necessitates high-resolution imaging. To address this gap in systems-level sensory investigation, we employed a whole-brain, multi-echo functional magnetic resonance imaging acquisition at 3T with multi-echo independent component analysis denoising and brainstem-specific modeling to enable detection of activation across the entire sensory system. In healthy participants, we examined patterns of activity in response to nonpainful brushing of the right hand, left hand, and right foot (n = 10 per location), and found the expected lateralization, with distinct cortical and subcortical responses for upper and lower limb stimulation. At the brainstem level, we differentiated the adjacent cuneate and gracile nuclei, corresponding to hand and foot stimulation respectively. Our findings demonstrate that simultaneous cortical, subcortical, and brainstem mapping at 3T could be a key tool to understand the sensory system in both healthy individuals and clinical cohorts with sensory deficits.
Asunto(s)
Mapeo Encefálico , Tronco Encefálico , Imagen por Resonancia Magnética , Humanos , Tronco Encefálico/fisiología , Tronco Encefálico/diagnóstico por imagen , Femenino , Masculino , Imagen por Resonancia Magnética/métodos , Adulto , Mapeo Encefálico/métodos , Adulto Joven , Corteza Cerebral/fisiología , Corteza Cerebral/diagnóstico por imagen , Percepción del Tacto/fisiología , Estimulación Física , Mano/fisiologíaRESUMEN
Do sensory cortices process more than one sensory modality? To answer these questions, scientists have generated a wide variety of studies at distinct space-time scales in different animal models, and often shown contradictory conclusions. Some conclude that this process occurs in early sensory cortices, but others that this occurs in areas central to sensory cortices. Here, we sought to determine whether sensory neurons process and encode physical stimulus properties of different modalities (tactile and acoustic). For this, we designed a bimodal detection task where the senses of touch and hearing compete from trial to trial. Two Rhesus monkeys performed this novel task, while neural activity was recorded in areas 3b and 1 of the primary somatosensory cortex (S1). We analyzed neurons' coding properties and variability, organizing them by their receptive field's position relative to the stimulation zone. Our results indicate that neurons of areas 3b and 1 are unimodal, encoding only the tactile modality in both the firing rate and variability. Moreover, we found that neurons in area 3b carried more information about the periodic stimulus structure than those in area 1, possessed lower response and coding latencies, and had a lower intrinsic time scale. In sum, these differences reveal a hidden processing-based hierarchy. Finally, using a powerful nonlinear dimensionality reduction algorithm, we show that the activity from areas 3b and 1 can be separated, establishing a clear division in the functionality of these two subareas of S1.
Asunto(s)
Corteza Somatosensorial , Percepción del Tacto , Animales , Corteza Somatosensorial/fisiología , Percepción del Tacto/fisiología , Tacto , Lóbulo Parietal , Células Receptoras SensorialesRESUMEN
Perhaps the most recognizable sensory map in all of neuroscience is the somatosensory homunculus. Although it seems straightforward, this simple representation belies the complex link between an activation in a somatotopic map and the associated touch location on the body. Any isolated activation is spatially ambiguous without a neural decoder that can read its position within the entire map, but how this is computed by neural networks is unknown. We propose that the somatosensory system implements multilateration, a common computation used by surveying and global positioning systems to localize objects. Specifically, to decode touch location on the body, multilateration estimates the relative distance between the afferent input and the boundaries of a body part (e.g., the joints of a limb). We show that a simple feedforward neural network, which captures several fundamental receptive field properties of cortical somatosensory neurons, can implement a Bayes-optimal multilateral computation. Simulations demonstrated that this decoder produced a pattern of localization variability between two boundaries that was unique to multilateration. Finally, we identify this computational signature of multilateration in actual psychophysical experiments, suggesting that it is a candidate computational mechanism underlying tactile localization.
Asunto(s)
Redes Neurales de la Computación , Percepción del Tacto/fisiología , Tacto/fisiología , Adulto , Animales , Teorema de Bayes , Mapeo Encefálico , Femenino , Humanos , Ratones , Modelos Neurológicos , Neuronas/fisiología , Estimulación Física , Corteza Somatosensorial/fisiología , Adulto JovenRESUMEN
Intrinsic delays in sensory feedback can be detrimental for motor control. As a compensation strategy, the brain predicts the sensory consequences of movement via a forward model on the basis of a copy of the motor command. Using these predictions, the brain attenuates somatosensory reafference to facilitate the processing of exafferent information. Theoretically, this predictive attenuation is disrupted by (even minimal) temporal errors between the predicted and actual reafference; however, direct evidence of such disruption is lacking as previous neuroimaging studies contrasted nondelayed reafferent input with exafferent input. Here, we combined psychophysics with functional magnetic resonance imaging to test whether subtle perturbations in the timing of somatosensory reafference disrupt its predictive processing. Twenty-eight participants (14 women) generated touches on their left index finger by tapping a sensor with their right index finger. The touches on the left index finger were delivered close to the time of contact of the two fingers or with a temporal perturbation (i.e., 153 ms delay). We found that such a brief temporal perturbation disrupted the attenuation of the somatosensory reafference at both the perceptual and neural levels, leading to greater somatosensory and cerebellar responses and weaker somatosensory connectivity with the cerebellum, proportional to the perceptual changes. We interpret these effects as the failure of the forward model to predictively attenuate the perturbed somatosensory reafference. Moreover, we observed increased connectivity of the supplementary motor area with the cerebellum during the perturbations, which could indicate the communication of the temporal prediction error back to the motor centers.SIGNIFICANCE STATEMENT Our brain receives somatosensory feedback from our movements with a delay. To counteract these delays, motor control theories postulate that the brain predicts the timing of somatosensory consequences of our movements and attenuates sensations received at that time. Thus, a self-generated touch feels weaker than an identical external touch. However, how subtle temporal errors between the predicted and actual somatosensory feedback perturb this predictive attenuation remains unknown. We show that such errors make the otherwise attenuated touch feel stronger, elicit stronger somatosensory responses, weaken cerebellar connectivity with somatosensory areas, and increase this connectivity with motor areas. These findings show that motor and cerebellar areas are fundamental in forming temporal predictions about the sensory consequences of our movements.
Asunto(s)
Corteza Motora , Corteza Sensoriomotora , Percepción del Tacto , Humanos , Femenino , Cerebelo/fisiología , Percepción del Tacto/fisiología , Tacto/fisiología , Movimiento/fisiologíaRESUMEN
Seeing social touch triggers a strong social-affective response that involves multiple brain networks, including visual, social perceptual, and somatosensory systems. Previous studies have identified the specific functional role of each system, but little is known about the speed and directionality of the information flow. Is this information extracted via the social perceptual system or from simulation from somatosensory cortex? To address this, we examined the spatiotemporal neural processing of observed touch. Twenty-one human participants (seven males) watched 500-ms video clips showing social and nonsocial touch during electroencephalogram (EEG) recording. Visual and social-affective features were rapidly extracted in the brain, beginning at 90 and 150 ms after video onset, respectively. Combining the EEG data with functional magnetic resonance imaging (fMRI) data from our prior study with the same stimuli reveals that neural information first arises in early visual cortex (EVC), then in the temporoparietal junction and posterior superior temporal sulcus (TPJ/pSTS), and finally in the somatosensory cortex. EVC and TPJ/pSTS uniquely explain EEG neural patterns, while somatosensory cortex does not contribute to EEG patterns alone, suggesting that social-affective information may flow from TPJ/pSTS to somatosensory cortex. Together, these findings show that social touch is processed quickly, within the timeframe of feedforward visual processes, and that the social-affective meaning of touch is first extracted by a social perceptual pathway. Such rapid processing of social touch may be vital to its effective use during social interaction.SIGNIFICANCE STATEMENT Seeing physical contact between people evokes a strong social-emotional response. Previous research has identified the brain systems responsible for this response, but little is known about how quickly and in what direction the information flows. We demonstrated that the brain processes the social-emotional meaning of observed touch quickly, starting as early as 150 ms after the stimulus onset. By combining electroencephalogram (EEG) data with functional magnetic resonance imaging (fMRI) data, we show for the first time that the social-affective meaning of touch is first extracted by a social perceptual pathway and followed by the later involvement of somatosensory simulation. This rapid processing of touch through the social perceptual route may play a pivotal role in effective usage of touch in social communication and interaction.
Asunto(s)
Percepción del Tacto , Tacto , Humanos , Masculino , Afecto/fisiología , Encéfalo/fisiología , Mapeo Encefálico/métodos , Electroencefalografía , Imagen por Resonancia Magnética , Corteza Somatosensorial/diagnóstico por imagen , Corteza Somatosensorial/fisiología , Tacto/fisiología , Percepción del Tacto/fisiología , FemeninoRESUMEN
When manipulating objects, humans begin adjusting their grip force to friction within 100 ms of contact. During motor adaptation, subjects become aware of the slipperiness of touched surfaces. Previously, we have demonstrated that humans cannot perceive frictional differences when surfaces are brought in contact with an immobilised finger, but can do so when there is submillimeter lateral displacement or subjects actively make the contact movement. Similarly, in, we investigated how humans perceive friction in the absence of intentional exploratory sliding or rubbing movements, to mimic object manipulation interactions. We used a two-alternative forced-choice paradigm in which subjects had to reach and touch one surface followed by another, and then indicate which felt more slippery. Subjects correctly identified the more slippery surface in 87 ± 8% of cases (mean ± SD; n = 12). Biomechanical analysis of finger pad skin displacement patterns revealed the presence of tiny (<1 mm) localised slips, known to be sufficient to perceive frictional differences. We tested whether these skin movements arise as a result of natural hand reaching kinematics. The task was repeated with the introduction of a hand support, eliminating the hand reaching movement and minimising fingertip movement deviations from a straight path. As a result, our subjects' performance significantly declined (66 ± 12% correct, mean ± SD; n = 12), suggesting that unrestricted reaching movement kinematics and factors such as physiological tremor, play a crucial role in enhancing or enabling friction perception upon initial contact. KEY POINTS: More slippery objects require a stronger grip to prevent them from slipping out of hands. Grip force adjustments to friction driven by tactile sensory signals are largely automatic and do not necessitate cognitive involvement; nevertheless, some associated awareness of grip surface slipperiness under such sensory conditions is present and helps to select a safe and appropriate movement plan. When gripping an object, tactile receptors provide frictional information without intentional rubbing or sliding fingers over the surface. However, we have discovered that submillimeter range lateral displacement might be required to enhance or enable friction sensing. The present study provides evidence that such small lateral movements causing localised partial slips arise and are an inherent part of natural reaching movement kinematics.