Tactile hair in Manatees

• Prof. Roger Reep, McKnight Brain Institute, University of Florida

• Dr. Diana K. Sarko, Vanderbilt University, Nashville, TN, USA

Figure 1: Manatee face. The oral disk (od) is flared and its bristle-like hairs are everted. The large perioral bristles of the upper lip (U2) are withdrawn into their fleshy pad. Reproduced from Reep and Sarko (2006) with permission from Elsevier Press.

Tactile hairs function to detect mechanosensory stimuli rather than for warmth or protection, which is the main function of pelage hair. Vibrissae, which have a specific set of structural features, are the main class of tactile hair.

Manatee hair

Figure 2: Schematic drawings of the structure and innervation of manatee tactile hair follicle-sinus complexes. These correspond externally to the large bristles on the upper lip (U2), intermediate bristle-like hairs on the oral disk (BLH), and thin hairs on the postfacial body. Several types of axons and nerve endings are found, resulting in a complex receptor anatomy. Reproduced from Sarko et al. (2007) with permission from Wiley-Liss.

Florida manatees (Figure 1) have ~5300 vibrissae scattered over the entire body, with ~2000 on the face and ~3300 on the postfacial body (Reep et al., 1998). This is unusual because in other mammals vibrissae are generally confined to the face area (whiskers), with some taxa exhibiting a few vibrissae on the limbs or ventrum (Sokolov and Kulikov, 1987). The follicles associated with vibrissae differ from those of other hairs in being associated with a circumferential blood sinus, dense connective tissue capsule, and a variety of mechanoreceptors that are extensively innervated. Because of these distinctions they are referred to as Follicle-Sinus Complexes (FSCs). Vibrissae are specialized for detecting movement rather than for providing protection or warmth. Manatees and dugongs are unique among mammals in having only vibrissae and no other type of hair on their bodies. Why is this the case?

The rock hyrax, one of the closest living relatives of manatees, has vibrissae interspersed among its fur (or pelage) over the entire body (Reep et al., 2007). Since vibrissae are part of highly specialized and well-innervated FSCs, the elaboration of their distribution to the entire body in both manatees and hyraxes indicates a dedication of neural resources (and by extension, perceptual capabilities) to somatosensation. Naked mole-rats have only sparsely scattered hairs that are sensory but these do not have the structural features of vibrissae, possibly representing an example of convergent evolution. For each of these species, elaboration of the tactile system appears to compensate for a reduced reliance on visual cues. This raises an interesting evolutionary question: is the condition of having vibrissae distributed over the entire body a primitive or derived mammalian condition? Furthermore, what developmental mechanisms may have been modified to produce an arrangement of vibrissae on the entire body as opposed to the distribution limited to restricted regions that occurs in most species?

Facial vibrissae

Two prominent features of the manatee facial region are a broad oral disk (analogous to the mystacial region in other mammals) containing ~600 bristle-like hairs (thin vibrissae) and six distinct paired fields of perioral bristles (thick vibrissae), each containing 8-30 vibrissae per side. Vibrissae in each of these regions of the face vary with respect to length, diameter, and innervation density (Reep et al., 1998; 2001). The largest, stoutest vibrissae are found on the lateral margin of each upper lip. Vibrissae of the oral disk are much thinner than the perioral bristles (diameter/length ratio of ~0.03 vs. 0.30). The number of axons innervating perioral bristles ranges from 70-225 per FSC; the number innervating vibrissae of the oral disk is ~54 per FSC. It is estimated that there is a total of ~110,000 axons innervating the ~2000 facial FSCs. This is comparable to the ~100,00 axons that innervate the nasal appendages in the star-nosed mole (Catania and Kaas, 1997), another tactile specialist.

Vibrissae of the oral disk are used for tactile investigation of objects. In the relaxed state the oral disk vibrissae are withdrawn into the fleshy folds of skin of the oral disk. As a manatee approaches an object to be investigated, it engages in a ‘flare response’, in which orofacial muscles contract to flatten and expand the oral disk (Marshall et al., 1998). This causes the vibrissae of the oral disk to extend outward as a collective sensory array that is used to perform tactile investigations during direct contact with objects. These investigations can take the form of brief touches or sweeping scans.

Perioral bristles are used to grasp objects, including plants that are ingested during feeding (Marshall et al., 1998). Because this grasping involves the face rather than the hand, it is referred to as ‘oripulation’. Often, tactile scanning by the oral disk is followed by vigorous, repetitive oripulation by the large perioral vibrissae on the upper lips. This occurs not only with plants during feeding, but also during investigation of novel objects including anchor lines, bathing suits, and human legs. Such a behavioral specialization may be indicative of extensive sensorimotor integration within the central nervous system representations for the face. Psychophysical tests of a few captive subjects have demonstrated that tactile acuity by manatees using the vibrissae of the face is at least as good as that of an elephant using the tip of its trunk (Weber fraction of 3-14%; Bachteler and Dehnhardt, 1999; Bauer et al., 2005). Interestingly, the eyes often close during feeding, which may heighten tactile acuity.

Postfacial vibrissae

The postfacial vibrissae are not actively involved in tactile exploration. It has been hypothesized that they function to detect water movements, thus functioning like a mammalian version of the lateral line system found in fishes and amphibians (Reep et al., 2002). This possibility is currently being examined through behavioral psychophysics experiments involving two captive manatees at Mote Marine Laboratory. Such an ability would be useful for detecting water movements associated with conspecifics, tides, and currents. It may also function to detect energy reflected from objects as a manatee moves underwater, thereby assisting in navigating the murky water environment in which manatees spend much of their time.

Postfacial vibrissae are smaller and thinner (diameter/length ratio of ~0.01) than those on the face, and their FSCs are less extensively innervated (~30 axons/ FSC) (Reep et al., 2002). However, innervation density appears to scale with size of FSC (Reep et al., 2001), perhaps preserving a relatively constant innervation density per unit area. Considering that there are ~3300 postfacial FSCs innervated by ~30 axons/FSC, this represents a total investment of ~100,000 axons.

Innervation of FSCs

Immunolabeling studies have revealed that all manatee FSCs (Figure 2) have large Aß fibers terminating as club endings, longitudinal lanceolate endings, and Merkel endings (Sarko et al., 2007a). The particularly dense distribution of Merkel endings indicates that manatees may be especially attuned to detecting the directionality of follicle deflection. Other types of endings generally seen in mammalian FSCs at a deeper level of the FSC known as the cavernous sinus include reticular and spiny endings; these mechanoreceptors were notably absent in manatees and may have been functionally replaced by a novel type of nerve ending thought to be adaptive to the aquatic environment. This novel ending, termed a “trabecular ending,” was found only in facial FSCs and terminates along the connective tissue traversing between the FSC capsule and the basement membrane at the cavernous sinus level. A second novel mechanoreceptor type discovered in the same study consisted of gigantic, spindle-shaped “tangle” endings abutting the mesenchymal sheath at the lower extent of the inner conical body level of all FSCs studied. Both novel types of nerve endings, the trabecular and tangle endings, appear to be low-threshold mechanoreceptors (as indicated by positive BNaC labeling) and may confer additional directionality detection at the lower and upper levels of each FSC, respectively. The stout perioral follicles involved in oripulation displayed an additional specialization - the medullary core of the hair papilla exhibited dense, superficially extensive, small-caliber innervation. This adaptation is thought to allow these specialized vibrissae to detect force applied to the follicle with extremely little displacement of the follicle, much like what occurs in tooth pulp.

Vibrissal information and the brain

A total of >200,000 axons is devoted to conveying neural signals from the manatee vibrissal FSCs to the central nervous system. This is a sizable investment, and implies that rather elaborate CNS machinery is required to analyze this information. Regions of the brainstem, thalamus, and cerebral cortex dedicated to somatic sensation are disproportionately large, and exhibit lobulations or specialized cell aggregations indicative of functional compartmentalization.

Brainstem

Figure 3: Within the cuneate-gracile complex of the brainstem are separate zones hypothesized to correspond to representations of tactile information coming from the fluke, body, and flipper. Tactile information from the face reaches the trigeminal complex (Sp5c). Reproduced from Sarko et al. (2007) with permission from Wiley-Liss.

Histochemical assessments of the manatee brainstem (Figure 3), combined with analysis of cytoarchitecture, have shown that the brainstem nuclei dedicated to somatosensation are well-developed (Sarko et al., 2007b). Subdivisions of the trigeminal nucleus, receiving sensory inputs from the face, revealed dense cytochrome oxidase staining and parcellation potentially related to the oral disk and perioral divisions of facial vibrissae. The cuneate-gracile complex, which represents sensory input from the upper and lower body, also stained densely for cytochrome oxidase and appeared lobulated. Bischoff’s nucleus, which has been noted in animals with functionally important tails, is large in manatees and is thought to represent the fluke. The facial motor nucleus, which innervates the facial musculature involved in the flare response and oripulation, is also large and parcellated (Marshall et al., 2007). Although the manatee cerebral cortex contains cellular aggregates similar to “barrels” (see below), which are the functional representations of vibrissae in other taxa, no definitive counterparts (“barrelettes”) were seen in the brainstem.

Thalamus

Within the thalamus, the principal nucleus devoted to somatosensation (the ventroposterior nucleus, or VP) was disproportionately large compared to nuclei receiving inputs predominantly from other sensory modalities. In fact the lateral geniculate nucleus, devoted to visual inputs, appears greatly diminished in size and displaced by somatosensory and auditory nuclei (Sarko et al., 2007b). As in the brainstem, no definitive counterparts to cortical barrels (“barreloids” in the thalamus) were seen in the manatee.

Cerebral Cortex

Figure 4: Sensory areas of cerebral cortex as revealed by cytochrome oxidase staining. Yellow areas are presumed visual cortex, green areas are presumed auditory cortex. Red areas are presumed somatic sensory cortex, which includes regions thought to represent the fluke (a), flipper (b), tactile hairs of the perioral face (c), and tactile hairs of the oral disk and postfacial body (d). Reproduced from Reep and Sarko (2006) with permission from Elsevier Press.

Based on flattened cortex preparations using cytochrome oxidase staining to delineate primary sensory areas, the presumptive primary somatosensory cortex (SI) (see Figure 4) occupies approximately 25% of total cortical area (comparable to 31% of neocortex in naked mole-rats; Catania and Remple, 2002). In contrast, presumptive primary visual and auditory cortices combined occupied 4-17% of total cortex in the specimens examined (Sarko and Reep, 2007).

One of the most definitive and intriguing specializations within the sirenian CNS is the Rindenkerne (‘cortical nuclei’; Figure 5), first described by Dexler in 1912. Rindenkerne are aggregates of neurons found in layer VI of the presumptive somatosensory cortex (Reep et al., 1989; Marshall and Reep, 1995). The largest Rindenkerne are found in the presumed face area. Rindenkerne stain positively for cytochrome oxidase and acetylcholinesterase. These features, together with their location, suggest that Rindenkerne may be the sirenian counterpart to the neuron aggregates known as barrels, which are found in layer IV of the face area in rodents and marsupials. Barrels are known to constitute a topographic array in which each barrel processes information related to one vibrissa. Thus, it may be that Rindenkerne represent another case of convergent evolution. Some Rindenkerne are found in presumed auditory cortex. This may represent a region of overlap between somatosensory and auditory processing, perhaps reflecting the ability of low frequency energy to stimulate the postfacial vibrissae, and the inherent continuity between these two modes of detecting vibratory stimuli.

Figure 5: Rindenkerne are clusters of neurons hypothesized to process information from individual tactile hairs. Here they appear as light oval regions (arrows) in layer VI of areas CL1 and CL2 within presumed somatic sensory cerebral cortex. Reproduced from Reep and Sarko (2006) with permission from Elsevier Press.

References

• Bachteler, D and Dehnhardt, G (1999). Active touch performance in the Antillean manatee: Evidence for a functional differentiation of facial tactile hairs. Zoology 102: 61-69.
• Bauer, G B et al. (2005). Tactile discrimination by Florida manatees, Trichechus manatus latirostris. Presented at the Conference on the Biology of Marine Mammals, San Diego, December 2005.
• Catania, K C and Kaas, J H (1997). Somatosensory fovea in the star-nosed mole: Behavioral use of the star in relation to innervation patterns and cortical representation. Journal of Comparative Neurology 387: 215-233.
• Catania, K C and Remple, M S (2002). Somatosensory cortex dominated by the representation of teeth in the naked mole-rat brain. Proceedings of the National Academy of Sciences of the United States of America 99: 5692-5697.
• Marshall, C D; Vaughn, S D; Sarko, D K and Reep, R L (2007). Topographical organization of the facial motor nucleus in Florida manatees (Trichechus manatus latirostris). Brain, Behavior and Evolution 70: 164-173.
• Marshall, C D and Reep, R L (1995). Manatee cerebral cortex: Cytoarchitecture of the caudal region in Trichechus manatus latirostris. Brain, Behavior and Evolution 45: 1-18.
• Marshall, C D; Huth, G D; Edmonds, V M; Halin, D L and Reep, R L (1998). Prehensile use of perioral bristles during feeding and associated behaviors of the Florida manatee (Trichechus manatus latirostris). Marine Mammal Science 14: 274-289.
• Reep, R L and Sarko, D K (2006). Somatosensory specializations in the nervous systems of manatees. In: J H Kaas (Ed.), Evolution of Nervous Systems, Vol. 3 (pp. 207-214). Oxford: Elsevier.
• Reep, R L and Bonde, R K (2006). The Florida Manatee: Biology and Conservation. University Press of Florida. 189.
• Reep, R L; Sarko, D K and Rice, F L (2007). Rock hyraxes (Procavia capensis) possess vibrissae over the entire postfacial body. Poster presented at Society for Neuroscience.
• Reep, R L; Marshall, C D and Stoll, M L (2002). Tactile hairs on the postcranial body in Florida manatees: A mammalian lateral line? Brain, Behavior and Evolution 59: 141-154.
• Reep, R L; Marshall, C D; Stoll, M L; Homer, B L and Samuelson, D A (2001). Microanatomy of facial vibrissae in the Florida manatee: The basis for specialized sensory function and oripulation. Brain, Behavior and Evolution 58: 1-14.
• Reep, R L; Marshall, C D; Stoll, M L and Whitaker, D M (1998). Distribution and innervation of facial bristles and hairs in the Florida manatee (Trichechus manatus latirostris). Marine Mammal Science 14: 257-273.
• Reep, R L; Johnson, J I; Switzer, R C and Welker, W I (1989). Manatee cerebral cortex: Cytoarchitecture of the frontal region in Trichechus manatus latirostris. Brain, Behavior and Evolution 34: 365-386.
• Sarko, D K; Rice, F L; Reep, R L and Mazurkiewicz, J E (2007a). Adaptations in the structure and innervation of follicle-sinus complexes to an aquatic environment as seen in the Florida manatee (Trichechus manatus latirostris). Journal of Comparative Neurology 504: 217-237.
• Sarko, D K; Johnson, J I; Switzer, R C; Welker, W I and Reep, R L (2007b). Somatosensory nuclei of the brainstem and thalamus in Florida manatees. The Anatomical Record 290: 1138-1165.
• Sarko, D K and Reep, R L (2007). Somatosensory areas of manatee cerebral cortex: Histochemical characterization and functional implications. Brain, Behavior and Evolution 69: 20-36.
• Sokolov, V E and Kulikov, V F (1987). The structure and function of the vibrissal apparatus in some rodents. Mammalia 51: 125-138.

Internal references

• Llinas, R (2008). Neuron. Scholarpedia 3(8): 1490. http://www.scholarpedia.org/article/Neuron.

• Sherman, S M (2006). Thalamus. Scholarpedia 1(9): 1583. http://www.scholarpedia.org/article/Thalamus.

Recommended Reading

• Hughes, H C (2001). Sensory Exotica Cambridge, MA: MIT Press.

See also

tactile sensing in the naked mole rat, tactile exploration

Sponsored by: Prof. Tony J. Prescott, Dept Psychology, Univ of Sheffield, UK

Reviewed by: Anonymous

Reviewed by: Prof. Guido Dehnhardt, Institut fur Biowissenschaften, University of Rostock, Germany

Reviewed by: Dr. Wolf Hanke, Institute for Biosciences, University of Rostock, Rostock, Germany

Accepted on: 2009-03-20 15:59:47 GMT