Tactile sensing in the naked mole rat

• Dr. Christine M Crish, Northeast Ohio Medical University, Rootstown, OH, United States

• Dr. Samuel D Crish, Northeast Ohio Medical University, Rootstown, OH, United States

• Prof. Christopher Comer, Division of Biological Sciences, University of Montana, Missoula, Montana, USA

Tactile sensing in the naked mole rat refers to the ability of this naturally blind species to respond to, and localize, stimuli that deflect facial vibrissae, but also an array of somatic vibrissae.

Naked mole-rat sensory world

Naked mole-rats (Heterocephalus glaber) are eusocial rodents that spend their entire lives in extensive subterranean burrows where visual and auditory cues are poor. As such, they have reduced their dependence on these systems; they exhibit microphthalmia and have small external ears (Fig 1.; Hetling et al., 2005). Form vision is essentially lost, with related atrophy of brain structures dedicated to processing vision (Catania and Remple, 2002; Crish et al., 2006a). However, structures mediating circadian rhythms in the naked mole-rat brain appear relatively normal (Crish et al., 2006a), the retina does respond to light (Hetling et al., 2005), and they can be entrained to light cues (Riccio and Goldman, 2000a,b). This is a similar degree of highly limited visual processing to that present in other subterranean mammals, such as the blind mole rat (Spalax ehrenbergi; Cooper et al., 1993)1. Naked mole-rats also have poor high frequency hearing and an inability to localize sound effectively (Heffner and Heffner, 1993). Little is known about their chemical senses. They display what appears to be scent marking, but unlike other rodents, they have an underdeveloped vomeronasal organ necessary for pheromone sensation (Smith et al., 2007).

Figure 1: Photograph of two adult naked mole-rats. Note the small eyes, reduced auditory pinnae, and prominent sensory body hairs that line the body and tail.

Somatosensation

Like many other underground mammals such as the star-nosed mole, naked mole-rats have a highly derived somatosensory system. This system consists of increased capabilities compared with “standard” rodent features, addition of new features, and loss of functions (such as certain types of pain).

Skin

As their name indicates, naked mole rats lack fur that characterizes nearly all mammals except for humans, cetaceans, and manatees. They are not completely devoid of dermal appendages however. In addition to a dense array of facial vibrissae characteristic of rodents, they have a sparse arrangement of stiff sensory hairs (body vibrissae) on the rest of their head and along the entire body, including the tail. These “vibrissae” lack the blood sinus characteristic of true vibrissae but are heavily innervated. Thus they resemble guard hairs that are found interspersed among the fur of many mammals. The mechanism by which naked mole-rats have lost insulating fur but retained these dermal specializations is unknown.

The body vibrissae are not randomly arranged on the body but occur in a more or less regular array of about 40-50 receptors on each side of the body (Crish et al., 2003). In this sense, they share some general organizational similarities with arrays of somatic receptors in a few other mammals including manatees and rock hyraxes (Reep et al., 1998; 2007).

These mole-rat body vibrissae are not vestigial remnants left after evolutionary loss of fur. These receptors mediate a well-organized topographic orienting behavior (Fig. 2. Crish et al., 2003). This indicates that spatial information from these hairs is processed centrally in a distinct, systematic way. This non-visual orienting behavior has been shown by lesion studies to be mediated, at least in part, by the superior colliculus (Crish et al., 2006b). This midbrain area is well known for its involvement in visual orientation and multisensory integration in mammals. Mole-rats seem to provide an intriguing case where the midbrain tectum has reduced or lost its circuitry for visual orientation but retained components that process non-visual spatial information in parallel to the more typical visual circuitry.

The skin between hairs is also unusual when compared to other mammals. It is heavily innervated by a-delta fibers which transmit certain types of pain and temperature information to the central nervous system. C-fibers, which carry other types of painful stimuli, are absent, and the CNS shows a lack of CGRP-positive cells in early somatosensory processing areas (Park et al., 2008). Because of this absence naked mole-rats lack the ability to sensitize to chemicals such as capsaicin and are relatively unperturbed by acid and formalin challenge (Park et al., 2008).

Naked-mole rat burrow systems present a very atypical mammalian environment. The temperature in mole-rat burrows remains fairly constant and the concentration of carbon dioxide is unusually high. Not surprisingly, naked mole-rats are poikilothermic (unable to physiologically regulate their own body temperature) and huddle together for warmth as well as move to warmer areas when their core temperature is low. Additionally, there is speculation that the loss of CGRP positive components of the pain system is related to the fact that these components may play a role in signaling pain toward high CO2 concentrations (Park et al., 2008).

Figure 2: Panel A. Schematic depicting distribution of sensory body hairs on the dorsal and lateral surfaces of a naked mole-rat. Tactile stimulation of hairs in the numbered rostral-caudal zones shown on the schematic produce a topographic turning response that orients the mole-rat’s snout to the locations depicted by the arrows in Panel B. For example, stimulation of the extreme caudal hairs in zone 5 produce the greatest magnitude turns. Figure adapted from Crish et al. Brain, Behavior & Evolution, 62(3): 145-51. Copyright 2003 with permission from Karger Publishers.

Teeth

As evident in Figure. 1, naked mole-rats have prominent upper and lower incisors that are used for a range of tasks that include digging through harsh substrates, harvesting food, manipulating objects, and delicately carrying pups. The mandibular symphysis in the naked mole-rat jaw is unusually flexible, enabling them to move their contralateral lower incisors independently. Both upper and lower incisors are also highly sensitive to tactile stimulation, with each incisor having its own receptive field in primary somatosensory cortex (Catania & Remple, 2002; Henry et al., 2006). In fact, these 4 upper and lower teeth have a hypertrophied representation in the brain-- occupying 10% of the entire neocortex (Catania & Remple, 2002).

Brain structures involved in sensation and perception

Naked mole-rats have a large primary somatosensory cortex (S1) that significantly extends into the extreme caudal-medial cortices that are usually dominated by primary visual cortex (V1) and other visual areas. Somatosensory cortex accounts for 47% of all sensory-related cortices in the naked mole-rat, contrasting with 27% of cortical sensory tissue in other rodents with well-developed somatosensory systems such as the rat (Fig. 3; Catania & Remple, 2002). The incisors occupy approximately 1/3 of naked mole-rat S1 (Catania & Remple, 2002), suggesting a specialized role for teeth in the uniquely enhanced somatosensory system of this animal.

Naked mole-rat subcortex also has some striking features. Areas responsible for visual processing such as the superficial superior colliculus, lateral geniculate nucleus, and central zone of the cerebellum are greatly reduced (Crish et al., 2006; Marzban et al., 2011; Sarko et al., 2013). It is unknown whether these areas do not form normally or develop and then degenerate; recent investigations indicate that the superficial SC and LGN are reduced at birth (Dengler-Crish et al., 2013).

Like cortex, areas of the brainstem and cerebellum responsible for processing somatosensation are expanded (Henry et al., 2008; Marzban et al., 2011; Sarko et al., 2013). The deep superior colliculus, which contains visual, auditory, and somatosensory information in other animals, exhibits normal organization. Lesions of this structure abolish the tactile orienting behavior to stimulation of body vibrissae (Crish et al., 2003).

Figure 3: Panel A. Map of flattened naked mole-rat neocortex depicting electrode penetrations from electrophysiological recording experiments where neurons responded to tactile stimulation of the body surface. Color-coded regions indicate the extent of the representation of each body part. Note the large representation of the teeth as indicated in green. Panel B. Map of sensory cortices in the rat neocortex can contrasted with the same map (Panel C) in naked mole-rats. Note the expansion of primary somatosensory cortex (S1) in naked-mole rat and relative absence of primary visual (V1) and auditory (A1) cortices compared to the laboratory rat. Figures reprinted from Catania, KC and Remple MS. 2002. PNAS, 99 (5) 5692-7, Figures 2 & 4. Copyright 2002, The National Academy of Sciences.

Computational properties of somatosensory function

There are very few instances in which the computational abilities of touch-sensory processing in mammals have been amenable to investigation. However naked-mole-rats have yielded some very clear information on this processing. Studies of the tactile orienting behavior of naked mole-rats in response to deflection of their sensory body hairs have shown that the brains of these animals use computational strategies similar to that shown in other mammals’ midbrain-mediated visual orienting responses (i.e. saccades). Deflecting two unilateral sensory hairs in located in rostral and caudal trunk regions of naked mole-rats will produce an orienting response to a location intermediate of the two regions (Fig. 4). This outcome suggests that neural activity is averaged across the active populations of neurons in one hemisphere of the superior colliculus to produce this movement (Crish et al., 2006). Other computational strategies are employed by collicular neurons when naked mole-rat sensory hairs in the same rostral-caudal plane are stimulated on contralateral sides of the body—producing a turn to one side or the other but no intermediate response (Crish et al., 2006). This strategy known as “winner-take-all” has been demonstrated previously in the visual orienting responses of primates (Groh, 1998).

Figure 4: Data from behavioral experiments investigating neuronal population coding strategies in the tactile orienting response of naked mole-rats. Two vibrissa were stimulated either individually or simultaneously and the schematic shows the approximate location of the vibrissae tested [red arrowheads] on a gray drawing of an animal. Circular histograms display the distribution of turns elicited by each stimulus condition [blue bars] and the mean turn vector [red arrow] is also shown. Panel A shows orienting turns produced when deflecting sensory hairs in unilateral rostral and caudal regions. Simultaneous deflection produces an intermediate response indicative of a neuronal averaging computation. Panel B shows orienting turns elicited by stimulating sensory hairs bilaterally in the rostral plane. Simultaneous deflection produces a turn towards one side or the other, indicative of a winner-take-all neuronal computational strategy. Figure adapted from Crish et al. Neuroscience, 139(4): 1461-6. Copyright 2006 with permission of Elsevier.

1Naked mole-rats are Bathyergid rodents, a family of more than a dozen species found in sub-Saharan Africa. Blind mole rats are taxonomically quite distinct. They are in the Family Spalicidae (notice lack of hyphen for rodents in this taxon) and inhabit the eastern Mediterranean region.

References

• 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(8): 5692–5697. doi:10.1073/pnas.072097999.

• Cooper, H M; Herbin, M and Nevo, E (1993). Visual system of a naturally microphthalmic mammal: The blind mole rat, Spalax ehrenbergi. Journal of Comparative Neurology 328(3): 313-350.

• Crish, S D; Rice, F L; Park, T J and Comer C M (2003). Somatosensory organization and behavior in naked mole-rats I: Vibrissa-like body hairs comprise a sensory array that mediates orientation to tactile stimuli. Brain, Behavior and Evolution 62(3): 141-151.

• Crish, S D; Dengler-Crish, C M and Catania, K C (2006a). Central visual system of the naked mole-rat (Heterocephalus glaber). The Anatomical Record. Part A, Discoveries in Molecular, Cellular, and Evolutionary Biology 288(2): 205-212.

• Crish, S D; Dengler-Crish, C M and Comer, C M (2006b). Population coding strategies and involvement of the superior colliculus in the tactile orienting behavior of naked mole-rats. Neuroscience 139(4): 1461-1466.

• Dengler-Crish, C M and Crish, S D (2013). Postnatal development of the subcortical visual system in naked mole-rats. Presented at the Society for Neuroscience Annual Meeting.

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• Sarko, D K; Leitch, D B and Catania, K C (2013). Cutaneous and periodontal inputs to the cerebellum of the naked mole-rat (Heterocephalus glaber). Frontiers in Neuroanatomy 7: 39. doi:10.3389/fnana.2013.00039.

• Smith, T D; Bhatnagar, K P; Dennis, J C; Morrison, E E and Park, T J (2007). Growth-deficient vomeronasal organs in the naked mole-rat (Heterocephalus glaber). Brain Research 1132(1): 78-83.

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

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

Reviewed by: Prof. Ehud Ahissar, Department of Neurobiology, The Weizmann Institute, Rehovot

Accepted on: 2015-03-23 19:34:43 GMT