Hannes P. Saal

Spatial and temporal codes mediate the tactile perception of natural textures

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Multiplexing stimulus information through rate and temporal codes in primate somatosensory cortex.

In somatosensory cortex, stimulus amplitude is represented at a relatively coarse temporal resolution, while stimulus frequency is represented by precisely timed action potentials.

Touch is a team effort: interplay of submodalities in cutaneous sensibility

Traditionally, different classes of cutaneous mechanoreceptive afferents are ascribed different and largely non-overlapping functional roles (for example texture or motion) stemming from their different response properties. This functional segregation is thought to be reflected in cortex, where each neuron receives input from a single submodality. We summarize work that challenges this notion. First, while it is possible to design artificial stimuli that preferentially excite a single afferent class, most natural stimuli excite all afferents and most tactile percepts are shaped by multiple submodalities. Second, closer inspection of cortical responses reveals that most neurons receive convergent input from multiple afferent classes. We argue that cortical neurons should be grouped based on their function rather than on their submodality composition.

Millisecond Precision Spike Timing Shapes Tactile Perception

In primates, the sense of touch has traditionally been considered to be a spatial modality, drawing an analogy to the visual system. In this view, stimuli are encoded in spatial patterns of activity over the sheet of receptors embedded in the skin. We propose that the spatial processing mode is complemented by a temporal one. Indeed, the transduction and processing of complex, high-frequency skin vibrations have been shown to play an important role in tactile texture perception, and the frequency composition of vibrations shapes the evoked percept. Mechanoreceptive afferents innervating the glabrous skin exhibit temporal patterning in their responses, but the importance and behavioral relevance of spike timing, particularly for naturalistic stimuli, remains to be elucidated. Based on neurophysiological recordings from Rhesus macaques, we show that spike timing conveys information about the frequency composition of skin vibrations, both for individual afferents and for afferent populations, and that the temporal fidelity varies across afferent class. Furthermore, the perception of skin vibrations, measured in human subjects, is better predicted when spike timing is taken into account, and the resolution that predicts perception best matches the optimal resolution of the respective afferent classes. In light of these results, the peripheral representation of complex skin vibrations draws a powerful analogy with the auditory and vibrissal systems.

Natural scenes in tactile texture

Sensory systems are designed to extract behaviorally relevant information from the environment. In seeking to understand a sensory system, it is important to understand the environment within which it operates. In the present study, we seek to characterize the natural scenes of tactile texture perception. During tactile exploration complex high-frequency vibrations are elicited in the fingertip skin, and these vibrations are thought to carry information about the surface texture of manipulated objects. How these texture-elicited vibrations depend on surface microgeometry and on the biomechanical properties of the fingertip skin itself remains to be elucidated. Here we record skin vibrations, using a laser-Doppler vibrometer, as various textured surfaces are scanned across the finger. We find that the frequency composition of elicited vibrations is texture specific and highly repeatable. In fact, textures can be classified with high accuracy on the basis of the vibrations they elicit in the skin. As might be expected, some aspects of surface microgeometry are directly reflected in the skin vibrations. However, texture vibrations are also determined in part by fingerprint geometry. This mechanism enhances textural features that are too small to be resolved spatially, given the limited spatial resolution of the neural signal. We conclude that it is impossible to understand the neural basis of texture perception without first characterizing the skin vibrations that drive neural responses, given the complex dependence of skin vibrations on both surface microgeometry and fingertip biomechanics.

Biomimetic approaches to bionic touch through a peripheral nerve interface

State-of-the-art prosthetic hands nearly match the dexterity of the human hand, and sophisticated approaches have been developed to control them intuitively. However, grasping and dexterously manipulating objects relies heavily on the sense of touch, without which we would struggle to perform even the most basic activities of daily living. Despite the importance of touch, not only in motor control but also in affective communication and embodiment, the restoration of touch through bionic hands is still in its infancy, a shortcoming that severely limits their effectiveness. Here, we focus on approaches to restore the sense of touch through an electrical interface with the peripheral nerve. First, we describe devices that can be chronically implanted in the nerve to electrically activate nerve fibers. Second, we discuss how these interfaces have been used to convey basic somatosensory feedback. Third, we review what is known about how the somatosensory nerve encodes information about grasped objects in intact limbs and discuss how these natural neural codes can be exploited to convey artificial tactile feedback. Finally, we offer a blueprint for how these codes could be implemented in a neuroprosthetic device to deliver rich, natural, and versatile tactile sensations.

The neural basis of perceived intensity in natural and artificial touch

Electrical connections between nerves and a prosthetic device enable amputees to discern precise, graded sensory intensity ranging from light touch to intense pressure. Perceived intensity: A touchy subject for neuroprostheses Without tactile sensory input, amputees discern a firm handshake from a bone-crushing grip by visual cues and learned behavior. Next-generation prostheses aim to lend a more natural feel to artificial touch by transmitting nuanced sensory feedback. Graczyk et al. looked at direct stimulation of the radial, ulnar, and median nerves via implanted electrodes in two amputees to understand how levels of intensity are perceived and how tactile sensory feedback is transmitted. By modulating the number of nerve fibers stimulated and the frequency of stimulation, sensory information could be transmitted such that the amputees could distinguish distinct levels of tactile intensity, that is, the difference between a 7 and a 10 on a scale of intensity. Electrical stimulation of sensory nerves is a powerful tool for studying neural coding because it can activate neural populations in ways that natural stimulation cannot. Electrical stimulation of the nerve has also been used to restore sensation to patients who have suffered the loss of a limb. We have used long-term implanted electrical interfaces to elucidate the neural basis of perceived intensity in the sense of touch. To this end, we assessed the sensory correlates of neural firing rate and neuronal population recruitment independently by varying two parameters of nerve stimulation: pulse frequency and pulse width. Specifically, two amputees, chronically implanted with peripheral nerve electrodes, performed each of three psychophysical tasks—intensity discrimination, magnitude scaling, and intensity matching—in response to electrical stimulation of their somatosensory nerves. We found that stimulation pulse width and pulse frequency had systematic, cooperative effects on perceived tactile intensity and that the artificial tactile sensations could be reliably matched to skin indentations on the intact limb. We identified a quantity we termed the activation charge rate (ACR), derived from stimulation parameters, that predicted the magnitude of artificial tactile percepts across all testing conditions. On the basis of principles of nerve fiber recruitment, the ACR represents the total population spike count in the activated neural population. Our findings support the hypothesis that population spike count drives the magnitude of tactile percepts and indicate that sensory magnitude can be manipulated systematically by varying a single stimulation quantity.

Importance of spike timing in touch: an analogy with hearing?

Touch is often conceived as a spatial sense akin to vision. However, touch also involves the transduction and processing of signals that vary rapidly over time, inviting comparisons with hearing. In both sensory systems, first order afferents produce spiking responses that are temporally precise and the timing of their responses carries stimulus information. The precision and informativeness of spike timing in the two systems invites the possibility that both implement similar mechanisms to extract behaviorally relevant information from these precisely timed responses. Here, we explore the putative roles of spike timing in touch and hearing and discuss common mechanisms that may be involved in processing temporal spiking patterns.

Active estimation of object dynamics parameters with tactile sensors

The estimation of parameters that affect the dynamics of objects—such as viscosity or internal degree of freedom—is an important step in autonomous and dexterous robotic manipulation of objects. However, accurate and efficient estimation of these object parameters may be challenging due to complex, highly nonlinear underlying physical processes. To improve on the quality of otherwise hand-crafted solutions, automatic generation of control strategies can be helpful. We present a framework that uses active learning to help with sequential gathering of data samples,using information-theoretic ciriteria to find the optimal actions to perform at each time step. We demonstrate the usefulness of our approach on a robotic hand-arm setup, where the task involves shaking bottles of different liquids in order to determine the liquids viscosity from only tactile feedback. We optimize the shaking frequency and the rotation angle of shaking in an online manner in order to speed up convergence of estimates.

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. DOI: http://dx.doi.org/10.7554/eLife.10450.001