The role of fingerprints in the coding of tactile information probed with a biomimetic sensor

In humans, the tactile perception of fine textures (spatial scale <200 micrometers) is mediated by skin vibrations generated as the finger scans the surface. To establish the relationship between texture characteristics and subcutaneous vibrations, a biomimetic tactile sensor has been designed whose dimensions match those of the fingertip. When the sensor surface is patterned with parallel ridges mimicking the fingerprints, the spectrum of vibrations elicited by randomly textured substrates is dominated by one frequency set by the ratio of the scanning speed to the interridge distance. For human touch, this frequency falls within the optimal range of sensitivity of Pacinian afferents, which mediate the coding of fine textures. Thus, fingerprints may perform spectral selection and amplification of tactile information that facilitate its processing by specific mechanoreceptors.Comment: 25 pages, 11 figures, article + supporting materia

Rate and timing of cortical responses driven by separate sensory channels

The sense of touch comprises multiple sensory channels that each conveys characteristic signals during interactions with objects. These neural signals must then be integrated in such a way that behaviorally relevant information about the objects is preserved. To understand the process of integration, we implement a simple computational model that describes how the responses of neurons in somatosensory cortex—recorded from awake, behaving monkeys—are shaped by the peripheral input, reconstructed using simulations of neuronal populations that reproduce natural spiking responses in the nerve with millisecond precision. First, we find that the strength of cortical responses is driven by one population of nerve fibers (rapidly adapting) whereas the timing of cortical responses is shaped by the other (Pacinian). Second, we show that input from these sensory channels is integrated in an optimal fashion that exploits the disparate response behaviors of different fiber types

Separate Mechanisms for Audio-Tactile Pitch and Loudness Interactions

A major goal in perceptual neuroscience is to understand how signals from different sensory modalities are combined to produce stable and coherent representations. We previously investigated interactions between audition and touch, motivated by the fact that both modalities are sensitive to environmental oscillations. In our earlier study, we characterized the effect of auditory distractors on tactile frequency and intensity perception. Here, we describe the converse experiments examining the effect of tactile distractors on auditory processing. Because the two studies employ the same psychophysical paradigm, we combined their results for a comprehensive view of how auditory and tactile signals interact and how these interactions depend on the perceptual task. Together, our results show that temporal frequency representations are perceptually linked regardless of the attended modality. In contrast, audio-tactile loudness interactions depend on the attended modality: Tactile distractors influence judgments of auditory intensity, but judgments of tactile intensity are impervious to auditory distraction. Lastly, we show that audio-tactile loudness interactions depend critically on stimulus timing, while pitch interactions do not. These results reveal that auditory and tactile inputs are combined differently depending on the perceptual task. That distinct rules govern the integration of auditory and tactile signals in pitch and loudness perception implies that the two are mediated by separate neural mechanisms. These findings underscore the complexity and specificity of multisensory interactions

Multiplexing Stimulus Information through Rate and Temporal Codes in Primate Somatosensory Cortex

Our ability to perceive and discriminate textures relies on the transduction and processing of complex, high-frequency vibrations elicited in the fingertip as it is scanned across a surface. How naturalistic vibrations, and by extension texture, are encoded in the responses of neurons in primary somatosensory cortex (S1) is unknown. Combining single unit recordings in awake macaques and perceptual judgments obtained from human subjects, we show that vibratory amplitude is encoded in the strength of the response evoked in S1 neurons. In contrast, the frequency composition of the vibrations, up to 800 Hz, is not encoded in neuronal firing rates, but rather in the phase-locked responses of a subpopulation of neurons. Moreover, analysis of perceptual judgments suggests that spike timing not only conveys stimulus information but also shapes tactile perception. We conclude that information about the amplitude and frequency of natural vibrations is multiplexed at different time scales in S1, and encoded in the rate and temporal patterning of the response, respectively.</p

The frequency of cortical microstimulation shapes artificial touch

Intracortical microstimulation (ICMS) of the somatosensory cortex evokes vivid tactile sensations and can be used to convey sensory feedback from brain-controlled bionic hands. Changes in ICMS frequency lead to changes in the resulting sensation, but the discriminability of frequency has only been investigated over a narrow range of low frequencies. Furthermore, the sensory correlates of changes in ICMS frequency remain poorly understood. Specifically, it remains to be elucidated whether changes in frequency only modulate sensation magnitude - as do changes in amplitude - or whether they also modulate the quality of the sensation. To fill these gaps, we trained monkeys to discriminate the frequency of ICMS pulse trains over a wide range of frequencies (from 10 to 400 Hz). ICMS amplitude also varied across stimuli to dissociate sensation magnitude from ICMS frequency and ensure that animals could not make frequency judgments based on magnitude. We found that animals could consistently discriminate ICMS frequency up to ∼200 Hz but that the sensory correlates of frequency were highly electrode dependent: On some electrodes, changes in frequency were perceptually distinguishable from changes in amplitude - seemingly giving rise to a change in sensory quality; on others, they were not. We discuss the implications of our findings for neural coding and for brain-controlled bionic hands. © 2020 National Academy of Sciences. All rights reserved

Texture is encoded in precise temporal spiking patterns in primate somatosensory cortex

Humans are exquisitely sensitive to the microstructure and material properties of surfaces. In the peripheral nerves, texture information is conveyed via two mechanisms: coarse textural features are encoded in spatial patterns of activation that reflect their spatial layout, and fine features are encoded in highly repeatable, texture-specific temporal spiking patterns evoked as the skin moves across the surface. Here, we examined whether this temporal code is preserved in the responses of neurons in somatosensory cortex. We scanned a diverse set of everyday textures across the fingertip of awake macaques while recording the responses evoked in individual cortical neurons. We found that temporal spiking patterns are highly repeatable across multiple presentations of the same texture, with millisecond precision. As a result, texture identity can be reliably decoded from the temporal patterns themselves, even after information carried in the spike rates is eliminated. However, the combination of rate and timing is more informative than either code in isolation. The temporal precision of the texture response is heterogenous across cortical neurons and depends on the submodality composition of their input and on their location along the somatosensory neuraxis. Furthermore, temporal spiking patterns in cortex dilate and contract with decreases and increases in scanning speed, respectively, and this systematic relationship between speed and patterning may contribute to the observed perceptual invariance to speed. Finally, we find that the quality of a texture percept can be better predicted when these temporal patterns are taken into consideration. We conclude that high-precision spike timing complements rate-based signals to encode texture in somatosensory cortex

Stability of Sensory Topographies in Adult Cortex

Textbooks teach us that the removal of sensory input to sensory cortex, for example, following arm amputation, results in massive reorganisation in the adult brain. In this opinion article, we critically examine evidence for functional reorganisation of sensory cortical representations, focusing on the sequelae of arm amputation on somatosensory topographies. Based on literature from human and non-human primates, we conclude that the cortical representation of the limb remains remarkably stable despite the loss of its main peripheral input. Furthermore, the purportedly massive reorganisation results primarily from the formation or potentiation of new pathways in subcortical structures and does not produce novel functional sensory representations. We discuss the implications of the stability of sensory representations on the development of upper-limb neuroprostheses

Chronic Use of a Sensitized Bionic Hand Does Not Remap the Sense of Touch

Electrical stimulation of tactile nerve fibers that innervated an amputated hand results in vivid sensations experienced at a specific location on the phantom hand, a phenomenon that can be leveraged to convey tactile feedback through bionic hands. Ideally, electrically evoked sensations would be experienced on the appropriate part of the hand: touch with the bionic index fingertip, for example, would elicit a sensation experienced on the index fingertip. However, the perceived locations of sensations are determined by the idiosyncratic position of the stimulating electrode in the nerve and thus are difficult to predict or control. This problem could be circumvented if perceived sensations shifted over time to become consistent with the position of the sensor that triggers them. We show that, after long-term use of a neuromusculoskeletal prosthesis that featured a mismatch between the sensor location and the resulting tactile experience, the perceived location of the touch did not change