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  1. eLife assessment

    This paper will be of broad interest to anyone aiming to understand the neural basis of human touch perception. This is an important paper that provides compelling evidence for peripheral tactile encoding of orientation that reflects perceptual capabilities, by using a wide range of stimulus conditions. The results will be valuable to inform both future experiments and computational investigations into the neural representation and processing of small tactile spatial features at the edge of perceptual resolvability and on the emergence of invariant representations in touch more generally.

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  2. Reviewer #1 (Public Review):

    Sukumar et al. examine the orientation selectivity of individual peripheral tactile afferents in humans at the limits of perceptual resolvability. They report that spike rates and similar measures were only moderately informative, while the temporal profile of the spiking responses was highly informative, an effect that was most likely driven by complex sub-field structure of the receptive field itself. Once temporal responses were corrected for scanning speeds, different orientations could be discriminated across a wide range of different scanning speeds.

    Strengths: The paper tackles an open question and will inform future research, both electrophysiological and psychophysical. The study is built on high-quality data and the analysis is well described and rigorous.

    Weaknesses: The link with the existing psychophysical literature is rather weak, for example there is no discussion on the effects of scanning speeds or other factors that have been described in that literature and that would appear relevant here.

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  3. Reviewer #2 (Public Review):

    This study tests the capacity of single glabrous skin human tactile afferent to discriminate the orientation of edges scanned over their receptive fields (RF) at different speeds spanning 2.5 to 180 mm/s. Raised bars of different orientations (-10,-5,5,10 degrees) were glued on a rotating drum that contacted the skin and rotated at different speeds. Afferent recordings were obtained using microneurography. Both the intensity of the response (i.e. firing rate) and the response profile (precise spike timing) were used as input for discrimination. Indeed, tactile RFs have multiple sensitive zones or hotspots, and different edge orientations will activate those hotspots with a slightly different sequence.

    It is found that using intensity measures, discrimination is possible within but not across speeds. Discrimination performance is, as expected, better using the temporal spiking profile, and is also possible across speed, if the spike trains are represented in the spatial domain, that is if the spike trains are compressed or expanded according to the scanning speed. Furthermore, it is found that filtering the spike trains with a spatial Gaussian of approx. 60-70 um SD optimizes discrimination performance. Contrary to previous reports, it is found the FA-I afferent have better discrimination performance than SA-I afferents.

    This study is mainly a follow-up of a previous report (Pruszynski et al., 2014) that showed the capacity of tactile afferents to signal orientation thanks to their complex RF profiles. It uses the same procedures and analyses but tests smaller orientation differences and a much wider range of different speeds. The dataset is rich and unique, the analyses are straightforward but rigorously carried out and the conclusions are well supported but the results.

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  4. Reviewer #3 (Public Review):

    In this manuscript, the authors describe experiments that were performed to investigate the peripheral neural mechanism of geometric feature extraction in human glabrous skin. The cutaneous sensory space of fast-adapting type 1 (FA-1) and slow-adapting type 1 (SA-1) afferents comprises multiple sensitive zones (subfields) spanning several fingerprint ridges, and the authors had earlier shown that subfield layout and edge orientation sensitivity are linked. In that study, the authors used edges with large orientation differences. Here they examine the signaling mechanism for fine edge orientation differences and the role of the scanning speed. They find that the same mechanism extends to the signaling of fine edge orientation differences and that it is maintained across a broad range of scanning speeds. Both FA-1 and SA-1 afferents perform well, albeit the former better than the latter, in signaling fine edge orientation differences when the sequential structure of their spiking response is considered. Further, the edge orientation sensitivity is tuned to natural scanning speeds with both afferent types showing speed-invariant orientation signaling when spike trains are represented in the spatial domain. These findings advance the idea that the subfield layout/terminal organization of primary tactile afferents in human glabrous skin is important for the early processing of geometric features.

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