Follicle Microstructure and Innervation Vary between Pinniped Micro- and Macrovibrissae

Abstract

Histological data from terrestrial, semiaquatic, and fully aquatic mammal vibrissa (whisker) studies indicate that follicle microstructure and innervation vary across the mystacial vibrissal array (i.e. medial microvibrissae to lateral macrovibrissae). However, comparative data are lacking, and current histological studies on pinniped vibrissae only focus on the largest ventrolateral vibrissae. Consequently, we investigated the microstructure, medial-to-lateral innervation, and morphometric trends in harp seal (Pagophilus groenlandicus) vibrissal follicle-sinus complexes (F-SCs). The F-SCs were sectioned either longitudinally or in cross-section and stained with a modified Masson's trichrome stain (microstructure) or Bodian's silver stain (innervation). All F-SCs exhibited a tripartite blood organization system. The dermal capsule thickness, the distribution of major branches of the deep vibrissal nerve, and the hair shaft design were more symmetrical in medial F-SCs, but these features became more asymmetrical as the F-SCs became more lateral. Overall, the mean axon count was 1,221 ± 422.3 axons/F-SC and mean axon counts by column ranged from 550 ± 97.4 axons/F-SC (medially, column 11) to 1,632 ± 173.2 axons/F-SC (laterally, column 2). These values indicate a total of 117,216 axons innervating the entire mystacial vibrissal array. The mean axon count of lateral F-SCs was 1,533 ± 192.9 axons/ F-SC, which is similar to values reported in the literature for other pinniped F-SCs. Our data suggest that conventional studies that only examine the largest ventrolateral vibrissae may overestimate the total innervation by ∼20%. However, our study also accounts for variation in quantification methods and shows that conventional analyses likely only overestimate innervation by ∼10%. The relationship between axon count and cross-sectional F-SC surface area was nonlinear, and axon densities were consistent across the snout. Our data indicate that harp seals exhibit microstructural and innervational differences between their microvibrissae (columns 8-11) and macrovibrissae (columns 1-7). We hypothesize that this feature is conserved among pinnipeds and may result in functional compartmentalization within their mystacial vibrissal arrays.

Innervation patterns of mystacial vibrissae support active touch behaviors in California sea lions (Zalophus californianus)

“…Pinnipeds (seals, sea lions, fur seals, and walruses) have the largest vibrissae of any mammalian group, and, in general, their largest F‐SCs are innervated by ~1,600–2,000 axons per F‐SC or more (Hyvärinen, ; Hyvärinen, Palviainen, Strandberg, & Holopainen, ; Ling, ; Marshall, Amin, Kovacs, & Lydersen, ; Mattson & Marshall, ; McGovern, Marshall, & Davis, ). The size of the nerve bundle and the number of axons innervating the peripheral sensory structures can be used as a proxy for whisker sensitivity or any type of sensory modality (e.g., George & Holliday, ; McGovern et al, ).…”

Does Vibrissal Innervation Patterns and Investment Predict Hydrodynamic Trail Following Behavior of Harbor Seals (Phoca vitulina)?

“…The number of axons for the largest ventrolateral vibrissae and total estimate of the mystacial array are similar to that reported for other phocid species and sea otters (Table ). Based on Mattson and Marshall (), this likely overestimates the mystacial innervation by approximately 10% since only the largest F‐SCs were measured. A corrected mean value for innervation of the whole muzzle would be approximately 128,858 axons per muzzle instead of 143,176 axons.…”

“…Harbor seals have increased density of axons in the ventrolateral vibrissae compared to harp seal ( Pagophilus groenlandicus ) vibrissae from the same region. The vibrissae in columns 8, 9, and 10 have higher density of axons in harbor seals than vibrissae in the same location in harp seals (Table ), the only other phocids for which density data are available (Mattson and Marshall, ). Harp seal vibrissae from column 8 had 297.7 axons per mm 2 compared to the 437 axons per mm 2 in harbor seal column 8 vibrissae.…”

“…The ventrolateral macrovibrissae are much larger (in F‐SC size and hair shaft length) than other vibrissae, particularly the smallest vibrissae located most medially and dorsally. These presumptive microvibrissae, or the whiskers clustered medially around the nose (as described in Mattson and Marshall, ), appear to be more important in active touch reception. Harbor seals have been observed to use the most medial vibrissae for fine‐scale tactile discrimination tasks (Dehnhardt and Kaminski, ; Grant et al, ; Eberhardt et al, ).…”

“…Hair shaft movement is thought to stimulate mechanoreceptors at the glassy membrane and in the densely innervated inner-conical body and ringwulst, which are located around the fluid-filled ring sinus (RS) about halfway through the F-SC. How pinniped vibrissae detect mechanosensory signals is poorly understood, since to date functional studies have either focused on microstructure, and innervation patterns (Hyvärinen, 1995;Marshall et al, 2006, Marshall et al, 2014aMcGovern et al, 2015;Mattson and Marshall, 2016;Jones, 2017;Sprowls, 2017), hair shaft morphology and mechanics (Hanke et al, 2010;Wieskotten et al, 2010aWieskotten et al, , 2010bMurphy et al, 2013;Summarell et al, 2015), behavioral performance studies and psychophysical testing (Dehnhardt, 1994;Dehnhardt and Kaminski, 1995;Dehnhardt et al, 2001;Gläser et al, 2011;Murphy et al, 2015;Eberhardt et al, 2016), experimental behavioral studies (Marshall et al, 2014b;Marshall et al, 2015), or studies on individual whisker use in live harbor seals (Grant et al, 2013;Murphy et al, 2017). However, few studies have attempted to integrate morphological, neurobiological, and behavioral data to provide a holistic function hypothesis.…”