Vibrissal touch in pinnipeds
|Wolf Hanke and Guido Dehnhardt (2015), Scholarpedia, 10(3):6828.||doi:10.4249/scholarpedia.6828||revision #150473 [link to/cite this article]|
Vibrissal touch is the sensory modality that enables animals to detect and analyse objects and to orient themselves using their vibrissae (whiskers). Pinnipeds (Pinnipedia) are aquatic carnivores of the families Phocidae (true seals), Otariidae (eared seals), and Odobenidae (walruses). All pinnipeds possess prominent vibrissae (whiskers) in the facial region (Figure 1). Pinnipeds use their whiskers for orientation by directly touching objects (Dehnhardt, 1990; Dehnhardt, 1994; Dehnhardt and Dücker, 1996; Dehnhardt and Kaminski, 1995; Dehnhardt and Mauck, 2008; Kastelein et al., 1990) and by perceiving and analyzing water movements (Dehnhardt et al., 1998a; Dehnhardt et al., 2001; Gläser et al., 2011; Hanke et al., 2013; Hanke et al., 2012; Wieskotten et al., 2010a; Wieskotten et al., 2010b; Wieskotten et al., 2011).
Morphology and Anatomy
The vibrissae of pinnipeds are mostly located on the snout (mystacial vibrissae), but also above the eyes (supraorbital or superciliary vibrissae) and above the nares (rhinal vibrissae, only in true seals). Numbers of mystacial vibrissae range from approximately 15 (in the Ross seal Ommatophoca) to 350 (in the walrus Odobenus) on each side (Ling, 1977), with considerable intraspecific as well as interspecific variability. True seals and eared seals have approximately 3 to 7 supraorbital vibrissae above each eye (Ling, 1977), while supraorbital vibrissae in the walrus are rarely noticeable in animals more than a few weeks old (Fay, 1982). True seals have one (rarely two) additional vibrissa above each nare (rhinal vibrissae) (Ling, 1977). In the harbour seal (Phoca vitulina), which is the true seal species best studied behaviourally to date, there are approximately 44 mystacial vibrissae (Dehnhardt and Kaminski, 1995), exactly one rhinal vibrissa (Ling, 1977) and usually 5 supraorbital vibrissae (pers. obs.) per side. The California sea lion (Zalophus californianus), which is the eared seal species best studied behaviourally to date, has 38 mystacial vibrissae on each side (counted in 4 animals) (Dehnhardt, 1994), no rhinal vibrissae (Ling, 1977), but supraorbital vibrissae, which are less prominent than in true seals (pers. obs.).
Each vibrissa emerges from a vibrissal follicle-sinus complex (F-SC). F-SCs are found at the base of the vibrissae of all mammals and constitute complex and richly innervated sensory organs. They consist of large blood-filled sinuses in a dermal capsule, and the hair follicle around the hair shaft. The blood sinuses supply nutrients, but must also crucially influence the biomechanics of vibrissal sensing, as they form the bearing where the vibrissa is supported. Pinnipeds have particularly large F-SCs that can reach a length of more than 2 cm (Marshall, 2006). F-SCs are richly endowed with receptor cells and nerve endings.
Figure 2 shows the F-SC of a ringed seal (Phoca hispida) based on information and presentations in Dehnhardt et al. (1998b), Hyvärinen and Katajisto (1984), and Hyvärinen et al. (2009). F-SCs of California sea lions (Zalophus californianus) (Stephens et al., 1973), bearded seals (Erignathus barbatus) (Marshall et al., 2006) and Northern elephant seals (Mirounga angustirostris) (McGovern et al., 2014) are generally similar to the F-SCs of ringed seals. The F-SCs of all pinnipeds are particularly large and possess a feature that distinguishes them from the F-SCs of almost all other mammals except the sea otter (Enhydra lutris): the blood sinus is not bipartite, but tripartite. In addition to a (lower) cavernous sinus and a ring sinus found in all mammalian F-SCs, pinnipeds (Stephens, 1973; Hyvärinen and Katajisto, 1984) and sea otters (Marshall et al., 2014) have an upper cavernous sinus (Figure 2a). The upper cavernous sinus, possibly in addition to biomechanical functions that are not yet fully understood, serves to protect the receptors from cooling by the surrounding water (Erdsack et al., 2014). The ring sinus surrounds the vibrissa basally to the upper cavernous sinus, separating it from the lower cavernous sinus at the basal end of the F-SC. The ring sinus is strongly believed to play a crucial role in the biomechanics of the vibrissa. The ring sinus is separated from the upper cavernous sinus by the inner conical body, a collagenous structure. At the level of the ring sinus, a ringwulst (also called ring bulge) surrounds the outer root sheath of the hair. The ringwulst is an asymmetrical bulge of connective tissue attached to the glassy membrane by strong collagenous bundles. The F-SC is equipped with mechanoreceptors at the level of the lower cavernous sinus and especially the ring sinus, but not the upper cavernous sinus. Figure 2b shows a transverse section of the F-SC of a ringed seal at the lower part of the ring sinus, above the ringwulst. The vibrissal hair shaft is surrounded subsequently by an inner root sheath, an outer root sheath, a glassy membrane, and a mesenchymal root sheath (these are general features of a hair follicle), followed by the conical body, the ring sinus, and a dermal capsule. Nerve endings are located on each side of the glassy membrane. On the inside of the glassy membrane, within the basal layer of the outer root sheath, there are Merkel cells in Merkel cell-neurite-complexes; on the outside of the glassy membrane, there are lanceolate nerve endings within the outer root sheath. The number of Merkel cell-neurite-complexes is up to 20 000, and the number of lanceolate endings is approximately 1000 -8000 (Hyvärinen et al., 2009). The F-SC also contains 100-400 lamellated endings and numerous free nerve endings in the ring sinus and lower cavernous sinus area (Dehnhardt and Mauck, 2008).
The F-SC is innervated by a deep vibrissal nerve (DVN) that penetrates the outer capsule at the base of the F-SC. A superficial vibrissal nerve, as found in other mammals, is lacking in pinnipeds. The DVN is part of the trigeminal nerve and can contain approximately 1000 to 1600 nerve fibers in harp seals (Hyvärinen and Katajisto, 1984), bearded seals (Marshall et al., 2006) and Northern elephant seals (McGovern et al., 2014), that is about ten times as many as in the rat, the cat and most other terrestrial mammals (Hyvärinen et al., 2009).
Little is known about the central neuroanatomy of the vibrissal system of pinnipeds (see below, neurophysiology).
The vibrissal hair shaft has an ellipsoidal cross section (Watkins and Wartzok, 1985; Hyvärinen, 1989; Ginter et al., 2010), contrary to the vibrissal hair shafts of terrestrial mammals, which are round in cross section. The vibrissal hair shaft (often called the vibrissa for short) is strongly flattened in most of the true seals (Dehnhardt and Mauck, 2008), and slightly flattened in eared seals (Dehnhardt and Mauck, 2008) and walruses (Fay, 1982). In most true seals, the vibrissa is undulated (synonymously called “waved” or “beaded”) (King, 1983; Ling, 1977, Ginter et al. 2010, 2012), that means that the diameter changes along the length sinusoidally with a period of a few millimeters, reminding of a pearl necklace at first glance (Figure 1a, 3a, b). However, the greater and the smaller diameter of the cross section change out of phase by approximately 180 deg. along the length of the vibrissa (Dehnhardt and Mauck, 2008; Hanke et al., 2010). The shape of the undulated vibrissae shows interspecific variation (Ginter et al. 2012). Within the true seals, the monk seals (Monachus spp.) and the bearded seal (Erignathus barbatus) are exceptions, their vibrissae are smooth in outline. Eared seals (Figure 1b, 3 c, d) and the walrus (Figure 1c) have smooth vibrissae.
Dykes (1975) recorded action potentials from the infraorbital nerve (a branch of the trigeminal nerve) in grey seals (Halichoerus grypus) and harbour seals (Phoca vitulina concolor). The nerve consisted of about 45 bundles. In most bundles, most of the nerve fibers were associated with vibrissae. Among these, slowly adapting (SA) and rapidly adapting (RA) fibers could be distinguished; two thirds of these fibers were RA. SA fibers were defined by ongoing neural activity after a vibrissa had been deflected and held steady for about 1 s; in RA fibers, neural activity had ceased at that point.
Ladygina et al. (1985) mapped somatic projections in the cerebral cortex of northern fur seals (Callorhinus ursinus). They recorded neuronal activity (multiple spike activity) in a depth range of 600-1000 µm and monitored it acoustically (by listening to the action potentials fed into a loudspeaker). Neuronal activity upon touching the body surface was found in a region on the dorso-rostral part of the cerebral cortex, bounded caudally by the anterior suprasylvian sulcus, dorsomedially by the ansate sulcus, rostrally by the postcruciate and coronal sulci. Only contralateral touch of the body elicited responses in this part of the cortex. Receptive fields (body surface areas that on touch elicited response at a given electrode position in the brain) were smallest on the tip of the nose and anterior regions of the upper and lower lips. Within the somatosensory cortex, vibrissae were overrepresented with each vibrissa corresponding to a considerable portion of the cortex, up to 3-4 mm in diameter. Representations of the vibrissae were arranged somatotopically in the cortex. Intensive neuronal responses were recorded from all vibrissae regardless of position or length. The region mapped was believed to correspond to the primary somatosensory cortex (SI) studied in other animals. The method of acoustical monitoring did not allow for further conclusions beyond the somatotopic organization of the cortex and the approximate size of receptive fields and the approximate size of the cortex representing a vibrissa.
In summary, neurophysiological data on the vibrissal system of pinnipeds is scarce.
The biomechanical properties of the vibrissal hair shaft are largely influenced by its moment of inertia (that is, by its cross-sectional shape). The modulus of elasticity (a measure of how the material itself deforms elastically under stress) of a harbour seal vibrissa is similar to other keratinous structures and decreases after immersion in water (Marine Center Rostock, unpublished data). Contrary to the vibrissae of rats, the modulus of elasticity of harbour seal vibrissae changes along the length of the vibrissa (Hans et al., 2014).
The undulated shape of harbour seal vibrissae reduces vortex-induced vibrations as the animal swims (Hanke et al., 2010). Vortex-induced vibrations are vibrations of cylindroid objects in a perpendicular flow that are caused by vortices detaching from the object on alternating sides. Figure 4 represents a numerical simulation of the flow behind a harbour seal vibrissa compared with the flow behind cylinders with an elliptical cross section and a round cross section, respectively. Behind the vibrissa, vortices form at a greater distance, they are weaker, and they constitute a complex three-dimensional pattern that makes forces on the vibrissa more symmetrical (Hanke et al., 2010; Witte et al., 2012). By reducing vortex-induced vibrations at the vibrissa, the signal-to-noise ratio at the receptors in the F-SC is enhanced. Not surprisingly, the orientation of the flattened vibrissal cross section towards the flow influences fluid mechanical properties including vortex-induced vibrations (Murphy et al., 2013). Phocid vibrissae appear specifically designed to reduce vortex-induced vibrations during forward swimming.
On shore, use of the vibrissae appears to be limited to social interactions. Pinnipeds use their vibrissae predominantly under water, making it difficult to observe this behaviour in the natural habitat. Seals have been observed in the wild that were blind but nevertheless well nourished (Hyvärinen, 1989). In the light of the fact that pinnipeds have highly developed vibrissal systems while they do not possess any noticeably advanced form of biosonar (Schusterman et al., 2000), it was hypothesized that the vibrissae play a most important role in prey capture and underwater feeding.
Use of the vibrissae in underwater orientation tasks other that feeding has been investigated by Wartzok et al. (1992) and Oliver (1978). Wartzok and coauthors found that ringed seals and Weddell seals navigating under ice towards breathing holes can use their vibrissae to center within the hole, but not to find the hole. Oliver found that a blindfolded grey seal in an artificial pool could navigate through a maze of vertical rods without displacing the rods. It was suggested that the vibrissae played a role in this task.
Experiments on direct touch
Pinnipeds have been investigated for their ability to discriminate objects by touching them with their vibrissae in behavioural experiments (reviewed by Dehnhardt, 2002; Dehnhardt and Mauck, 2008). Psychophysical experiments have shown that all three groups of pinnipeds (investigated in harbour seals as representatives of the true seals, California sea lions as representatives of the eared seals, and in the walrus) can discriminate objects with high accuracy by direct touch with their vibrissae. This direct vibrissal touch is an example of a haptic sense, i. e. information from cutaneous mechanosensation and kinesthetic mechanosensation is integrated. Pinnipeds applied adequate exploratory strategies by performing head movements while whiskers were in contact with the objects. Contrary to terrestrial mammals such as rats, pinnipeds did not apply movement of whiskers relative to the head (whisking), although their mystacial vibrissae are mobile. The experimental setup for a size discrimination experiment is exemplified in Figure 5 a, b. A sea lion was trained to wait near two test objects (Perspex discs of different size) while blindfolded (Figure 5a). On an acoustic start signal, the sea lion began investigating the objects with its vibrissae (Figure 5b). The animal protracted its vibrissae as it actively investigated the objects (Figure 5b). Similar behaviour is observed in pinnipeds in experiments on shape discrimination (Dehnhardt, 1990; Dehnhardt and Dücker, 1996; Dehnhardt and Kaminski, 1995) or surface structure discrimination (Dehnhardt et al., 1998b). Alternatively, in a discrimination task where size differences between objects were large, harbour seals appeared to discriminate sizes by the number of vibrissae that were in touch with the objects (Grant et al., 2013). Sea lions performing the complex sensorimotor task of balancing balls on their snouts moved their vibrissae independently of head movements to some degree (Milne and Grant, 2014).
Tactile shape recognition in California sea lions matches their visual shape recognition in speed and reliability. Harbour seals tested in similar experiments detected size differences of objects tactually with a resolution similar to the haptic resolution of some primates. Behavioural experiments also showed that tactile sensitivity in harbour seals is not affected by ambient temperature (Dehnhardt et al., 1998b), contrary to human tactile sensitivity. Temperature measurements on vibrissal pads and inside F-SCs (Erdsack et al., 2014) confirmed the hypothesis that extensive heating of the F-SCs is responsible for this performance.
Experiments on hydrodynamic perception
True seals and eared seals can detect water movements with high sensitivity using their whiskers (Dehnhardt et al., 1998a; Dehnhardt et al., 2001; Hanke et al., 2013). Harbour seals (Phoca vitulina) detect the water movements caused by a sinusoidally vibrating sphere (hydrodynamic dipole stimuli) at water velocities down to 245 µm/s when presented with 3 s long stimuli in a go/no-go experiment (Dehnhardt et al., 1998a). Figure 6 depicts the experimental setup and results from the experiment on hydrodynamic dipole detection in harbor seals. California sea lions are even more sensitive to this kind of stimuli (Dehnhardt and Mauck, 2008). Harbour seals can not only detect hydrodynamic dipole stimuli, but also discriminate between stimuli of different amplitude (Dehnhardt and Mauck, 2008).
Harbour seals and California sea lions are also able to detect and follow hydrodynamic trails (Dehnhardt et al., 2001; Gläser et al., 2011). Hydrodynamic trails (Hanke et al., 2000) are the water movements left behind by swimming objects such as prey fish. They can last up to several minutes after a fish swam by (Hanke, 2014; Hanke and Bleckmann, 2004; Hanke et al., 2000; Niesterok and Hanke, 2013) and thus form a trail tens of meters in length that leads to a prey fish. Using this kind of stimulus, seals extend their range of hydrodynamic perception, which would otherwise be limited to a few tens of centimeters. Behavioural experiments with both species led to the conclusion that harbour seals are more accomplished hydrodynamic trail followers than California sea lions. This is in accordance with the effect of the undulated whisker structure in harbour seals that reduces vortex-induced vibrations (see above, Biomechanics).
Figure 7 exemplifies an experiment where a harbour seal followed the hydrodynamic trail generated by a miniature submarine. The submarine (Figure 7a) was remote controlled to swim arbitrary paths. The harbour seal was blindfolded and used only its vibrissae. Harbour seals can follow the swimming path of the submarine when the submarine and the animal both start at the same position (Figure 7b) or when the animal intercepts the submarine’s trail (Figure 7c) (Dehnhardt et al., 2001).
Harbour seals can extract more information from a hydrodynamic trail beyond the mere presence of an object. They can discriminate different moving directions, sizes and shapes of the objects that generated the trail (Wieskotten et al., 2010a; Wieskotten et al., 2011). Harbour seals also cope with the reduced hydrodynamic trail that passively gliding objects generate as compared to propelled objects, in line with the hypothesis that they need to pursue fish that swim in burst-and-coast mode (Wieskotten et al., 2010b). Hydrodynamic trail following can also be used to follow other seals instead of fish (Schulte-Pelkum et al., 2007). This may serve in the interaction of pups with their mothers or many other intraspecific interactions, as living in groups offers a variety of benefits (Krause and Ruxton, 2002).
Pinnipeds not only live in different climate zones, but also have different feeding habits. Accordingly, the roles of vibrissal direct touch versus vibrissal hydrodynamic perception are expected to be differently weighed across species. This is in line with the observation that most true seal species possess the undulated whisker structure that improves hydrodynamic perception while the animal swims, while eared seals and walruses do not. True seals tend to live in temperate and arctic waters where vision is more limited as compared to clear tropical waters; catching actively swimming fish when vision is low will greatly benefit from improved hydrodynamic perception. Exceptions among the true seals are the bearded seal (Erignathus barbatus) and the monk seals (Monachus spp.) that do not possess the specialized whisker structure. The former feeds on benthic prey (Marshall et al., 2006; Marshall et al., 2008 and references therein), while the latter live in clear tropical or subtropical waters.
Different true seal species (Phocidae) possess similar numbers of nerve fibers per vibrissa (Hyvärinen, 1989; Marshall et al., 2006; McGovern et al. 2014) (note that fiber counts for eared seals or walruses are not yet available). The picture emerges that numbers of axons per F-SC are similar in different pinniped species. Another marine carnivore, the sea otter (Enhydra lutris), possesses a similar number of nerve fibers per F-SC as pinnipeds (Marshall et al., 2014), adding to this picture for marine carnivores. Differences between species appear to manifest themselves mainly in the number of F-SC of the mystacial array, their arrangement on the snout, and the morphology of the hair shafts.
True seals (Phocidae) are mostly opportunistic feeders with a broad prey spectrum including pelagic and benthic species, and their vibrissae are adapted to both feeding situations. The two pinniped species that are most specialized for benthic feeding are the bearded seal (Erignathus barbatus, Phocidae) and the walrus (Odobenus rosmarus, Odobenidae). They possess the best endowed vibrissal systems in terms of number of vibrissae and therefore also total nerve fibers (Marshall et al., 2006), indicating that vibrissal systems designed for direct touch may generally have higher counts of vibrissae and F-SCs than vibrissal systems designed for hydrodynamic perception.
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