Cyto- and chemoarchitecture of the sensory trigeminal nuclei of the echidna, platypus and rat

Ashwell, Ken W.S.; Hardman, Craig D.; Paxinos, George

doi:10.1016/j.jchemneu.2005.08.007

Cited by 12 publications

(19 citation statements)

References 62 publications

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“…3B). The mole's principle nucleus is proportionally much larger than the corresponding nucleus in rodents (37).…”

Section: Star Representation In the Cnsmentioning

confidence: 90%

Evolution of brains and behavior for optimal foraging: A tale of two predators

Catania

2012

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

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Star-nosed moles and tentacled snakes have exceptional mechanosensory systems that illustrate a number of general features of nervous system organization and evolution. Star-nosed moles use the star for active touch-rapidly scanning the environment with the nasal rays. The star has the densest concentration of mechanoreceptors described for any mammal, with a central tactile fovea magnified in anatomically visible neocortical modules. The somatosensory system parallels visual system organization, illustrating general features of high-resolution sensory representations. Starnosed moles are the fastest mammalian foragers, able to identify and eat small prey in 120 ms. Optimal foraging theory suggests that the star evolved for profitably exploiting small invertebrates in a competitive wetland environment. The tentacled snake's facial appendages are superficially similar to the mole's nasal rays, but they have a very different function. These snakes are fully aquatic and use tentacles for passive detection of nearby fish. Trigeminal afferents respond to water movements and project tentacle information to the tectum in alignment with vision, illustrating a general theme for the integration of different sensory modalities. Tentacled snakes act as rare enemies, taking advantage of fish C-start escape responses by startling fish toward their strike-often aiming for the future location of escaping fish. By turning fish escapes to their advantage, snakes increase strike success and reduce handling time with head-first captures. The latter may, in turn, prevent snakes from becoming prey when feeding. Findings in these two unusual predators emphasize the importance of a multidisciplinary approach for understanding the evolution of brains and behavior.neocortex | neuroethology S tar-nosed moles and tentacled snakes each have novel sensory appendages protruding from their faces. These appendages give both animals a unique appearance unparalleled among their peers-no other mammal or snake has comparable appendages ( Fig. 1). However, there is more than the bizarre appearance of these animals to attract our attention. Extreme sensory specializations often reveal general principles of nervous system function and organization that are less obvious in other species (1-7). More generally, extremes in morphology provide informative case studies in evolutionary biology. Indeed, Darwin (8) devoted a special section of On the Origin of Species by Means of Natural Selection to "Organs of extreme perfection and complication." One can argue whether these unusual species seem in some way perfected, but surprisingly, the complexity of the mole's star has been cited as evidence of a divine creator (9).My goal is to review recent studies of these two species beginning with star-nosed moles, the species for which we have the most information from many years of study. The mole's nose is exceptional not only in appearance but also in the high density of mechanoreceptors that covers the nasal rays and the complexity of the modular neocortical net...

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“…3B). The mole's principle nucleus is proportionally much larger than the corresponding nucleus in rodents (37).…”

Section: Star Representation In the Cnsmentioning

confidence: 90%

Evolution of brains and behavior for optimal foraging: A tale of two predators

Catania

2012

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

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“…Molecular clock studies have argued for separation of monotreme and therian lineages at 217-161 million years ago, and divergence of ornithorhynchids and tachyglossids at 48-18 million years ago [Phillips et al, 2009], but morphological analysis of the fossil monotreme Teinolophos has led others to argue that the two monotreme clades were already distinct in the Cretaceous . The paucity of the monotreme fossil record, particularly with respect to the echidnas, makes it difficult to apply independent tests to claims made from mo- Organization of trigeminal sensory nuclei in the platypus and echidna as described previously [Ashwell et al, 2006]. Photomicrographs show the principal trigeminal sensory nucleus (Pr5) divided into dorsolateral (Pr5DL) and ventromedial (Pr5VM) components in a juvenile platypus ( a ) and adult echidna ( b ).…”

Section: Introductionmentioning

confidence: 99%

“…c Ventral projections of the right trigeminal sensory column, i.e. Pr5 and oral, interpolar and caudal components of the nucleus of the trigeminal spinal tract (Sp5O, Sp5I and Sp5C, respectively) in platypus, echidna and laboratory rat [Ashwell et al, 2006]. Rostral is to the top and medial is to the right for each diagram.…”

Section: Introductionmentioning

confidence: 99%

“…The platypus has an extremely large principal nucleus and large rostral parts of the spinal trigeminal group [achieved by lateral expansion and increased overlap between nuclei, fig. 1 ; Hines, 1929;Watson et al, 1977;Ashwell et al, 2006] and there are large numbers of granule cells in the principal nucleus. Unlike the platypus, the anatomical and chemoarchitectural features of the trigeminal sensory nuclei of the shortbeaked echidna are in many respects similar to those in rodents ( fig.…”

Section: Introductionmentioning

confidence: 99%

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Distinct Development of the Trigeminal Sensory Nuclei in Platypus and Echidna

Ashwell¹,

Hardman²

2012

Brain Behav Evol

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Both lineages of the modern monotremes have been reported to be capable of electroreception using the trigeminal pathways and it has been argued that electroreception arose in an aquatic platypus-like ancestor of both modern monotreme groups. On the other hand, the trigeminal sensory nuclear complex of the platypus is highly modified for processing tactile and electrosensory information from the bill, whereas the trigeminal sensory nuclear complex of the short-beaked echidna (Tachyglossus aculeatus) is not particularly specialized. If the common ancestor for both platypus and echidna were an electroreceptively and trigeminally specialized aquatic feeder, one would expect the early stages of development of the trigeminal sensory nuclei in both species to show evidence of structural specialization from the outset. To determine whether this is the case, we examined the development of the trigeminal sensory nuclei in the platypus and short-beaked echidna using the Hill and Hubrecht embryological collections. We found that the highly specialized features of the platypus trigeminal sensory nuclei (i.e. the large size of the principal nucleus and oral part of the spinal trigeminal nuclear complex, and the presence of a dorsolateral parvicellular segment in the principal nucleus) appear around the time of hatching in the platypus, but are never seen at any stage in the echidna. Our findings support the proposition that the modern echidna and platypus are derived from a common ancestor with only minimal trigeminal specialization and that the peculiar anatomy of the trigeminal sensory nuclei in the modern platypus emerged in the ornithorhynchids after divergence from the tachyglossids.

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“…For example, in rats, the vibrissal map in the principal trigeminal nucleus is relatively small, while the map in the subnucleus interpolaris is large. In contrast, in star-nosed moles, these 2 maps are similar in size [Ashwell et al, 2006;Catania et al, 2011;Sawyer et al, 2014]. More quantitative comparisons of somatotopic maps, combined with more detailed research into the facial tactile exploratory behavior of these animals, may help to generate novel hypotheses about the specialized sensory functions of these brainstem nuclei.…”

mentioning

confidence: 99%

Conserved Patterns of Trigeminal Somatosensory System Organization in Mammals

Sawyer

2017

Brain Behav Evol

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Cyto- and chemoarchitecture of the sensory trigeminal nuclei of the echidna, platypus and rat

Cited by 12 publications

References 62 publications

Evolution of brains and behavior for optimal foraging: A tale of two predators

Evolution of brains and behavior for optimal foraging: A tale of two predators

Distinct Development of the Trigeminal Sensory Nuclei in Platypus and Echidna

Conserved Patterns of Trigeminal Somatosensory System Organization in Mammals

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