Somatosensory cortex dominated by the representation of teeth in the naked mole-rat brain

Abstract

We investigated naked mole-rat somatosensory cortex to determine how brain areas are modified in mammals with unusual and extreme sensory specializations. Naked mole-rats (Heterocephalus glaber) have numerous anatomical specializations for a subterranean existence, including rows of sensory hairs along the body and tail, reduced eyes, and ears sensitive to low frequencies. However, chief among their adaptations are behaviorally important, enlarged incisors permanently exterior to the oral cavity that are used for digging, object manipulation, social interactions, and feeding. Here we report an extraordinary brain organization where nearly one-third (31%) of primary somatosensory cortex is devoted to the representations of the upper and lower incisors. In addition, somatosensory cortex is greatly enlarged (as a proportion of total neocortical area) compared with closely related laboratory rats. Finally, somatosensory cortex in naked mole-rats encompasses virtually all of the neocortex normally devoted to vision. These findings indicate that major cortical remodeling has occurred in naked mole-rats, paralleling the anatomical and behavioral specializations related to fossorial life. N aked mole-rats (Heterocephalus glaber) are rodents in the family Bathyergidae that lead an almost entirely subterranean existence. They are best known for their eusocial colony structure with morphological castes, division of labor, and a single breeding female or ''queen'' (1-5). In addition to their unique social organization, naked-mole rats are renowned for their unusual physical appearance-a consequence of their many adaptations to underground life. They exhibit a suite of anatomical traits that set them apart from most other rodents. These traits include reduced eyes and small ears with a hearing range restricted primarily to the low frequencies that are easily transmitted through soil (6, 7). Naked mole-rats also have sensory and motor specializations related to touch.Most rodents have an array of sensory vibrissae on the face and distal snout, and this is also true for naked mole-rats. In addition, naked mole-rats have unique rows of sensory hairs covering their otherwise furless bodies and tail (Fig. 1). Using these postcranial sensory hairs they have little trouble navigating without eyesight and are easily able to travel both forward and backward through their underground tunnels. But the hallmark specialization of mole-rats is the enlarged incisors that are located permanently exterior to the oral cavity. This dentition plays an important role in the daily lives of the mole-rat worker caste, and it has been reported that 25% of their total musculature is devoted to the jaws (8). To examine how mole-rats use these teeth, we filmed them manipulating small wooden sticks and chewing through obstructions within a Plexiglas tunnel system. Slow-motion analysis revealed their remarkable ability to move the lower pair of incisors independently of one another (Fig. 1 F and G). This ability presumably allows for greater versatility ...

Central visual system of the naked mole‐rat (Heterocephalus glaber)

“…These findings support the conclusion suggested from investigation of peripheral structures (Nikitina et al, 2004;Hetling et al, 2005) and cortical mapping (Catania and Remple, 2002) that naked mole-rats lack the ability to form visual images. Although form vision may be lost in these mammals, a well-organized LGN is not required for light detection, pupil constriction, and contrast cues (Kaas and Huerta, 1988) and evidence suggests that these visual abilities may be conserved in naked mole-rats (Nikitina et al, 2004).…”

“…The naked mole-rat has a sizable, moderately innervated SCN, suggesting that it has selectively retained the ability to detect light for photoentrainment. (Catania and Remple, 2002) were severely atrophied. Considering the mole-rat lives in an environment where visual cues are almost nonexistent, a well-developed, metabolically costly visual system would be of little or no use.…”

“…However, naked mole-rats are somatosensory specialists with a novel array of somatic vibrissae for guiding orienting behavior (Crish et al, 2003a;Park et al, 2003) and large front incisors used for digging tunnels and manipulating objects. They have a correspondingly hypertrophied somatosensory cortex for processing tactile information that includes a greatly expanded representation of the dentition (Catania and Remple, 2002). …”

Central Projections of Trigeminal Afferents Innervating the Face in Naked Mole‐Rats (Heterocephalus glaber)

“…S1 itself is 50% larger (as a proportion of total neocortex) in mole-rats compared with laboratory rats (Catania and Remple, 2002). Within S1, the two contralateral incisors take up a remarkable 30% of the body representation (Catania and Remple, 2002;Henry et al, 2006). This expansion of the dental representation seems to reflect the importance of the front teeth in mole-rat behavior.…”

“…Both the facial vibrissae and the incisors have large representations in primary somatosensory cortex (S1). S1 itself is 50% larger (as a proportion of total neocortex) in mole-rats compared with laboratory rats (Catania and Remple, 2002). Within S1, the two contralateral incisors take up a remarkable 30% of the body representation (Catania and Remple, 2002;Henry et al, 2006).…”