Search PubMed⌕ Search

Biomedical subjects

Kenneth C Catania

Publications and source records attributed to Kenneth C Catania.

At least 19 recordsLinked to original sources

Growing out of a caste--reproduction and the making of the queen mole-rat.

Naked mole-rats have a eusocial colony structure consisting of non-reproductive workers and a reproductively active caste where a single, dominant queen and 1-3 males produce all of the offspring. Well-established queens have elongated bodies that characterize their caste. Worker females retain the ability to transform into queens, however the trigger and time course for this physical transformation remain a mystery. Here, we show a direct link between periods of pregnancy and vertebral lengthening in nascent queens. Adult female mole-rats were paired with a male and radiographed weekly for two and a half years to track the growth of the lumbar vertebrae as the mole-rats became sexually mature and experienced pregnancies. The lumbar vertebrae of breeding females grew at an increased rate during each pregnancy but growth rates returned to normal between pregnancies and during extended periods without reproduction. The rate of lumbar lengthening was reduced to normal rates in older, established queens experiencing pregnancies. Our results imply that the length of a new queen mole-rat is proportional to the number of pregnancies experienced and suggest that hormones related to pregnancy may play the critical role in bone growth associated with caste transformation.

Age Factors↗

Olfaction: underwater 'sniffing' by semi-aquatic mammals.

Terrestrial species that forage underwater face challenges because their body parts and senses are adapted for land--for example, it is widely held that mammals cannot use olfaction underwater because it is impossible for them to inspire air (sniff) to convey odorants to the olfactory epithelium. Here I describe a mechanism for underwater sniffing used by the semi-aquatic star-nosed mole (Condylura cristata) and water shrew (Sorex palustris). While underwater, both species exhale air bubbles onto objects or scent trails and then re-inspire the bubbles to carry the smell back through the nose. This newly described behaviour provides a mechanism for mammalian olfaction underwater.

Air↗

Telomerase activity coevolves with body mass not lifespan.

In multicellular organisms, telomerase is required to maintain telomere length in the germline but is dispensable in the soma. Mice, for example, express telomerase in somatic and germline tissues, while humans express telomerase almost exclusively in the germline. As a result, when telomeres of human somatic cells reach a critical length the cells enter irreversible growth arrest called replicative senescence. Replicative senescence is believed to be an anticancer mechanism that limits cell proliferation. The difference between mice and humans led to the hypothesis that repression of telomerase in somatic cells has evolved as a tumor-suppressor adaptation in large, long-lived organisms. We tested whether regulation of telomerase activity coevolves with lifespan and body mass using comparative analysis of 15 rodent species with highly diverse lifespans and body masses. Here we show that telomerase activity does not coevolve with lifespan but instead coevolves with body mass: larger rodents repress telomerase activity in somatic cells. These results suggest that large body mass presents a greater risk of cancer than long lifespan, and large animals evolve repression of telomerase activity to mitigate that risk.

Animals↗

Touching on somatosensory specializations in mammals.

Specialized species often reveal general principles of brain organization and provide systems for analysis of sensory function. Subterranean species dependent on touch have particularly large somatosensory areas with modular cortical representations of sensory surfaces. Some species have added cortical areas to processing networks, have developed tactile foveas and have superior colliculi primarily devoted to somatosensation rather than vision. Recent studies reveal surprisingly large cortical representations of oral structures in primates and mole-rats. Cortical modules represent a range of different sensory surfaces in rodents, star-nosed moles and primates, indicating that similar developmental mechanisms operate in diverse species. Finally, manipulation of patterning genes in mice suggests evolutionary mechanisms for producing the specialized corticies of subterranean species.

Afferent Pathways↗

Neuroanatomical evidence for segregation of nerve fibers conveying light touch and pain sensation in Eimer's organ of the mole.

Talpid moles are small insectivores that live in dark underground tunnels. They depend heavily on touch to navigate and find food. Most species have an array of complex epidermal sensory structures called Eimer's organs that cover the tip of the nose. In this study, the anatomy of Eimer's organ was examined in the coast mole and star-nosed mole by using the fluorescent styryl pyridinium dye AM1-43 and immunocytochemical staining for neurofilament 200 and substance P. In addition, DiI was used to label neural components of Eimer's organ. AM1-43 labeled all of the Eimer's organ receptors after systemic injection, suggesting a role in mechanotransduction. Immunostaining with neurofilament 200 and substance P labeled distinct subtypes of sensory fibers. Substance P labeled a group of free nerve endings along the outer edge of Eimer's organ, indicating a nociceptive role for these fibers. In contrast, neurofilament 200 labeled a more central set of nerve endings, suggesting that these fibers function as low-threshold mechanoreceptors. By labeling subsets of trigeminal afferents distant from the receptor array with DiI, we revealed innervation patterns indicating that one afferent supplies the outer, substance P-positive set of free nerve endings, whereas several afferents differentially innervate the central free nerve endings. Our results suggest that the free nerve endings innervating Eimer's organ are largely mechanosensitive and may play an important role in the rapid sensory discrimination observed in these species.

Afferent Pathways↗

Organization of somatosensory cortical areas in the naked mole-rat (Heterocephalus glaber).

Multiunit electrophysiology was combined with histological analysis of cortical sections to investigate the organization of somatosensory areas in the naked mole-rat. We provide new details for the organization of primary somatosensory cortex (S1) and identify cortical modules and barrels that correspond to the representations of different body parts. In addition, details of the location and organization of secondary somatosensory cortex (S2) are reported, and evidence for a third somatosensory representation, likely the parietal ventral area (PV), is provided and discussed. S1 contained a complete and systematic representation of the contralateral body surface and oral structures. The orientation of S1 was inverted, with the lower body represented medially and the face and oral structures located rostrolaterally. The S2 representation was found in caudolateral cortex forming a mirror image of S1. The two areas were joined at the representation of the vibrissae and snout, so that the orientation of S2 formed an upright representation of the body in cortex. Receptive fields for S2 were consistently larger than those in S1. Evidence for the presumptive parietal ventral area, lateral to S2, suggests that this area may be an inverted mirror image of S2. By aligning the electrophysiological maps of body representations with cytochrome oxidase-reacted cortical sections we were able to identify modules related to the buccal pad, chin, vibrissae, forelimb, hindlimb, trunk, tongue, lower incisor, and upper incisors. The orofacial modules in lateral cortex resemble similar modules reported to relate to oral structures previously described in the laboratory rat, owl monkey, and squirrel monkey.

Animals↗

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

Naked mole-rats are fossorial rodents native to eastern Africa that spend their lives in extensive subterranean burrows where visual cues are poor. Not surprisingly, they have a degenerated eye and optic nerve, suggesting they have poor visual abilities. However, little is known about their central visual system. To investigate the organization of their central visual system, we injected a neuronal tracer into the eyes of naked mole-rats and mice to compare the neural structures mediating vision. We found that the superior colliculus and lateral geniculate nucleus were severely atrophied in the naked mole-rat. The olivary pretectal nucleus was reduced but still retained its characteristic morphology, possibly indicating a role in light detection. In addition, the suprachiasmatic nucleus is well innervated and resembles the same structure in other rodents. The naked mole-rat appears to have selectively lost structures that mediate form vision while retaining structures needed for minimal entrainment of circadian rhythms. Similar results have been reported for other mole-rat species. Taken together, these data suggest that light detection may still play an important role in the lives of these "blind" animals: most likely for circadian entrainment or setting seasonal rhythms.

Adaptation, Ocular↗

Cortical, callosal, and thalamic connections from primary somatosensory cortex in the naked mole-rat (Heterocephalus glaber), with special emphasis on the connectivity of the incisor representation.

We investigated the distribution of cortical, callosal, and thalamic connections from the primary somatosensory area (S1) in naked mole-rats, concentrating on lower incisor and forelimb representations. A neuronal tracer (WGA-HRP) was injected into the center of each respective representation under guidance from microelectrode recordings of neuronal activity. The locations of cells and terminals were determined by aligning plots of labeled cells with flattened cortical sections reacted for cytochrome oxidase. The S1 lower incisor area was found to have locally confined intrahemispheric connections and longer connections to a small cluster of cells in the presumptive secondary somatosensory (S2) and parietal ventral (PV) incisor fields. The S1 incisor area also had sparse connections with anterior cortex, in presumptive primary motor cortex. Homotopic callosal projections were identified between the S1 lower incisor areas in each hemisphere. Thalamocortical connections related to the incisor were confined to ventromedial portions of the ventral posterior medial subnucleus (VPM) and posterior medial nucleus (Po). Injections into the S1 forelimb area revealed reciprocal intrahemispheric connections to S2 and PV, to two areas in frontal cortex, and to two areas posterior to S1 that appear homologous to posterior lateral area and posterior medial area in rats. The S1 forelimb representation also had callosal projections to the contralateral S1 limb area and to contralateral S2 and PV. Thalamic distribution of label from forelimb injections included ventral portions of the ventral posterior lateral subnucleus (VPL), dorsolateral Po, the ventral lateral nucleus, and the ventral medial nucleus and neighboring intralaminar nuclei.

Animals↗

Organization of the somatosensory cortex in elephant shrews (E. edwardii).

The superorder Afrotheria consists of a diverse group of mammals, including elephants, hyraxes, dugongs, sea cows, aardvarks, tenrecs, golden moles, and elephant shrews. Recent studies suggest this clade diverged from other placental mammals 100 million years ago and thus may represent the sister group to the remaining placental mammals. Despite this important taxonomic position, relatively few studies have investigated cortical organization in these species. Here we present results of an investigation of the somatosensory cortex in the Cape elephant shrew (Elephantulus edwardii). Using multiunit electrophysiological recording techniques, we identified a topographic map of the elephant shrew's body in a location and orientation consistent with the primary somatosensory cortex (S1). The elephant shrew's elongated snout, extensive facial vibrissae, and long tongue accounted for a large portion of the somatosensory representation, located in a relatively rostral area of cortex. Evidence for an additional somatosensory area, presumed to be secondary somatosensory cortex (S2), was found just lateral to S1. Visual and auditory responsive areas were also identified and the extent of visual cortex appeared to be quite large in these highly visual mammals. Despite the elephant shrew's exceptionally well-developed eyes, ears, and vibrissae, there were no anatomical correlates to sensory areas, or body part representations (e.g., barrels), that could be identified in the flatted cortex.

Animals↗

Plasticity of the cortical dentition representation after tooth extraction in naked mole-rats.

Naked mole-rats (Heterocephalus glaber) have a large cortical representation of their behaviorally important front teeth, accounting for 30% of primary somatosensory cortex (SI). Here we investigated the plasticity of this dental representation after the extraction of a single lower tooth. The representation of the contralateral lower incisor normally accounts for approximately 15% of somatosensory cortex in mole-rats. In five mole-rats the lower right incisor was extracted on either postnatal day 7 or 21. After 5-8 months the deprived tooth zone in S1 was investigated with multiunit microelectrode recordings. The results revealed a dramatic reorganization of the orofacial representation in SI. Neurons in the cortical lower tooth representation were responsive to tactile inputs from surrounding orofacial structures, including the contralateral upper incisor, ipsilateral lower incisor, tongue, chin, gums, and buccal pad. Neurons in the former lower tooth zone had complex receptive fields that often encompassed multiple sensory surfaces surrounding the extracted tooth in the periphery. These results suggest that the representation of the dentition in mammals is capable of significant reorganization after the loss of sensory inputs from the teeth. These data parallel findings in the somatosensory hand area of primates after deafferentation where cortex can become activated by a mixture of widely spaced surrounding sensory surfaces (e.g., chin and upper arm).

Afferent Pathways↗

Asymptotic prey profitability drives star-nosed moles to the foraging speed limit.

Foraging theory provides models for predicting predator diet choices assuming natural selection has favoured predators that maximize their rate of energy intake during foraging. Prey profitability (energy gained divided by prey handling time) is an essential variable for estimating the optimal diet. Time constraints of capturing and consuming prey generally result in handling times ranging from minutes to seconds, yet profitability increases dramatically as handling time approaches zero, providing the potential for strong directional selection for increasing predator speed at high encounter rates (tiny increments in speed increase profitability markedly, allowing expanded diets of smaller prey). We provide evidence that the unusual anatomical and behavioural specializations characterizing star-nosed moles resulted from progressively stronger selection for speed, allowing the progressive addition of small prey to their diet. Here we report handling times as short as 120 ms (mean 227 ms) for moles identifying and eating prey. 'Double takes' during prey identification suggest that star-nosed moles have reached the speed limit for processing tactile information. The exceptional speed of star-nosed moles, coupled with unusual specializations for finding and eating tiny prey, provide new support for optimal foraging theory.

Animals↗

Evolution of sensory specializations in insectivores.

Although insectivores have traditionally been thought of as primitive mammals with few specializations, recent studies have revealed great diversity in the sensory systems and brain organization of members of this mammalian order. The present article reviews some of these findings in three insectivore families that are thought to form a monophyletic group. These include hedgehogs (Erinaceidae), moles (Talpidae), and shrews (Soricidae). Members of each group live in unique ecological niches, have differently specialized senses, and exhibit different behaviors. Hedgehogs have well-developed visual, auditory, and somatosensory systems. Shrews make use of visual and auditory cues, but appear to depend most heavily on touch, particularly through prominent vibrissae. Moles are somatosensory specialists with small eyes and ears and unique epidermal mechanoreceptors called Eimer's organs used to identify prey and investigate their environment. In contrast to historical views of the insectivore order, members of this group have discrete and well-organized cortical sensory areas with sharp borders as determined from both electrophysiological mapping and analysis of cortical histology. Comparison of cortical organization across species reveals a number of specializations, including expansion of cortical representations of important sensory surfaces, the addition of cortical areas to some processing networks, and the subdivision of areas into separate cortical modules. In the case of the star-nosed mole, the somatosensory system has a tactile fovea and shares a number of features in common with the visual systems of sighted mammals.

Animals↗

Tactile foveation in the star-nosed mole.

Star-nosed moles have a specialized somatosensory system with 22 mechanosensory appendages surrounding the nostrils. A pair of appendages (the 11th pair on the ventral midline) acts as the tactile fovea and is used for detailed investigations. Here we used a high speed video camera to document movements of the star while moles searched for small prey items. Mole foraging behavior was very fast; the star, which is just over a centimeter in diameter, was touched to different areas of the environment approximately 13 times per second. This suggests that a mole foraging without interruption could potentially investigate 46,000 cm2 of surface area per hour. In 100% of 526 trials in which prey was identified and eaten, star-nosed moles made rapid, saccadic movements of the star to investigate the contacted prey with the foveal appendages. The movements of the star were similar to visual saccades in other species. Maximum velocity of the star during saccades was approximately 40 cm/s, and most saccades were between 30 and 60 ms in duration. As in the primate visual system, small corrective saccades were often needed to accurately foveate. We quantified the number of contacts different appendages made with prey items of various sizes during each encounter and compared this distribution to a previously proposed simulation of star movements during prey encounters. The behavior pattern and the simulation produced similar distributions of contact between the appendages and prey, and both distributions were closely correlated with the degree of cortical magnification of the appendage representations in primary somatosensory cortex (S1).

Animals↗

Organization of somatosensory cortex in the laboratory rat (Rattus norvegicus): Evidence for two lateral areas joined at the representation of the teeth.

Lateral somatosensory areas have not been explored in detail in rats, and theories on the organization of this region are based largely on anatomical tracing experiments. We investigated the topography of this region by using microelectrode recordings, which were related to flattened cortical sections processed for cytochrome oxidase (CO). Two lateral somatosensory areas were identified, each containing a complete representation of the body. A larger, more medial representation formed a mirror image of S1 along the rostrocaudal axis of the head region corresponding to the previously identified secondary somatosensory area (S2). A smaller, more lateral representation formed a mirror image of S2 along the rostrocaudal axis of the forelimb and hindlimb regions and likely corresponds to the parietal ventral area (PV) identified in other mammals. We also investigated the representation of the dentition and identified regions of cortex responsive to tooth stimulation. The lower incisor representation was rostral to the lower lip region of S1, and the upper incisor representation was lateral to the buccal pad region of S1. The upper and lower incisors flanked the tongue representation. An additional large region of far lateral cortex responded to both incisors. Finally, five CO-dense modules were consistently identified rostral and lateral to the S1 face representation, which we refer to as OM1, OM2, OM3, FM, and HM. These modules closely correspond to the physiologically identified areas representing the lower incisor (OM1) and tongue (OM2) regions of S1 and the mixed tooth (OM3), forelimb (FM1), and hindlimb (HM) representations of S2 and PV.

Animals↗

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 mole's 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 mole's SC.

Animals↗

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

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.

Animals↗

How do features of sensory representations develop?

Sensory representations in the brainstem and cortex have a number of features that support the idea that neural activity patterns are important in their development. Many of these features vary across species in ways that could result from perturbances in the balance of the effects of activity patterns and position-dependent gene expression. (1) Most notably, disruptions or septa in sensory maps often reflect actual discontinuities in the receptor sheet, and the discontinuities may be reflected in a series of interconnected maps. Species with different disruption patterns in sensory sheets have different matching disruption patterns in the sensory maps and variant individuals and strains of the same species have matching variations in the receptor disruption patterns and their sensory maps. (2) In addition, mutations that misdirect some of the retinal afferents from one side of the brain to the other create new sensory maps that preserve continuities in the altered pattern of input, while creating new structural discontinuities. (3) Furthermore, functionally different classes of afferents that are mixed in the receptor sheet often segregate to activate separate populations of target cells. (4) Finally, early developing portions of receptor sheets may gain more than their share of territory in sensory maps. These and other variable features of sensory maps are most readily accommodated by theories that involve roles for instruction by evoked and spontaneous neural activity patterns.

Animals↗