Trigeminal ganglion and sensory nerves suggest tactile specialization of elephants

Purkart, Leopold; Tuff, John Michael; Shah, Malav; Kaufmann, Lena V.; Altringer, Carlotta; Maier, Eduard; Schneeweiß, Undine; Tunçkol, Elçin; Eigen, Lennart; Holtze, Susanne; Fritsch, Guido; Hildebrandt, Thomas; Brecht, Michael

doi:10.1016/j.cub.2021.12.051

Cited by 26 publications

(19 citation statements)

References 25 publications

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“…One possibility is the loss of limbs, which should lift the imposition on cerebellar processing that otherwise mediates the stabilization of the sensory surfaces of the limbs through fine motor control. This possibility is consistent with the other extreme in neuronal composition that is the cerebellum of the African elephant, which harbors 12 times the predicted number of neurons for a generic mammal, which we have speculated that might be associated to fine sensorimotor processing of the uniquely large appendage, the trunk (Herculano-Houzel et al, 2014b), mediated by a massively enlarged trigeminal ganglion (Pukart et al, 2022).…”

Section: Discussionsupporting

confidence: 81%

Mammals, birds and non-avian reptiles have signature proportions of numbers of neurons across their brain structures: Numbers of neurons increased differently with endothermy in birds and mammals

Herculano‐Houzel

2022

Preprint

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Modern mammals, birds, and non-avian reptiles have shared developmental and evolutionary origins in the ancestral amniotes of 300 million years ago. A previous analysis of a newly completed dataset on the cellular composition of the major parts of the brain of 242 amniote species, generated using the same cell counting method, the isotropic fractionator, argued for changes in the body-brain relationship in amniote evolution (Kverkova et al., 2022), but did not explore how the brains of amniotes diverged in their neuronal composition. Here I show, using the same dataset but focusing instead on the cellular composition of the brains regardless of body mass and phylogenetic relatedness, that the brains of extant mammalian, avian, and non-avian reptile species are characterized by signature proportions of numbers of neurons across the pallium, the cerebellum, and the rest of brain. An increase to a higher, fixed proportion of 4.5 neurons in the cerebellum to every neuron in the rest of brain, with variable numbers of pallial neurons, characterizes the avian brain compared to other reptiles, whereas mammalian brains are characterized by an average 4 neurons in the cerebellum to every neuron in the pallium regardless of numbers of neurons in the rest of brain, which also differs from the proportion in most non-avian reptilian brains of 1.4 neurons in the pallium and 0.5 neuron in the cerebellum to every neuron in the rest of brain. Thus, the independent evolution of endothermy in birds and mammals occurred with dramatic increases in numbers of neurons in all brain structures that differed markedly between birds and mammals. Additionally, there are marked continuities in the scaling of extant amniote brains that allow for the neuronal composition of the brain of ancestral amniotes to be estimated. Using these similarities in the neuronal scaling rules between living mammals and non-avian reptiles, I provide scaling relationships that allow predicting the composition of early mammaliaform and synapsid brains in amniote evolution, and I propose a simple model of amniote brain evolution that accounts for the diversity of modern mammalian, avian, and non-avian reptilian brains with only a few clade-shifting events in brain connectivity between cerebral cortex and cerebellum in mammals and between the cerebellum and rest of brain in birds, building on the increased availability of energy supply to the brain associated with the evolution of the increased oxidative and cardiovascular capacities that underlie endothermy.

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Section: Discussionsupporting

confidence: 81%

Mammals, birds and non-avian reptiles have signature proportions of numbers of neurons across their brain structures: Numbers of neurons increased differently with endothermy in birds and mammals

Herculano‐Houzel

2022

Preprint

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“…Similar foveation is observed in the star-nosed mole somatosensory system (25). The idea that African elephants have a trunk tip motor fovea aligns with their behavior (15), specializations of the trunk tip (26), and the tactile trunk innervation (27). We identified Asian versus African elephant neural specializations, neural adaptations to body size and motor foveae, and putative mechanisms of dexterity.…”

Section: Motor Foveae and Elephant Trunk Motor Strategiesmentioning

confidence: 59%

Section: Discussionmentioning

confidence: 99%

Elephant facial motor control

et al. 2022

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We studied facial motor control in elephants, animals with muscular dexterous trunks. Facial nucleus neurons (~54,000 in Asian elephants, ~63,000 in African elephants) outnumbered those of other land-living mammals. The large-eared African elephants had more medial facial subnucleus neurons than Asian elephants, reflecting a numerically more extensive ear-motor control. Elephant dorsal and lateral facial subnuclei were unusual in elongation, neuron numerosity, and a proximal-to-distal neuron size increase. We suggest that this subnucleus organization is related to trunk representation, with the huge distal neurons innervating the trunk tip with long axons. African elephants pinch objects with two trunk tip fingers, whereas Asian elephants grasp/wrap objects with larger parts of their trunk. Finger “motor foveae” and a positional bias of neurons toward the trunk tip representation in African elephant facial nuclei reflect their motor strategy. Thus, elephant brains reveal neural adaptations to facial morphology, body size, and dexterity.

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“…The diversity of the Vibrissae are present on the face and the entire postfacial body in both manatees and hyraxes. Elephants possess facial vibrissae, particularly on the dorsal extension or "finger" of the trunk tip (Rasmussen & Munger, 1996), and have tremendously impressive trigeminal nerves to facilitate sensory inputs from the trunk in particular (Maseko et al, 2013;Purkart et al, 2022). However, the hair on the postfacial bodies of elephants are not vibrissae, although they may serve as tactile hair in addition to facilitating heat dissipation and enhancing thermoregulation in hot climates (Myhrvold et al, 2012).…”

Section: Body Barrelettes: An Evolutionary Perspectivementioning

confidence: 99%

Parcellation in the dorsal column nuclei of Florida manatees (Trichechus manatus latirostris) and rock hyraxes (Procavia capensis) indicates the presence of body barrelettes

Sarko

Reep

2022

J of Comparative Neurology

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Florida manatees (Trichechus manatus latirostris) and rock hyraxes (Procavia capensis) exhibit expanded tactile arrays of vibrissae that are distributed not only on the face but also on the entire postfacial body. In contrast, the vibrissae of most mammals are principally restricted to the face. These facial vibrissae may be associated with central nervous system representations known as barrels in the cerebral cortex, barreloids in the thalamus, and barrelettes in the trigeminal nuclei of the brainstem. To date, vibrissae representations found within the brainstem have been principally limited to facial vibrissae representations in the trigeminal nuclei. We hypothesized that the tactile specializations of the manatee and rock hyrax would produce a unique modification of typical mammalian central nervous system organization, with postfacial vibrissae representations appearing in the cuneate and gracile nuclei as "body barrelettes."Using histological and histochemical methods, including cresyl violet, myelin, and cytochrome oxidase processing, we first delineated the rostral, middle, and caudal zones of the cuneate and gracile nuclei. Within the middle zone, divisions were present, including extensive parcellation in the cluster region, particularly in manatees. These clusters were particularly densely distributed and distinguishable in the presumptive postfacial body representations in the cuneate and gracile nuclei but otherwise shared many attributes with the barrelettes found in the trigeminal nuclei of other species.This study represents the first characterization of postfacial body vibrissae representations, or "body barrelettes," in the brainstem of any species. Previous studies have predominantly focused on facial vibrissae representations, which have served for decades as a model for sensory organization and plasticity. Our results extend what is known about vibrissae representations in the central nervous system to include expansions related to peripheral specializations of the postfacial body. Unusual somatosensory adaptations in the manatee and rock hyrax are highly informative regarding how mammalian brain organization responds to evolutionary pressures on sensory systems.

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Trigeminal ganglion and sensory nerves suggest tactile specialization of elephants

Cited by 26 publications

References 25 publications

Mammals, birds and non-avian reptiles have signature proportions of numbers of neurons across their brain structures: Numbers of neurons increased differently with endothermy in birds and mammals

Mammals, birds and non-avian reptiles have signature proportions of numbers of neurons across their brain structures: Numbers of neurons increased differently with endothermy in birds and mammals

Elephant facial motor control

Parcellation in the dorsal column nuclei of Florida manatees (Trichechus manatus latirostris) and rock hyraxes (Procavia capensis) indicates the presence of body barrelettes

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