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Saal, H. P.

Publications and source records attributed to Saal, H. P..

13 recordsLinked to original sources

Illusory cold desensitizes touch

In Jack Londons To Build a Fire, the doomed protagonist notes that "the tremendous cold had already driven the life out of his fingers... dead fingers could neither touch nor clutch". Indeed, our hands are numbed when exposed to cold, a desensitization process traditionally attributed to biophysical and physiological effects on mechanoreceptor and afferent responses1. Yet, perception is not based solely on sensory inputs and often reflects prior beliefs and expectations2. Accordingly, the mere experience of coldness, given its association with tactile desensitization, conceivably modulates touch independent of physical effects. We dissociated the physical and subjective influences of cooling on touch by leveraging the Thermal Referral Illusion3-7, in which cooling of the index and ring fingers induces an illusory perception of coldness that is referred to the middle finger which did not experience local cooling. We found that both veridical and illusory cold elevated tactile detection thresholds. Threshold shifts scaled with subjective ratings of cold intensity which varied with thermal adaptation. Thermal referral induction did not result in changes to skin temperature, ruling out indirect physical effects on the tested finger. To account for cold effects on touch, we implemented a computational model incorporating both physical and subjective factors by simulating changes in tactile afferent spiking activity8 and modulation of decision computations, respectively. The model reproduced empirical cooling effects on afferent responses9 and recapitulated psychophysical detection patterns. Our results reveal that subjective thermal perception contributes to cold-induced attenuation of touch, highlighting how multimodal experiences and expectations shape somatosensation.

neuroscience↗

Epidermal microstructure and tactile sensitivity in the glabrous skin of hands and feet

Glabrous skin on the human palms and soles is specialised for mechanical interaction and is characterised by papillary ridges, an absence of hair follicles, and a thick stratum corneum. While gross morphological differences, such as the increased thickness of the plantar stratum corneum, are well-documented, the fine-scale structural features associated with individual ridges and whether they help explain differences in tactile perception remain poorly understood. Here, we employed optical coherence tomography, automated image segmentation, and 3D reconstruction to generate high-resolution models of the stratum corneum and viable epidermis across six sites on the hand and foot for 27 participants. Our morphological analysis revealed that while the stratum corneum was thicker on the foot sole than the hand, the thickness of the viable epidermis remained remarkably consistent across all sites. Furthermore, papillary ridge width increased in a distal-to-proximal fashion and was larger on the foot. We also found that internal ridge architecture was considerably more pronounced than the topography observable on the skin surface. Correlating these structural parameters with psychophysical measures, specifically absolute force and two-point discrimination thresholds, demonstrated distinct drivers for tactile sensitivity. Force thresholds were primarily governed by a combination of skin thickness and innervation density, and additionally on the foot by papillary ridge width and internal ridge depth. In contrast, spatial acuity was best predicted by innervation and papillary ridge width. These findings provide a precise quantification of glabrous skin morphology and offer new insights into the process of mechanotransduction by highlighting how tissue architecture might contribute to human tactile perception.

neuroscience↗

Can we tell where our bodies end and the world begins? Evidence for precise three dimensional internal body models

Distinguishing our body from the external world is crucial for our sense of self, environmental interaction, and sensory processing. Yet the accuracy with which we perceive this boundary remains underexplored. Here, we developed a novel psychophysical protocol to directly assess how accurately individuals perceive their body boundaries. Participants were asked to determine whether the midpoint between two tactile stimuli applied on the skin was inside or outside their perceived body boundary. 3D scans of the tested regions were used to determine objective anatomical boundaries, allowing psychometric functions to be fitted. Results revealed remarkable overall accuracy, on average within millimeters, in localizing body boundaries across multiple body regions. However, accuracy was not uniform: while palm boundaries were localized with near-perfect precision, stimuli straddling the wrist boundaries were frequently misjudged as extending beyond their true anatomical limit, revealing a systematic perceptual bias. Although perceptual judgments adapted to changes in posture, accuracy declined when the detailed local 3D structure was disregarded, indicating that proprioceptive cues are combined with detailed local body models. Finally, participants whose anatomy deviated from the average tended to align their responses with a typical body model rather than their unique physiology, suggesting that top-down processes influence boundary judgments. Together, our findings suggest that body boundary representation combines detailed three-dimensional body models with proprioceptive feedback into an integrated perceptual model of the anatomical body.

animal behavior and cognition↗

Local postural changes elicit extensive and diverse skin stretch around joints, on the trunk, and the face

Skin stretch, induced by bodily movements, offers a potential source of information about the conformation of the body that can be transmitted to the brain via stretch-sensitive mechanoreceptive neurons. While previous studies have primarily focused on skin stretch directly at joints, here we investigate the extent and complexity of natural skin stretch across various body regions, including the face and trunk. We used a quad-camera setup to image large ink-based speckle patterns stamped on participants skin and calculated the resulting stretch patterns on a millimeter scale during a range of natural poses. We observed that skin stretch associated with joint movement extends far beyond the joint itself, with knee flexion inducing stretch on the upper thigh. Large and uniform stretch patterns were found across the trunk, covering considerable portions of the skin. The face exhibited highly complex and non-uniform stretch patterns, potentially contributing to our capacity to control fine facial movements in the absence of traditional proprioceptors. Importantly, all regions demonstrated skin stretch in excess of mechanoreceptive thresholds, suggesting that behaviorally relevant skin stretch can occur anywhere on the body. These signals might provide the brain with valuable information about body state and conformation, potentially supplementing or even surpassing the capabilities of traditional proprioception.

neuroscience↗

Pre-neuronal biomechanical filtering modulates and diversifies whole-hand tactile encoding

Touching an object elicits skin oscillations that are biomechanically transmitted throughout the hand, driving responses in thousands of tactile receptors, including numerous exquisitely sensitive Pacinian corpuscles (PCs). Accepted descriptions of PC functionality characterize their response properties as highly stereotyped, based on experimental data gathered when stimuli are applied near the receptor. However, during natural touch, spiking activity in the majority of PCs is evoked by transmitted skin oscillations that are modified by biomechanical filtering. This filtering mechanism, stemming from dispersive wave dynamics in the skin, bears some similarity to the pre-neuronal filtering of auditory signals by the basilar membrane, a mechanical process that is instrumental to perception. Thus, we sought to clarify how skin biomechanics might influence tactile information encoding in the periphery. We used vibrometry imaging and computational neural experiments to examine the influence of biomechanical filtering on neural activity in whole-hand PC populations. We observed complex, location- and frequency-dependent patterns of filtering that were shaped by tissue mechanics and hand morphology. This source of biomechanical modulation diversified PC population spiking activity and enhanced tactile information encoding efficiency. These findings indicate that biomechanics furnishes a pre-neuronal mechanism that facilitates efficient tactile encoding and processing.

neuroscience↗

Sub-surface deformation of individual fingerprint ridges during tactile interactions

The human fingertip can detect small tactile features with a spatial acuity roughly the width of a fingerprint ridge. However, how individual ridges deform under contact to support accurate and high-precision tactile feedback is currently unknown. The complex mechanical structure of the glabrous skin, composed of multiple layers and intricate morphology within which mechanoreceptors are embedded, makes this question challenging. Here, we used optical coherence tomography to image and track sub-surface deformations of hundreds of individual fingerprint ridges across ten participants and four individual contact events at high spatial resolution in vivo. We calculated strain patterns in both the stratum corneum and viable epidermis in response to a variety of passively-applied tactile stimuli, including static indentation, stick-to-slip events, sliding of a flat surface in different directions, and interaction with small tactile features, such as edges and grooves. We found that ridges could stretch, compress, and undergo considerable shearing orthogonal to the skin surface, but there was limited horizontal shear. Therefore, it appears that the primary components of ridge deformation and, potentially, neural responses are deformations of the ridge flanks and their relative movement, rather than overall bending of the ridges themselves. We conclude that the local distribution of mechanoreceptors across the ridges might be ideally suited to extract the resulting strain gradients and that the fingertip skin may possess a higher mechanical spatial resolution than that of a single ridge.

neuroscience↗

Memory at your fingertips: how viscoelasticity affects tactile neuron signaling

Human skin and its underlying tissues constitute a viscoelastic medium, implying that any deformation depends not only on the currently applied force, but also the recent loading history. The extent to which this physical memory influences the signaling of first-order tactile neurons during natural hand use is not well understood. Here, we examined the effect of past loading on the responses of fast-adapting (FA-1) and slowly-adapting (SA-1 and SA-2) first-order tactile neurons innervating the human fingertip to loadings applied in different directions representative of object manipulation tasks. We found that variation in the preceding loading affected neurons overall signaling of force direction. Some neurons kept signaling the current direction, while others signaled both the current and preceding direction, or even primarily the preceding direction. In addition, ongoing impulse activity in SA-2 neurons between loadings signaled information related to the fingertips viscoelastic deformation state. We conclude that tactile neurons at the population level signal continuous information about the fingertips viscoelastic deformation state, which is shaped by both its recent history and current loading. Such information might be sufficient for the brain to correctly interpret current force loading and help in computing accurate motor commands for interactions with objects in manipulation and haptic tasks.

neuroscience↗

Complexity of spatiotemporal plantar pressure patterns during everyday behaviours

The human foot sole is the primary interface with the external world during balance and walking, and also provides important tactile information on the state of contact. However, prior studies on plantar pressure have focused mostly on summary metrics such as overall force or centre of pressure under limited conditions. Here, we recorded spatiotemporal plantar pressure patterns with high spatial resolution while participants completed a wide range of daily activities, including balancing, locomotion, and jumping tasks. Contact area differed across task categories, but was only moderately correlated with the overall force experienced by the foot sole. The centre of pressure was often located outside the contact area or in locations experiencing relatively low pressure, and therefore a result of disparate contact regions spread widely across the foot. Non-negative matrix factorisation revealed low-dimensional spatial complexity that increased during interaction with unstable surfaces. Additionally, pressure patterns at the heel and metatarsals decomposed into separately located and robustly identifiable components, jointly capturing most variance in the signal. These results suggest optimal sensor placements to capture task-relevant spatial information and provide insight into how pressure varies spatially on the foot sole during a wide variety of natural behaviours.

neuroscience↗

Population coding strategies in human tactile afferents

Sensory information is conveyed by populations of neurons, and coding strategies cannot always be deduced when considering individual neurons. Moreover, information coding depends on the number of neurons available and on the composition of the population when multiple classes with different response properties are available. Here, we study population coding in human tactile afferents by employing a recently developed simulator of mechanoreceptor firing activity. First, we demonstrate that the optimal afferent density for conveying maximal information depends on the tactile feature under consideration and the afferent class coding this feature. Second, we find that information is spread across different classes for all tactile features, such that combining information from multiple afferent classes improves information transmission, and is often more efficient than increasing the density of afferents from the same class. Finally, we test the importance of timing precision and afferent identity in the population code to probe whether temporal and spatial information can be traded against each other. Destroying temporal information turns out to be more destructive than removing spatial information, and the contribution of either cannot be completely recovered from the other. Overall, our results suggest that both optimal afferent innervation densities and the composition of the population depend in complex ways on the tactile features in question, potentially accounting for the variety in which tactile peripheral populations are assembled in different regions across the body.

neuroscience↗

Modelling novelty detection in the thalamocortical loop

In complex natural environments, sensory systems are constantly exposed to a large stream of inputs. Novel or rare stimuli, which are often associated with behaviorally important events, are typically processed differently than the steady sensory background, which has less relevance. Neural signatures of such differential processing, commonly referred to as novelty detection, have been identified on the level of EEG recordings as mismatch negativity and the level of single neurons as stimulus-specific adaptation. Here, we propose a multi-scale recurrent network with synaptic depression to explain how novelty detection can arise in the whisker-related part of the somatosensory thalamocortical loop. The architecture and dynamics of the model presume that neurons in cortical layer 6 adapt, via synaptic depression, specifically to a frequently presented stimulus, resulting in reduced population activity in the corresponding cortical column when compared with the population activity evoked by a rare stimulus. This difference in population activity is then projected from the cortex to the thalamus and amplified through the interaction between neurons of the primary and reticular nuclei of the thalamus, resulting in spindle-like, rhythmic oscillations. These differentially activated thalamic oscillations are forwarded to cortical layer 4 as a late secondary response that is specific to rare stimuli that violate a particular stimulus pattern. Model results show a strong analogy between this late single neuron activity and EEG-based mismatch negativity in terms of their common sensitivity to presentation context and timescales of response latency, as observed experimentally. Our results indicate that adaptation in L6 can establish the thalamocortical dynamics that produce signatures of SSA and MMN and suggest a mechanistic model of novelty detection that could generalize to other sensory modalities. Author summaryCortical sensory neurons have been shown to be capable of novelty detection, that is they respond more vigorously when a novel, unexpected stimulus is presented, and less so when the stimulus is part of a predictable sequence. However, the neural mechanism underlying this capability is not yet fully understood. Here, we developed a thalamocortical network model that accounts for novelty detection and reproduces physiologically observed neural response patterns in the somatosensory cortex. Specifically, our results demonstrate that the novelty signal arises from the complex recurrent interplay between thalamic neurons and cortical neurons in layers 4 and 6. This work therefore provides a concrete mechanism that can serve as a starting point for further investigating the neural circuit mechanisms underlying novelty detection.

neuroscience↗

Expansion and contraction of resource allocation in sensory bottlenecks

Topographic sensory representations often do not scale proportionally to the size of their input regions, with some expanded and others contracted. In vision, the foveal representation is magnified cortically, as are the fingertips in touch. What principles drive this allocation, and how should receptor density, e.g. the high innervation of the fovea or the fingertips, and stimulus statistics, e.g. the higher contact frequencies on the fingertips, contribute? Building on work in efficient coding, we address this problem using linear models that maximize information transmission through decorrelation. We introduce a sensory bottleneck to impose constraints on resource allocation and derive the optimal neural allocation. We find that bottleneck width is a crucial factor in resource allocation, inducing either expansion or contraction. Both receptor density and stimulus statistics affect allocation and jointly determine convergence for wider bottlenecks. Furthermore, we show a close match between the predicted and empirical cortical allocations in a well-studied model system, the star-nosed mole. Overall, our results suggest that the strength of cortical magnification depends on resource limits.

neuroscience↗

Malleability of the cortical hand map following a finger nerve block

Individual fingers in the primary somatosensory cortex (S1) are known to be represented separately and adjacently, forming a cortical hand map. Electrophysiological studies in monkeys show that finger amputation triggers increased selectivity to the neighbouring fingers within the deprived S1, causing local reorganisation. Neuroimaging research in humans, however, shows persistent S1 finger representation of the missing hand, even decades after amputation. We aimed to resolve these apparently contrasting evidence by examining finger representation in humans following pharmacological amputation using single-finger nerve block and 7T neuroimaging. We hypothesised that beneath the apparent selectivity of individual fingers in the hand map, peripheral and central processing is distributed across fingers. If each finger contributes to the cortical representation of the others, then localised input loss will weaken finger representation across the hand map. For the same reason, the non-blocked fingers will stabilise the blocked fingers representation, resulting in persistent representation of the blocked finger. Using univariate selectivity profiling, we replicated the electrophysiological findings of local S1 reorganisation. However, more comprehensive analyses confirmed that local blocking reduced representation of all fingers across the entire hand area. Importantly, multivariate analysis demonstrated that despite input loss, representation of the blocked finger remained persistent and distinct from the unblocked fingers. Computational modelling suggested that the observed findings are driven by distributed processing underlying the topographic map, combined with homeostatic mechanisms. Our findings suggest that the long-standing depiction of the somatosensory hand map is misleading. As such, accounts for map reorganisation, e.g. following amputation, need to be reconsidered.

neuroscience↗

Tactile innervation densities across the whole body

The skin is our largest sensory organ and innervated by afferent fibers carrying tactile information to the spinal cord and onto the brain. The density with which different classes of tactile afferents innervate the skin is not constant but varies considerably across different body regions. However, precise estimates of innervation density are only available for some body parts, such as the hands, and estimates of the total number of tactile afferent fibers are inconsistent and incomplete. Here we reconcile different estimates and provide plausible ranges and best estimates for the number of different tactile fiber types innervating different regions of the skin, using evidence from dorsal root fiber counts, microneurography, histology, and psychophysics. We estimate that the skin across the whole body is innervated by approximately 230,000 tactile afferent fibers (plausible range: 200,000-270,000). 15% innervate the palmar skin of both hands and 19% the region surrounding the face and lips. Around 60% of all tactile fibers are slowly-adapting, while the rest are fastadapting. Innervation density correlates well with psychophysical spatial acuity across different body regions, and additionally, on hairy skin, with hair follicle density. Innervation density is also weakly correlated with the size of the cortical somatotopic representation, but cannot fully account for the magnification of the hands and the face.

neuroscience↗