The sense of touch in the star-nosed mole: from mechanoreceptors to the brain

Star-nosed moles are somatosensory specialists that explore their environment with 22 appendages that ring their nostrils. The appendages are covered with sensory domes called Eimer's organs. Each organ is associated with a Merkel cell-neurite complex, a lamellated corpuscle, and a series of 5-10 free nerve endings that form a circle of terminal swellings. Anatomy and electrophysiological recordings suggest that Eimer's organs detect small shapes and textures. There are parallels between the organization of the mole's somatosensory system and visual systems of other mammals. The centre of the star is a tactile fovea used for detailed exploration of objects and prey items. The tactile fovea is over-represented in the neocortex, and this is evident in the modular, anatomically visible representation of the star. Multiple maps of the star are visible in flattened cortical preparations processed for cytochrome oxidase or NADPH-diaphorase. Star-nosed moles are the fastest known foragers among mammals, able to identify and consume a small prey item in 120 ms. Together these behavioural and nervous system specializations have made star-nosed moles an intriguing model system for examining general and specialized aspects of mammalian touch.     

Areal and callosal connections in the somatosensory cortex of the star-nosed mole

Star-nosed moles have a well-developed somatosensory cortex with multiple cortical areas representing the behaviorally important tactile star. In each of three cortical representations, the 11 mechanosensory appendages from the contralateral nose are represented in a series of dark cytochrome oxidase modules. Here the connections of this complex cortical network were explored with injections of the neuroanatomical tracer wheat germ agglutinin conjugated to horseradish peroxidase (WGA-H RP). The main goal was to determine the connection patterns of the somatosensory areas that represent the star. Injections of tracer made in or around the primary somatosensory representation (S1) of the star allowed us to determine the topography of local cortical connections and the projection and termination sites of corresponding interhemispheric connections. The results revealed precise topographic corticocortical connections reciprocally interconnecting the S1 star representation with its counterparts in S2 and in a third representation (S3) unique to star-nosed moles. Callosal connections from a widespread area of the contralateral hemisphere terminated primarily in the septa between cytochrome oxidase dark modules and in areas of cortex surrounding the star representations. However, midline structures of the star represented in S1 and S2 exhibited a high level of callosally labeled cells and terminals. This included label both within septa and within the centers of cytochrome oxidase dense modules representing midline appendages.     

Cortical organization in moles: evidence of new areas and a specialized S2

The somatosensory cortex of several mole species (family Talpidae), with different peripheral sensory adaptations, was investigated and compared to determine common and specialized features of cortical organization. Previously unidentified medial representations of the trunk and limbs were found in all species, indicating that S1 in moles occupies a medial to lateral strip of cortex as in most other mammals. This finding suggests a large lateral forelimb representation, previously attributed to S1, is actually part of S2. In the face representation, evidence was found for three representations of the unusual nose of the star-nosed mole ( Condylura cristata ). Each of these areas was divided into a series of modules (visible in cytochrome oxidase processed tissue) representing individual nasal appendages on the star. In the closely related but less specialized eastern mole ( Scalopus aquaticus ) and coast mole ( Scapanus orarius ), only two nose representations were identified in an area of cortex with a more uniform histological appearance. The results indicate that moles have enlarged somatosensory representations of the glabrous nose as compared to shrews and rats that instead have large vibrissal representations. In addition moles have a very large and specialized representation of the digging forepaw in S2. Since this part of S2 projects directly to the cervical spinal cord, the specialization may provide adaptive sensorimotor functions related to digging.     

Cortical-organization in moles: evidence of new areas and a specialized S2

The somatosensory cortex of several mole species (family Talpidae), with different peripheral sensory adaptations, was investigated and compared to determine common and specialized features of cortical organization. Previously unidentified medial representations of the trunk and limbs were found in all species, indicating that S1 in moles occupies a medial to lateral strip of cortex as in most other mammals. This finding suggests a large lateral forelimb representation, previously attributed to S1, is actually part of S2. In the face representation, evidence was found for three representations of the unusual nose of the star-nosed mole (Condylura cristata). Each of these areas was divided into a series of modules (visible in cytochrome oxidase processed tissue) representing individual nasal appendages on the star. In the closely related but less specialized eastern mole (Scalopus aquaticus) and coast mole (Scapanus orarius), only two nose representations were identified in an area of cortex with a more uniform histological appearance. The results indicate that moles have enlarged somatosensory representations of the glabrous nose as compared to shrews and rats that instead have large vibrissal representations. In addition moles have a very large and specialized representation of the digging forepaw in S2. Since this part of S2 projects directly to the cervical spinal cord, the specialization may provide adaptive sensorimotor functions related to digging.     

Sensory neuroscience: from skin to object in the somatosensory cortex

Humans can perceive the shape of objects by touch alone, by extracting geometric features such as edges. Recently recorded responses of single neurons in the secondary somatosensory cortex of monkeys suggest how the brain integrates tactile shape information across different regions of skin and builds up a representation of tactile objects.     

Organization of the primary somatosensory cortex and wing representation in the Big Brown Bat, <Emphasis Type="Italic">Eptesicus fuscus</Emphasis>

Bats are the only mammals capable of true powered flight. The bat wing exhibits specializations, allowing these animals to perform complicated flight maneuvers like landing upside-down, and hovering. The wing membrane contains various tactile receptors, including hair-associated Merkel receptors that might be involved in stabilizing bat flight. Here, we studied the neuronal representation of the wing membrane in the primary somatosensory cortex (S1) of the anesthetized Big Brown Bat, Eptesicus fuscus, using tactile stimulation with calibrated monofilaments (von Frey hairs) while recording from multi-neuron clusters. We also measured cortical response thresholds to tactile stimulation of the wings.The body surface is mapped topographically across the surface of S1, with the head, foot, and wing being overrepresented. The orientation of the wing representation is rotated compared to the hand representaion of terrestrial mammals, confirming results from other bat species. Although different wing membrane parts derive embryologically from different body parts, including the flank (plagiopatagium), the tactile sensitivity of the entire flight membrane (0.2–1.2 mN) is remarkably close or even higher (dactylopatagium) than the average tactile sensitivity of the human fingertip.     

The mole nose instructs the brain

Star-nosed moles normally have 11 mobile appendages, or rays, extending from each side of the nose. In cytochrome oxidase preparations, each ray is visible in primary somatosensory cortex as a dark band separated by light septa. When a single mole was found with 12 rays on each side of the nose, primary somatosensory cortex had 12 bands. We take this as further evidence that morphological features of somatosensory cortex are determined by the periphery.     

Behaviorally measured tactile sensitivity in the common bottlenose dolphin,Tursiops truncatus

Little research has been conducted on the somatosensory system of toothed whales and it remains uncertain how tactile sensitivity varies about their bodies. In this study, tactile sensitivity to high-frequency (250-Hz) displacement of the skin was quantified in three trained adult common bottlenose dolphins (Tursiops truncatus) using a vibratory device (tactor). The magnitude of skin displacement was controlled by varying the voltage to the tactor held against the skin surface with a constant force. Tactile thresholds were determined using an adaptive method of limits in which dolphins reported perception of the tactile stimulus by producing a whistle. Displacement thresholds ranged from 2.4 to 40 μm, with the greatest sensitivity found along the rostrum, melon, and blowhole. Sensitivity decreased caudally along the body, with the dorsal fin and tip of the fluke being the least sensitive locations tested. The results support hypotheses that the follicles on the dolphin rostrum are particularly important for perception. The reduction in tactile sensitivity at the appendages is consistent with their primary role in stabilization and locomotion compared to exploration or environmental sensing.     

Effects of Combining 2 Weeks of Passive Sensory Stimulation with Active Hand Motor Training in Healthy Adults

The gold standard to acquire motor skills is through intensive training and practicing. Recent studies have demonstrated that behavioral gains can also be acquired by mere exposure to repetitive sensory stimulation to drive the plasticity processes. Single application of repetitive electric stimulation (rES) of the fingers has been shown to improve tactile perception in young adults as well as sensorimotor performance in healthy elderly individuals. The combination of repetitive motor training with a preceding rES has not been reported yet. In addition, the impact of such a training on somatosensory tactile and spatial sensitivity as well as on somatosensory cortical activation remains elusive. Therefore, we tested 15 right-handed participants who underwent repetitive electric stimulation of all finger tips of the left hand for 20 minutes prior to one hour of motor training of the left hand over the period of two weeks. Overall, participants substantially improved the motor performance of the left trained hand by 34%, but also showed a relevant transfer to the untrained right hand by 24%. Baseline ipsilateral activation fMRI-magnitude in BA 1 to sensory index finger stimulation predicted training outcome for somatosensory guided movements: those who showed higher ipsilateral activation were those who did profit less from training. Improvement of spatial tactile discrimination was positively associated with gains in pinch grip velocity. Overall, a combination of priming rES and repetitive motor training is capable to induce motor and somatosensory performance increase and representation changes in BA1 in healthy young subjects.     

Shape Invariant Coding of Motion Direction in Somatosensory Cortex

Invariant representations of stimulus features are thought to play an important role in producing stable percepts of objects. In the present study, we assess the invariance of neural representations of tactile motion direction with respect to other stimulus properties. To this end, we record the responses evoked in individual neurons in somatosensory cortex of primates, including areas 3b, 1, and 2, by three types of motion stimuli, namely scanned bars and dot patterns, and random dot displays, presented to the fingertips of macaque monkeys. We identify a population of neurons in area 1 that is highly sensitive to the direction of stimulus motion and whose motion signals are invariant across stimulus types and conditions. The motion signals conveyed by individual neurons in area 1 can account for the ability of human observers to discriminate the direction of motion of these stimuli, as measured in paired psychophysical experiments. We conclude that area 1 contains a robust representation of motion and discuss similarities in the neural mechanisms of visual and tactile motion processing.     

Other developments regarding the concept of energy in biological systems

In order to recognize the realizability of inputs with different physical natures through a component, Yoneda's Lemma is applied. The major utility of this Lemma is when the components produce only energy. From this, it is assumed that a new material input must exist which was not recognized in the original developments in biological systems representation. Moreover, simple transfers of energy, between objects, components, and among both objects and components are developed under the generic name; energetical evolution. Thus, energetical evolution appears as anew element in the abstract representation of biological systems. These new concepts are incorporated into a new abstract diagram and a newM _β category. This paper was made possible by a Fellowship from the Consejo Nacional de Investigaciones Científicas y Técnicas of the República Argentina.     

Tactile sensing in specialized predators - from behavior to the brain

A number of predators depend heavily on tactile cues for pursuing and capturing prey. Here I describe and discuss the whiskers of carnivorous grasshopper mice and shrews, the sensory rays of the star-nosed mole, and the tactile appendages of the tentacled snake. These diverse sensors are accompanied by remarkable corresponding specializations in the central nervous system. But understanding their function and the significance of the central nervous system correlates requires the careful documentation of behavior inherent to a neuroethological approach.     

Are shy individuals less behaviorally variable? Insights from a captive population of mouse lemurs

Increasingly, individual variation in personality has become a focus of behavioral research in animal systems. Boldness and shyness, often quantified as the tendency to explore novel situations, are seen as personality traits important to the fitness landscape of individuals. Here we tested for individual differences within and across contexts in behavioral responses of captive mouse lemurs (Microcebus murinus) to novel objects, novel foods, and handling. We report consistent differences in behavioral responses for objects and handling. We also found that the responses to handling and novel objects were correlated and repeatable. Lastly, we show that shyer individuals may show less variability in their behavioral responses. This study provides new information on the potential for behavioral syndromes in this species and highlights differences in the degree to which behavioral types (e.g., shy/bold) vary in their behavioral responses.     

Sensory modulation and behavioral choice during feeding in the Australian frog, Cyclorana novaehollandiae

This study investigates how visual and tactile sensory information, as well as biomechanical effects due to differences in physical characteristics of the prey, influence feeding behavior in the frog Cyclorana novaehollandiae. Video motion analysis was used to quantify movement patterns produced when feeding on five prey types (termites, waxworms, crickets, mice and earthworms). Twelve kinematic variables differed significantly among prey types, and twelve variables were correlated with prey characteristics (including mass, length, height and velocity of movement). Results indicate that C.␣novaehollandiae uses a different strategy to capture each prey type. Visual assessment of prey characteristics appeared to be more important in modulating feeding behavior than tactile cues or biomechanical effects. We propose a hierarchical hypothesis of behavioral choice, in which decisions are based primarily on visual analysis of prey characteristics. In this model, the frogs first choose between jaw prehension and tongue prehension based on prey size. If they have chosen jaw prehension, they next choose between upward or downward head rotation based on length and height of the prey. If they have chosen tongue prehension, they next choose between behavior for fast and slow prey. Final decisions may be the result of behavioral fine tuning based on tactile feedback. Accepted: 5 August 1996     

Biologically plausible models of topographic map formation in the somatosensory and auditory cortices

Computational models of the somatosensory and auditory systems have been constructed with the neurosimulator GENESIS. The somatosensory model consists of a cortical layer with 1024 pyramidal cells and 512 basket cells connected to a hand surface with 512 tactile receptors. The auditory model consists of a cortical layer with 2256 pyramidal cells and 1128 basket cells connected to a cochlea with 47 receptors. The models reproduce processes related to the formation and maintenance of somatotopic and tonotopic maps and exhibit several features observed in experiments with animals such as variability in the shapes and sizes of areas of cortical representation and, in the case of somatotopy, cortical magnification values in agreement with experimental findings and linear decay of receptive field overlap as a function of cortical distance between recording sites in normal conditions.     

Detection of Optogenetic Stimulation in Somatosensory Cortex by Non-Human Primates - Towards Artificial Tactile Sensation

Neuroprosthesis research aims to enable communication between the brain and external assistive devices while restoring lost functionality such as occurs from stroke, spinal cord injury or neurodegenerative diseases. In future closed-loop sensorimotor prostheses, one approach is to use neuromodulation as direct stimulus to the brain to compensate for a lost sensory function and help the brain to integrate relevant information for commanding external devices via, e.g. movement intention. Current neuromodulation techniques rely mainly of electrical stimulation. Here we focus specifically on the question of eliciting a biomimetically relevant sense of touch by direct stimulus of the somatosensory cortex by introducing optogenetic techniques as an alternative to electrical stimulation. We demonstrate that light activated opsins can be introduced to target neurons in the somatosensory cortex of non-human primates and be optically activated to create a reliably detected sensation which the animal learns to interpret as a tactile sensation localized within the hand. The accomplishment highlighted here shows how optical stimulation of a relatively small group of mostly excitatory somatosensory neurons in the nonhuman primate brain is sufficient for eliciting a useful sensation from data acquired by simultaneous electrophysiology and from behavioral metrics. In this first report to date on optically neuromodulated behavior in the somatosensory cortex of nonhuman primates we do not yet dissect the details of the sensation the animals exerience or contrast it to those evoked by electrical stimulation, issues of considerable future interest.     

Things We Like: Human Preferences among Similar Organisms and Implications for Conservation

Human preferences will increasingly determine many species’ prospects for survival. However, aside from a small number of survey-based studies of preference among disparate taxa, human species preferences have received little attention. I determined human aesthetic preferences among a relatively homogenous group, the penguins, from representation in all recently published, comprehensive, popular books of photographs of penguins (n = 4 books; 304 photographs). Representation of visually distinguishable types of penguins, measured by total photograph area, was highly skewed and rankings were highly concordant across books, suggesting large and commonly held differences in aesthetic appeal. Multiple regression analysis indicated that amount of warm color was the only significant determinant of representation, and warm color was highly correlated (r ² = 0.96) with mean representation of the penguin types. Body size and neotenic form, traits found to influence human preferences among other animals, were not significant, suggesting that the bases of human species preferences differ by species type. The results of this study indicate that human aesthetic preferences discriminate finely among species and may be based on minor features. Conservationists must be vigilant to the potential for aesthetic responses to influence conservation efforts.     

Tactile motor learning in the antennal system of the honeybee (Apis mellifera L.)

Honeybees fixed in small tubes scan an object within the range of the antennae by touching it briefly and frequently. In our experiments the animals were able to scan an object for several minutes with the antennae. After moving the object out of the range of the antennae, the animals showed antennal movements for several minutes that were correlated with the position of the removed object. These changes of antennal movements are called “behavioural plasticity” and are interpreted as a form of motor learning. Bees showed behavioural plasticity only for objects with relatively large surfaces. Plasticity was more pronounced in bees whose compound eyes were occluded. Behavioural plasticity was related to the duration of object presentation. Repeated presentations of the object increased the degree of plasticity. After presentation durations of 30 min the animals showed a significant increase of antennal positions related to the surface of the object and avoidance of areas corresponding to the edges. Behavioural plasticity was compared with reward-dependent learning by conditioning bees to objects. The results of motor learning and reward-dependent conditioning suggest that bees have tactile spatial memory. Accepted: 13 May 1997     

Biological and bionic hands: natural neural coding and artificial perception

The first decade and a half of the twenty-first century brought about two major innovations in neuroprosthetics: the development of anthropomorphic robotic limbs that replicate much of the function of a native human arm and the refinement of algorithms that decode intended movements from brain activity. However, skilled manipulation of objects requires somatosensory feedback, for which vision is a poor substitute. For upper-limb neuroprostheses to be clinically viable, they must therefore provide for the restoration of touch and proprioception. In this review, I discuss efforts to elicit meaningful tactile sensations through stimulation of neurons in somatosensory cortex. I focus on biomimetic approaches to sensory restoration, which leverage our current understanding about how information about grasped objects is encoded in the brain of intact individuals. I argue that not only can sensory neuroscience inform the development of sensory neuroprostheses, but also that the converse is true: stimulating the brain offers an exceptional opportunity to causally interrogate neural circuits and test hypotheses about natural neural coding.     

Changing reference frames during the encoding of tactile events

The mindless act of swatting a mosquito on the hand poses a remarkable challenge for the brain. Given that the primary somatosensory cortex maps skin location independently of arm posture [1, 2], the brain must realign tactile coordinates in order to locate the origin of the stimuli in extrapersonal space. Previous studies have highlighted the behavioral relevance of such an external mapping of touch, which results from combining somatosensory input with proprioceptive and visual cues about body posture [3-7]. However, despite the widely held assumption about the existence of this remapping process from somatotopic to external space and various findings indirectly suggesting its consequences [8-11], a demonstration of its changing time course and nature was lacking. We examined the temporal course of this multisensory interaction and its implications for tactile awareness in humans using a crossmodal cueing paradigm [12, 13]. What we show is that before tactile events are referred to external locations [12-15], a fleeting, unconscious image of the tactile sensation abiding to a somatotopic frame of reference rules performance. We propose that this early somatotopic "glimpse" arises from the initial feed-forward sweep of neural activity to the primary somatosensory cortex, whereas the later externally-based, conscious experience reflects the activity of a somatosensory network involving recurrent connections from association areas.