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

Harvey, Michael; Saal, Hannes P.; Dammann, J. Francis; Bensmaı̈a, Sliman J.

doi:10.1371/journal.pbio.1001558

Cited by 170 publications

(205 citation statements)

References 35 publications

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“…In particular, the somatosensory system was found to simultaneously rely on both spike rates and timing (Harvey et al, 2013;Saal and Bensmaia, 2014). Mechanoreceptors of the primate glabrous skin and their downstream cortical targets seem to represent spatiotemporal features of tactile stimuli using temporal response properties (Johansson and Birznieks, 2004;Mackevicius et al, 2012;Harvey et al, 2013;Weber et al, 2013), whereas stimulus intensity is represented by a rate code (Bensmaia, 2008;Harvey et al, 2013). In good accordance with these results, we found evidence that the leech mechanosensory system also uses both types of encoding simultaneously.…”

Section: Rate Coding Versus Temporal Codingmentioning

confidence: 99%

Multiplexed Population Coding of Stimulus Properties by Leech Mechanosensory Cells

Pirschel

Kretzberg

2016

J. Neurosci.

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Sensory coding has long been discussed in terms of a dichotomy between spike timing and rate coding. However, recent studies found that in primate mechanoperception and other sensory systems, spike rates and timing of cell populations complement each other. They simultaneously carry information about different stimulus properties in a multiplexed way. Here, we present evidence for multiplexed encoding of tactile skin stimulation in the tiny population of leech mechanoreceptors, consisting of only 10 cells of two types with overlapping receptive fields. Each mechanoreceptor neuron of the leech varies spike count and response latency to both touch intensity and location, leading to ambiguous responses to different stimuli. Nevertheless, three different stimulus estimation techniques consistently reveal that the neuronal population allows reliable decoding of both stimulus properties. For the two mechanoreceptor types, the transient responses of T (touch) cells and the sustained responses of P (pressure) cells, the relative timing of the first spikes of two mechanoreceptors encodes stimulus location, whereas summed spike counts represent touch intensity. Differences between the cell types become evident in responses to combined stimulus properties. The best estimation performance for stimulus location is obtained from the relative first spike timing of the faster and temporally more precise T cells. Simultaneously, the sustained responses of P cells indicate touch intensity by summed spike counts and stimulus duration by the duration of spike responses. The striking similarities of these results with previous findings on primate mechanosensory afferents suggest multiplexed population coding as a general principle of somatosensation.

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Section: Rate Coding Versus Temporal Codingmentioning

confidence: 99%

Multiplexed Population Coding of Stimulus Properties by Leech Mechanosensory Cells

Pirschel

Kretzberg

2016

J. Neurosci.

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“…Indeed, there is good evidence to show that temporal coding of other qualities, including orientation of edges (Pruszynski and Johansson 2014) and vibration frequency (Harvey et al 2013), contributes to encoding tactile inputs. For the types of surfaces studied here, we do not believe that a temporal code contributes to the central representation of the intensity of tactile roughness.…”

Section: Coding Of Tactile Roughnessmentioning

confidence: 99%

Tactile texture signals in primate primary somatosensory cortex and their relation to subjective roughness intensity

Bourgeon

Dépeault

Meftah

et al. 2016

Journal of Neurophysiology

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Bourgeon S, Dépeault A, Meftah EM, Chapman CE. Tactile texture signals in primate primary somatosensory cortex and their relation to subjective roughness intensity. J Neurophysiol 115: 1767-1785, 2016. First published February 10, 2016 doi:10.1152/jn.00303.2015.-This study investigated the hypothesis that a simple intensive code, based on mean firing rate, could explain the cortical representation of subjective roughness intensity and its invariance with scanning speed. We examined the sensitivity of neurons in the cutaneous, finger representation of primary somatosensory cortex (S1) to a wide range of textures [1 mm high, raised-dot surfaces; spatial periods (SPs), 1.5-8.5 mm], scanned under the digit tips at different speeds (40 -115 mm/s). Since subjective roughness estimates show a monotonic increase over this range and are independent of speed, we predicted that the mean firing rate of a subgroup of S1 neurons would share these properties. Single-unit recordings were made in four alert macaques (areas 3b, 1 and 2). Cells whose discharge rate showed a monotonic increase with SP, independent of speed, were particularly concentrated in area 3b. Area 2 was characterized by a high proportion of cells sensitive to speed, with or without texture sensitivity. Area 1 had intermediate properties. We suggest that area 3b and most likely area 1 play a key role in signaling roughness intensity, and that a mean rate code, signaled by both slowly and rapidly adapting neurons, is present at the level of area 3b. Finally, the substantial proportion of neurons that showed a monotonic change in discharge limited to a small range of SPs (often independent of response saturation) could play a role in discriminating smaller changes in SP. tactile roughness; neuronal coding; passive touch; hierarchical processing WHEN WE TOUCH A SURFACE, THE tactile impression of smoothness/roughness is influenced by the physical structure of the surface. A number of factors contribute, including the number of projections (or tactile elements) that make up the surface, their spacing, density, size, form, degree of unevenness and the material from which they are constructed. Any tactile exploration of a surface necessarily activates all of the largediameter cutaneous mechanoreceptive afferents that are involved in discriminative touch, including (in the monkey) slowly adapting type I (SA), rapidly adapting (RA) and Pacinian (PC) afferents. The discharge evoked by textured surfaces is complex, reflecting not only the surface structure, but also factors intrinsic to the exploration process, including scanning speed and contact force.Although the nature of the relationship between subjective roughness and texture remains controversial, the bulk of the evidence suggests that, if the tactile elements are sufficiently high (Ն1 mm), then there is a linear relation between subjective roughness and tactile element spacing [spatial period (SP), distance center-to-center between adjacent elements] for sur-

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“…Given their high sensitivity and large receptive fields, PC afferents are likely to play a central role in conveying this cue (Srinivasan et al 1990;Vallbo and Johansson 1984), although SA and RA afferents could contribute as well (Johansson et al 1982;Talbot et al 1968). According to recent studies (Dépeault et al 2013, Harvey et al 2013, the integration of multiple tactile cues could occur in the primary somatosensory cortex (S1). Neurons of S1 were found to be sensitive to moving tactile stimuli of the types used in the present study (Dépeault et al 2013).…”

Section: Vibrations As a Cue To Tactile Speedmentioning

confidence: 99%

“…Neurons of S1 were found to be sensitive to moving tactile stimuli of the types used in the present study (Dépeault et al 2013). Moreover, they encoded vibration amplitude in the strength of their response and responded to a wide range of vibration frequencies, suggesting they receive input from PC and other afferents (Harvey et al 2013). …”

Section: Vibrations As a Cue To Tactile Speedmentioning

confidence: 99%

The role of vibration in tactile speed perception

Dallmann

Ernst

Moscatelli

2015

Journal of Neurophysiology

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Dallmann CJ, Ernst MO, Moscatelli A. The role of vibration in tactile speed perception. J Neurophysiol 114: 3131-3139, 2015. First published September 30, 2015 doi:10.1152/jn.00621.2015.-The relative motion between the surface of an object and our fingers produces patterns of skin deformation such as stretch, indentation, and vibrations. In this study, we hypothesized that motion-induced vibrations are combined with other tactile cues for the discrimination of tactile speed. Specifically, we hypothesized that vibrations provide a critical cue to tactile speed on surfaces lacking individually detectable features like dots or ridges. Thus masking vibrations unrelated to slip motion should impair the discriminability of tactile speed, and the effect should be surface-dependent. To test this hypothesis, we measured the precision of participants in discriminating the speed of moving surfaces having either a fine or a ridged texture, while adding masking vibratory noise in the working range of the fast-adapting mechanoreceptive afferents. Vibratory noise significantly reduced the precision of speed discrimination, and the effect was much stronger on the fine-textured than on the ridged surface. On both surfaces, masking vibrations at intermediate frequencies of 64 Hz (65-m peak-topeak amplitude) and 128 Hz (10 m) had the strongest effect, followed by high-frequency vibrations of 256 Hz (1 m) and lowfrequency vibrations of 32 Hz (50 and 25 m). These results are consistent with our hypothesis that slip-induced vibrations concur to the discrimination of tactile speed.

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

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

Cited by 170 publications

References 35 publications

Multiplexed Population Coding of Stimulus Properties by Leech Mechanosensory Cells

Multiplexed Population Coding of Stimulus Properties by Leech Mechanosensory Cells

Tactile texture signals in primate primary somatosensory cortex and their relation to subjective roughness intensity

The role of vibration in tactile speed perception

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