The Star-Nosed Mole Reveals Clues to the Molecular Basis of Mammalian Touch

Gerhold, Kristin A.; Pellegrino, Maurizio; Tsunozaki, Makoto; Morita, Takeshi; Leitch, Duncan B.; Tsuruda, Pamela R.; Brem, Rachel B.; Catania, Kenneth C.; Bautista, Diana M.

doi:10.1371/journal.pone.0055001

Cited by 40 publications

(60 citation statements)

References 37 publications

(45 reference statements)

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“…To test this, we quantified the proportion of heat-sensing TRPV1 (27) and cold-sensing TRPM8 (28,29) neurons by RNA in situ hybridization. We found that 45.7 ± 1.7% (mean ± SEM) of duck DRG neurons expresses TRPV1 and that 10.2 ± 1.6% expresses TRPM8, which is typical for somatosensory neurons in nonspecialized ganglia of other vertebrates (1,23,(28)(29)(30) (Fig. 2 E and F and Fig.…”

Section: Tactile-foraging Waterfowl Expand the Proportion Of Large-dimentioning

confidence: 67%

“…The neuron size distribution is usually similar between TG and DRG (e.g., in the mouse, Fig. S1) (22,23) except in animals with somatosensory specialization in the head, whose TG exhibit a neuronal size distribution shifted toward large-diameter cells (1,21,24). Similarly, only duck TG is dominated by large-diameter cells, whereas DRG has the typical size distribution dominated by smalldiameter neurons (Fig.…”

Section: Tactile-foraging Waterfowl Expand the Proportion Of Large-dimentioning

confidence: 88%

“…In vertebrates, the majority of somatosensory neurons are nociceptors and thermoreceptors with small (<30 μm) and medium (30-40 μm) soma diameter, whereas the least numerous light-touch mechanoreceptors have large (>40 μm) soma size (18,19). This size distribution is an evolutionarily conserved feature present in TG of different Chordate classes, including Mammalia (1,(21)(22)(23), Reptilia (24), and Aves and, in the latter case, is exemplified by the chicken (Gallus gallus domestica)-a visually foraging bird (Fig. 1B) (25).…”

Section: Tactile-foraging Waterfowl Expand the Proportion Of Large-dimentioning

confidence: 99%

“…A nimals with acute sense of touch provide an opportunity to study cellular and molecular principles of mechanoreception from an unconventional perspective (1,2). Tactile-foraging waterfowl of the Anatidae family rely on their acute sense of touch rather than vision to find food.…”

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Neuronal mechanism for acute mechanosensitivity in tactile-foraging waterfowl

Schneider

Mastrotto

Laursen

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Relying almost exclusively on their acute sense of touch, tactileforaging birds can feed in murky water, but the cellular mechanism is unknown. Mechanical stimuli activate specialized cutaneous end organs in the bill, innervated by trigeminal afferents. We report that trigeminal ganglia (TG) of domestic and wild tactileforaging ducks exhibit numerical expansion of large-diameter mechanoreceptive neurons expressing the mechano-gated ion channel Piezo2. These features are not found in visually foraging birds. Moreover, in the duck, the expansion of mechanoreceptors occurs at the expense of thermosensors. Direct mechanical stimulation of duck TG neurons evokes high-amplitude depolarizing current with a low threshold of activation, high signal amplification gain, and slow kinetics of inactivation. Together, these factors contribute to efficient conversion of light mechanical stimuli into neuronal excitation. Our results reveal an evolutionary strategy to hone tactile perception in vertebrates at the level of primary afferents.A nimals with acute sense of touch provide an opportunity to study cellular and molecular principles of mechanoreception from an unconventional perspective (1, 2). Tactile-foraging waterfowl of the Anatidae family rely on their acute sense of touch rather than vision to find food. Using a complex array of highly coordinated feeding techniques-straining, pecking, and dabbling-they can selectively collect gastropods, worms, crustaceans, and plant matter even in murky water with high precision and efficiency. This highly discriminatory feeding behavior relies on the acquisition and rapid processing of sensory information coming from numerous mechanoreceptors in the bill (3).Mechanoreceptors are cell-neurite complexes that specialize in the detection of diverse mechanical stimuli. The most numerous mechanoreceptors in the bill skin of Anatidae birds are Herbst and Grandry corpuscles, which are present at high density (up to 150 receptors per square millimeter) 50-100 μm below the epidermis of dorsal and ventral surfaces of the upper and lower bill (4, 5). The mechanoreceptors are innervated by rapidly adapting primary afferents projecting from the trigeminal ganglia (TG) (Fig. 1A) and are best tuned to detect vibration and velocity (6-10). In this sense, Herbst and Grandry organs appear functionally homologous to the mammalian Pacinian and Meissner corpuscles, respectively. Following stimulus detection, mechanosensory information is processed in the trigeminal nucleus (PrV) of the brainstem. In tactile foragers, such as ducks, PrV accounts for a significantly larger fraction of total brain volume compared with visual foragers, such as chicken (11). This augmented neural representation reflects the need to process the complex and abundant tactile information from the primary afferents of the trigeminal nerve. However, even though the general layout of the mechanosensory system is well established, the contribution of primary afferents in stimulus detection is unclear.In rodents, over 80% of somatose...

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Section: Tactile-foraging Waterfowl Expand the Proportion Of Large-dimentioning

confidence: 67%

Section: Tactile-foraging Waterfowl Expand the Proportion Of Large-dimentioning

confidence: 88%

Section: Tactile-foraging Waterfowl Expand the Proportion Of Large-dimentioning

confidence: 99%

mentioning

confidence: 99%

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Neuronal mechanism for acute mechanosensitivity in tactile-foraging waterfowl

Schneider

Mastrotto

Laursen

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…Condylura leads a subterranean and semi-aquatic life and is functionally blind. Its prey is located by using an array of mobile, fleshy appendages ("the star") at the end of the snout [44], a mechanosensory adaptation of the trigeminal system (e.g., [44,45]). Given its unusual lifestyle, Condylura is predicted by the mosaic model to show two specific adaptations in its cerebellar architecture: first, a reduction in visual areas, and secondly, an expansion of those parts of the cerebellum receiving trigeminal inputs.…”

Section: Introductionmentioning

confidence: 99%

Compartmentation of the Cerebellar Cortex: Adaptation to Lifestyle in the Star-Nosed Mole Condylura cristata

et al. 2014

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The adult mammalian cerebellum is histologically uniform. However, concealed beneath the simple laminar architecture, it is organized rostrocaudally and mediolaterally into complex arrays of transverse zones and parasagittal stripes that is both highly reproducible between individuals and generally conserved across mammals and birds. Beyond this conservation, the general architecture appears to be adapted to the animal's way of life. To test this hypothesis, we have examined cerebellar compartmentation in the talpid star-nosed mole Condylura cristata. The star-nosed mole leads a subterranean life. It is largely blind and instead uses an array of fleshy appendages (the "star") to navigate and locate its prey. The hypothesis suggests that cerebellar architecture would be modified to reduce regions receiving visual input and expand those that receive trigeminal afferents from the star. Zebrin II and phospholipase Cß4 (PLCß4) immunocytochemistry was used to map the zone-and-stripe architecture of the cerebellum of the adult star-nosed mole. The general zone-and-stripe architecture characteristic of all mammals is present in the star-nosed mole. In the vermis, the four typical transverse zones are present, two with alternating zebrin II/PLCß4 stripes, two wholly zebrin II+/PLCß4-. However, the central and nodular zones (prominent visual receiving areas) are proportionally reduced in size and conversely, the trigeminal-receiving areas (the posterior zone of the vermis and crus I/II of the hemispheres) are uncharacteristically large. We therefore conclude that cerebellar architecture is generally conserved across the Mammalia but adapted to the specific lifestyle of the species.

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Organization of the spinal trigeminal nucleus in star‐nosed moles

Sawyer

Leitch

Catania

2014

J of Comparative Neurology

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Somatosensory inputs from the face project to multiple regions of the trigeminal nuclear complex in the brainstem. In mice and rats three subdivisions contain visible representations of the mystacial vibrissae: the principal sensory nucleus, the spinal trigeminal subnucleus interpolaris and subnucleus caudalis. These regions are considered important for touch with high spatial acuity, active touch, and pain and temperature sensation, respectively. Like mice and rats, the star-nosed mole (Condylura cristata) is a somatosensory specialist. Given the visible star pattern in preparations of the star-nosed mole cortex and the principal sensory nucleus, we hypothesized there were star patterns in the spinal trigeminal nucleus subnuclei interpolaris and caudalis. In sections processed for cytochrome oxidase we found star-like segmentation consisting of lightly stained septa separating darkly stained patches in subnucleus interpolaris (juvenile tissue) and subnucleus caudalis (juvenile and adult tissue). Subnucleus caudalis represented the face in a three-dimensional map with the most anterior part of the face represented more rostrally than posterior parts of the face. Multi-unit electrophysiological mapping was used to map the ipsilateral face. Ray-specific receptive fields in adults matched the CO-segmentation. The mean areas of multiunit receptive fields in subnucleus interpolaris and caudalis were larger than previously mapped receptive fields in the mole's principal sensory nucleus. The proportion of tissue devoted to each ray's representation differed between subnucleus interpolaris and the principal sensory nucleus. Our finding that different trigeminal brainstem maps can exaggerate different parts of the face could provide new insights for the roles of these different somatosensory stations.

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The Star-Nosed Mole Reveals Clues to the Molecular Basis of Mammalian Touch

Cited by 40 publications

References 37 publications

Neuronal mechanism for acute mechanosensitivity in tactile-foraging waterfowl

Neuronal mechanism for acute mechanosensitivity in tactile-foraging waterfowl

Compartmentation of the Cerebellar Cortex: Adaptation to Lifestyle in the Star-Nosed Mole Condylura cristata

Organization of the spinal trigeminal nucleus in star‐nosed moles

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