S. D. Crish

Somatosensory Organization and Behavior in Naked Mole-Rats I: Vibrissa-Like Body Hairs Comprise a Sensory Array That Mediates Orientation to Tactile Stimuli

Orientation guided by mechanosensory stimuli is a fundamental behavior that has been analyzed most effectively in simple systems, but has been difficult to assess in mammals. This study demonstrates that sparsely distributed sensory ‘hairs’ on the body of naked mole-rats provide an ideal detector array for the assessment of touch guided orienting behavior. Naked mole-rats are fully subterranean rodents that are functionally blind and lack fur. About 40 tactile hairs (resembling facial vibrissae) are found on each side of the body, and they are systematically organized in a grid-like pattern from head to tail. Deflection of a single body hair triggered a highly accurate orientation of the snout toward the point of stimulation, thus topographically organized motor behavior can be elicited from this sensory array. This orienting behavior is specific to the body hair system: touch of intervening skin evoked responses less reliably, and observed responses were not topographically organized. Orientation elicited from this array was accurate regardless of the head-to-body position at the time of hair stimulation indicating that the orienting motor score takes relative head position into account. The consistent pattern of these hairs coupled with robust orienting behavior indicates that this mammalian model provides an appropriately simple system for analyzing the neuronal basis of sensorimotor integration involved in tactile orienting behavior.

Population coding strategies and involvement of the superior colliculus in the tactile orienting behavior of naked mole-rats

Even simple behaviors of vertebrates are typically generated by the concerted action of large numbers of brain cells. However, the mechanisms by which groups of neurons work together as functional populations to guide behavior remain largely unknown. One of the major model systems for exploring these mechanisms has been mammalian visuomotor behavior. We describe here experiments that establish a new model system for analyzing the sensory control of behavior by neuronal populations using a mammalian somatosensory response: orientation to touch cues in a rodent. We found that the CNS mechanisms used to direct these orientation responses to touch can be delineated from behavioral experiments. In this study we demonstrate that the superior colliculus, a component of the vertebrate midbrain most often thought of as a visual structure, is an essential component of the naked mole-rats unique tactile orienting behavior. Furthermore, the information processing that underlies this behavior displays striking parallels with that used for visual orientation at anatomical and computational levels.

Somatosensation in the superior colliculus of the star-nosed mole

The superior colliculus (or optic tectum in nonmammals) plays a critical role in the visual system and is essential for integrating sensory inputs to guide eye and head movements. However, what is the role of the superior colliculus (SC) in species that depend almost exclusively on touch? In this study we examined the SC of the star‐nosed mole, a subterranean mammal that, instead of using vision, explores its environment using its tactile star. The star acts like a mechanosensory eye with a central tactile fovea that is constantly shifted in a saccadic manner. Multiunit microelectrode recordings were used to determine the topography and receptive field organization of somatosensory inputs to the SC and to test for visual and auditory responses. Here we report an SC dominated by somatosensory inputs in which neurons in all layers responded to mechanosensory stimulation, forming a topographic representation of contralateral body dominated by the mechanosensory star. Receptive fields were large, and appendage representations overlapped, suggesting that the SC may use a distributed, population code to guide the saccadic movements of the moles touch fovea. No auditory or visual responses were recorded from the SC, although neurons in the neighboring inferior colliculus responded to auditory stimuli. Layers IVb–VII were identified, and a layer superficial to IVb contained neurons that responded to somatosensory stimulation, suggesting that there are unique patterns of afferents in the star‐nosed moles SC. J. Comp. Neurol. 464:415–425, 2003.

Underdeveloped extraocular muscles in the naked mole-rat (Heterocephalus glaber).

The extraocular muscles (EOM), the effector arm of the ocular motor system, have a unique embryological origin and phenotype. The naked mole‐rat (NMR) is a subterranean rodent with an underdeveloped visual system. It has not been established if their ocular motor system is also less developed. The NMR is an ideal model to examine the potential codependence of oculomotor and visual system development and evolution. Our goal was to compare the structural features of NMR EOMs to those of the mouse, a similar sized rodent with a fully developed visual system. Perfusion‐fixed whole orbits and EOMs were dissected from adult NMR and C57BL mice and examined by light and electron microscopy. NMR orbital anatomy showed smaller EOMs in roughly the same distribution around the eye as in mouse and surrounded by a very small Harderian gland. The NMR EOMs did not appear to have the two‐layer fiber distribution seen in mouse EOMs; fibers were also significantly smaller (112.3 ± 46.2 vs. 550.7 ± 226 sq μm in mouse EOMs, *P < 0.05). Myofibrillar density was less in NMR EOMs, and triad and other membranous structures were rudimentary. Finally, mitochondrial volume density was significantly less in NMR EOMs than in mouse EOM (4.5% ± 1.9 vs. 21.2% ± 11.6, respectively, *P < 0.05). These results demonstrate that NMR EOMs are smaller and less organized than those in the mouse. The “simpler” EOM organization and structure in NMR may be explained by the poor visual ability of these rodents, initially demonstrated by their primitive visual system. Anat Rec, 2010.