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

Abstract

Vibrissae or follicle-sinus complexes (F-SCs) are highly developed mammalian sensory structures. These blood-filled sinuses are richly innervated and possess novel mechanoreceptors. Although much is known regarding the function of F-SCs in terrestrial mammals, much less is known regarding marine carnivores such as pinnipeds. Pinnipeds possess the largest, most highly innervated vibrissae of any mammal. One such pinniped is the California sea lion, which are generalist marine predators that rely heavily upon tactile discrimination capabilities. Psychophysical studies demonstrate that haptic tactile discrimination using F-SCs is exceptionally sensitive. However, our knowledge of the structure and function of F-SCs in otariids is limited. Our objectives were to investigate the innervation and microstructure of F-SCs across the mystacial vibrissal field and infer function from haptic performance studies in California sea lions. Innervation and microstructure of vibrissae differed considerably compared to similar data available for phocids. Total innervation of mystacial vibrissae was estimated to be 86,042 axons. Investigations of innervation density and investment of microvibrissae versus macrovibrissae demonstrated a significantly increased axon density per F-SC in medial microvibrissal regions compared to lateral macrovibrissae, which supports psychophysical data and somatotopic organization of the central nervous system involved with tactile discrimination capability. Innervation increased from medial microvibrissae (705 ± 125 axons/F-SC) to lateral macrovibrissae (1,447 ± 154) as well as from dorsal (541 ± 60) to ventral (1,493 ± 327) vibrissal regions.These data provide a more complete picture of the sensory ecology of this important aquatic mammalian lineage; the specialization of peripheral sensory structures, central nervous structures with demonstrated enhanced haptic capabilities behaviorally has likely led to the ecological success of California sea lions.

Ecomorphology reveals Euler spiral of mammalian whiskers

“…Damping will occur within the follicle and will depend on the follicle anatomy, blood supply, and surrounding muscles, which all might be under active, or passive, control (Hartmann, Johnson, Towal, & Assad, 2003; Hyvärinen, 1989; Mitchinson et al, 2004). The arrangement of mechanoreceptors within follicles will also vary from species to species (Ebara et al, 2002; Hyvärinen, 1989; Jones & Marshall, 2019; Marshall, Amin, Kovacs, & Lydersen, 2006; Sprowls & Marshall, 2019), so exactly how and where whisker deflections and vibrations are detected will vary between species. It is evident that there is much to learn about whiskers; further studies could usefully explore relationships between morphological variation and evolutionary adaptations, in particular with respect to the “whisker specialists,” including aquatic and scansorial mammals.…”

“…Whisker morphology can vary between species, for example, many phocids have undulating, beaded whiskers (Ginter et al, 2012; Ginter, Fish, & Marshall, 2010; Hanke et al, 2010; Rinehart, Shyam, & Zhang, 2017), and aquatic mammals are thought to have more innervated whiskers than terrestrial species (Dehnhardt & Mauck, 2008; Mattson & Marshall, 2016; Mcgovern, Marshall, & Davis, 2015; Miersch et al, 2011; Rice, Mance, & Munger, 1986). Some aquatic species use their whiskers for both, touch and hydrodynamic sensing, such as California sea lions ( Zalophus californianus ; Gläser, Wieskotten, Otter, Dehnhardt, & Hanke, 2011; Milne & Grant, 2014) and Harbour seals ( Phoca vitulina ; Dehnhardt, Mauck, & Bleckmann, 1998; Grant, Wieskotten, Wengst, Prescott, & Dehnhardt, 2013), which may indicate functional differences between aquatic and terrestrial whiskers (Jones & Marshall, 2019; Sprowls & Marshall, 2019). Yet, while whisker shape and function are likely to differ between species, especially between aquatic and terrestrial species, the difficulty in comparing whisker shape quantitatively means that whisker morphology has not been explored across a wide range of mammalian species before.…”

“…. Some aquatic species use their whiskers for both, touch and hydrodynamic sensing, such as California sea lions (Zalophus californianus; Gläser, Wieskotten, Otter, Dehnhardt, & Hanke, 2011;Milne & Grant, 2014) and Harbour seals (Phoca vitulina; Dehnhardt, Mauck, & Bleckmann, 1998;Grant, Wieskotten, Wengst, Prescott, & Dehnhardt, 2013), which may indicate functional differences between aquatic and terrestrial whiskers (Jones & Marshall, 2019;Sprowls & Marshall, 2019). Yet, while whisker shape and function are likely to differ between species, especially between aquatic and terrestrial species, the difficulty in comparing whisker shape quantitatively means that whisker morphology has not been explored across a wide range of mammalian species before.…”

Comparing vibrissal morphology and infraorbital foramen area in pinnipeds

“…As well as having morphological specializations, pinniped vibrissae are also particularly sensitive (Hyvärinen, 1989;Jones & Marshall, 2019;Marshall, Amin, Kovacs, & Lydersen, 2006;Mattson & Marshall, 2016;Smodlaka, Galex, Palmer, Borovac, & Khamas, 2017;Sprowls & Marshall, 2019), further supporting the importance of vibrissal sensing in pinnipeds. The deep vibrissal nerve, which is a branch of the infraorbital nerve (ION), contains 10 times more nerve fibers in pinnipeds, than in terrestrial mammals (Hyvärinen, 1989;Hyvärinen, Palviainen, Strandberg, & Holopainen, 2009).…”

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

“…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.…”