Sub-surface deformation of individual fingerprint ridges during tactile interactions

Reviewer #1 (Public Review):

Summary:
This manuscript uses optical coherence tomography (OCT) to visualize tissue microstructures about 1-2 mm under the finger pad skin surface. Their geometric features are tracked and used to generate tissue strains upon skin surface indentation by a series of transparent stimuli both normal and tangential to the surface. Then movements of the stratum corneum and the upper portion of the viable epidermis are evaluated. Based upon this data, across a number of participants and ridges, around 300 in total, the findings report upon particular movements of these tissue microstructures in various loading states. A better understanding of the mechanics of the skin microstructures is important to understand how surface forces propagate toward the locations of mechanoreceptive end organs, which lie near the edge of the epidermis and dermis, from which tactile responses of at least two peripheral afferents originate. Indeed, the microstructures of the skin are likely to be important in shaping how neural afferents respond and enhance their sensitivity, receptive field characteristics, etc.

Strengths:
The use of OCT in the context of analyzing the movements of skin microstructures is novel. Also novel and powerful is the use of distinct loading cases, e.g., normal, tangential, and stimulus features, e.g., edges, and curves. I am unaware of other empirical visualization studies of this sort. They are state-of-the-art in this field. Moreover, in addition to the empirical imaging observations, strain vectors in the tissues are calculated over time.

Weaknesses:
The interpretation of the results and their framing relative to the overall hypotheses/questions and prior works could be articulated more clearly. In particular, the major findings of the manuscript are in newly describing a central concept regarding "ridge flanks," but such structures are neither anatomically nor mechanistically defined in a clear fashion. For example, "... 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." From an anatomical perspective, I think what the authors mean by "ridge flanks" is a differential in strain from one lateral side of a papillary ridge to the other. But is it unclear what about the continuous layers of tissue would cause such behaviors. Perhaps a sweat duct or some other structure (not visible to OCT) would subdivide the "flanks" of a papillary ridge somehow? If not due to particular anatomy, then is the importance of the "ridge flank" due to a mechanistic phenomenon of some sort? Given that the findings of the manuscript center upon the introduction of this new concept, I think a greater effort should be made to define what exactly are the "ridge flanks." It is clear from the results, especially the sliding case, that there is something important that the manuscript is getting at with this concept.

The OCT used herein cannot visualize deep and fully into what the manuscript refers to as a "ridge" (note others have previously broken apart this concept apart into "papillary", "intermediate" and "limiting" ridges) near locations of the mechanoreceptive end organs lie at the epidermal-dermal border. Therefore, the OCT must make inferences about the movements of these deeper tissues, but cannot see them directly, and it is the movements of these deeper tissues that are likely driving the intricacies of neural firing. Note the word "ridge" is used often in the manuscript's abstract, introduction, and discussion but the definition in Fig. 1 and elsewhere differs in important ways from prior works of Cauna (expert in anatomy). Therefore, the manuscript should clarify if "ridge" refers to the papillary ridge (visible at the exterior of the skin), intermediate ridge (defined by Cauna as what the authors refer to as the primary ridge), and limiting ridge (defined by Cauna as what the authors refer to as the secondary ridge). What the authors really mean (I think) is some combination of the papillary and intermediate ridge structures, but not the full intermediate ridge. The manuscript acknowledges this in the "Limitations and future work" section, stating that these ridges cannot be resolved. This is important because the manuscript is oriented toward tracking this structure. It sets up the narrative and hypotheses to evaluate the prior works of Cauna, Gerling, Swensson, and others who all directly addressed the movement of this anatomical feature which is key to understanding ultimately how stresses at these locations might move the peripheral end organs (i.e., Merkel cells, Meissner corpuscles).

Reviewer #2 (Public Review):

Summary:
The authors investigate sub-skin surface deformations to a number of different, relevant tactile stimuli, including pressure and moving stimuli. The results demonstrate and quantify the tension and compression applied from these types of touch to fingerprint ridges, where pressure flattens the ridges. Their study further revealed that on lateral movement, prominent vertical shearing occurred in ridge deformation, with somewhat inconsistent horizontal shear. This also shows how much the deeper skin layers are deformed in touch, meaning the activation of all cutaneous mechanoreceptors, as well as the possibility of other deeper non-cutaneous mechanoreceptors.

Strengths:
The paper has many strengths. As well as being impactful scientifically, the methods are sound and innovative, producing interesting and detailed results. The results reveal the intricate workings of the skin layers to pressure touch, as well as sliding touch over different conditions. This makes it applicable to many touch situations and provides insights into the differential movements of the skin, and thus the encoding of touch in regards to the function of fingerprints. The work is very clearly written and presented, including how their work relates to the literature and previous hypotheses about the function of fingerprint ridges. The figures are very well-presented and show individual and group data well. The additional supplementary information is informative and the video of the skin tracking demonstrates the experiments well.

Weaknesses:
There are very few weaknesses in the work, rather the authors detail well the limitations in the discussion. Therefore, this opens up lots of possibilities for future work.

Impact/significance:
Overall, the work will likely have a large impact on our understanding of the mechanics of the skin. The detail shown in the study goes beyond current understanding, to add profound insights into how the skin actually deforms and moves on contact and sliding over a surface, respectively. The method could be potentially applied in many other different settings (e.g. to investigate more complex textures, and how skin deformation changes with factors like dryness and aging). This fundamental piece of work could therefore be applied to understand skin changes and how these impact touch perception. It can further be applied to understand skin mechanoreceptor function better and model these. Finally, the importance of fingertip ridges is well-detailed, demonstrating how these play a role in directly shaping our touch perception and how they can shape the interactions we have with surfaces.

Reviewer #3 (Public Review):

Summary:
The publication presents unique in-vivo images of the upper layer of the epidermis of the glabrous skin when a flat object compresses or slides on the fingertip. The images are captured using OCT, and are the process of recovering the strain that fingerprints experience during the mechanical stimulation.

The most important finding is, in my opinion, that fingerprints undergo pure compression/tension without horizontal shear, hinting at the fact that the shear stress caused by the tangential load is transferred to the deeper tissues and ultimately to the mechanoreceptors (SA-I / RA-I).

Strengths:
- Fascinating new insights into the mechanics of glabrous skin. To the best of my knowledge, this is the first experimental evidence of the mechanical deformation of fingerprints when subjected to dynamic mechanical stimulation. The OCT measurement allows an unprecedented measurement of the depth of the skin whereas previous works were limited to tracking the surface deformation.
- The robust data analysis reveals the continuum mechanics underlying the deformation of the fingerprint ridges.

Weaknesses:
I do not see any major weaknesses. The work is mainly experimental and is rigorously executed. Two points pique my curiosity, however:

1. How do the results presented in this study compare with previous finite element analysis? I am curious to know if the claim that the horizontal shear strain is transferred to the previous layer is also captured by these models. The reason is that the FEA models typically use homogeneous materials and whether or not the behavior in-silico and in-vivo matches would offer an idea of the nature of the stratum corneum.
2. Was there a specific reason why the authors chose to track only one fingerprint? From the method section, it seems that nothing would have prevented tracking a denser point cloud and reconstructing the stain on a section of the skin rather than just one ridge. With such data, the author could extend their analysis to multiple ridges interaction and get a better sense of the behavior of the entire strip of skin.