The World of Touch

• Prof. Tony J. Prescott, Dept Psychology, Univ of Sheffield, UK

• Prof. Volker Dürr, Bielefeld University, Bielefeld, Germany

Despite its behavioural significance and omnipresence throughout the animal kingdom, the sense of touch is still one of the least studied and understood modalities. There are multiple forms of touch, and the mechanosensory basis underlying touch perception must be divided into several distinct sub-modalities (such as vibration or pressure), as will be made clear by the contributions elsewhere in this encyclopaedia. The commonality of all touch sensing systems is that touch experience is mediated by specialised receptors embedded in the integument—the outer protective layers of the animal such as the mammalian skin or the arthropod cuticle. Comparative research on touch, and its neuroethology, is only just beginning to provide a larger picture of the different forms of touch sensing within the animal kingdom. We begin our volume by reviewing works on several different invertebrate and vertebrate species, focusing on mechanosensation, each one with a specific requirement for tactile information. The aim of this introductory overview is to give selected examples of research on important model organisms from various classes of the animal kingdom, ranging from the skin of worms to the feelers of insects, and from the whiskers of a rat to the human hand. We conclude by discussing forms of human touch and the possibility of its future extension via synthetic systems.

Touch in invertebrates

The evolutionary origins of touch

Figure 1: The ciliate Paramecium is a unicellular organism that responds to touch on either end of its oval-shaped cell body by active movement away from the stimulus. The corresponding change in the beat of the cilia is triggered by ion currents that are activated through touch (Fotograph by Barfooz, CC BY-SA 3.0).

Mechanical perturbation of the outer membrane of a ciliate such as Paramecium, will cause it to respond by moving away from the stimulus source (Naitoh and Eckert, 1969). Thus, single-celled organisms already have a capacity for directional detection of tactile stimuli (Figure 1). The most primitive multicellular animals, the sponges, lack neurons, yet still show some capacity to respond to changes in water flow and pressure triggered by the deflection of non-motile cilia (Ludeman et al., 2014). Non-neural forms of sensitivity to tactile stimuli are also seen in many plants (Monshausen & Gilroy, 2009; Coutand, 2010). However, the evolution of neural conduction brings about a step-change in the capacity to respond rapidly and flexibly to tactile stimuli. Cnidarians, such as jellyfish and Hydra, despite having relatively simple nervous systems, can exhibit coordinated patterns of motor response to sensory stimuli and many have a rich capacity to respond to touch. For example, the nematocytes of Hydra are hair-like structures that respond to selective deflection and are thought to provide a good model for understanding the mechanoreceptors of more complex invertebrates (Thurm et al., 2004). In jellyfish such as Aglantha digitale, groups of hair cells, known as tactile combs, regulate complex behaviors including escape, feeding and locomotion (Arkett et al., 1988). The benefits of sensitivity to mechanical stimuli provided by hair-like structures may have encouraged their convergent evolution in multiple animal lineages. For instance, the hair cells of jellyfish appear to be sufficiently different from those in vertebrates that a common origin for both is unlikely (Arkett et al., 1988). Studies of the molecular basis of mechanosensation across different animal classes also suggest that cellular mechanisms to support tactile sensing may have evolved multiple times (Garcia-Anoveros & Corey, 1997).

Lower invertebrate model systems

Figure 2: The nematode Caenorhabditis elegans is an important model organism in neuroscience. It has 16 sensory and interneurons involved in touch-mediated behaviour (CC BY-SA 2.5).

All animals with a Central Nervous System (CNS) respond to touch. Even the tiny, un-segmented worm Caenorhabditis elegans, a nematode, shows touch-induced locomotion away from the stimulus (Figure 2). As in all higher animals, the corresponding mechanosensory cells are located in the integument, in this case beneath the cuticle. This worm's relevance to neuroscience stems from the fact that all of its 302 (somatic) neurons have been labelled and mapped. As a result, it has become the first animal system in which the entire network involved in touch-mediated behaviour - six sensory neurons, ten interneurons and 69 motoneurons - has been identified (Chalfie et al., 1985). Thirty years after the identification of all cellular components, many more details, including the biophysics of mechanosensory transduction (O'Hagan et al., 2005) and the molecular identity of several modulating signalling cascades (Chen and Chalfie, 2014), have been unravelled.

Figure 3: An important model organism for the electrophysiological study of touch-mediated movements is the medicinal leech (Hirudo medicinalis). The neurons of its ganglia have been mapped and many of them have been characterised individually (Photograph by Karl Ragnar Gjertsen, CC BY 2.5).

In larger, arguably more advanced, animals such as the leech (Hirudo medicinalis, Figure 3), touch-induced behaviour becomes more versatile and complex. However, increased complexity generally means less complete understanding. In terms of complete mapping and understanding of touch-induced behaviour, the leech comes second to the champion nematode. Owing to the larger size of its neurons, the neurobiology of touch has been investigated primarily by means of electrophysiological recordings, which are almost impossible in tiny Caenorhabditis. As a result, behaviourally relevant processing of touch-related information is perhaps best-studied in the leech (Muller et al., 1981). Because of its segmented body structure, the CNS of the leech has a chain of ganglia (one per segment), all of which contain the same or at least very similar sets of cellular elements. With regard to touch, three groups of mechanosensory neurons can be found in each ganglion, all of which respond to mechanical stimulation of the body, but with varying response thresholds: Touch cells (T-cells) are the most sensitive and respond to gentle touch of the body wall; Pressure cells (P cells) respond to stronger touch stimuli, and Nociceptive cells (N-cells) respond to very strong, potentially harmful, stimuli (Nicholls and Baylor, 1968). After the original description of what has meanwhile become a textbook example of range fractionation of stimulus intensity, a number of general aspects of sensorimotor systems have been studied in leech: Notable examples are the recruitment of T-, P- and N- cells in crawling (Carlton and McVean, 1995), the “mapping” of sensory input to distinct motor output by means of a population code (Lewis and Kristan, 1998a), the encoding and decoding of touch (Thomson and Kristan, 2006), and the modelling of the entire sensorimotor pathway underlying directed touch-induced directed movements (Lewis and Kristan, 1998b).

Tactile learning in molluscs

Among the molluscs, a sister group of the segmented invertebrates, several species have become important model organisms in neuroscience, particularly with regard to research on learning and memory (see e.g. Brembs, 2014). Most famous of these is probably the sea hare Aplysia californica, in which a number very fundamental cellular mechanisms underlying learning have been described for the first time. Although the "historical paradigm" of sensitisation and habituation of the siphon/gill withdrawal response can be induced by mechanical stimuli, the modality of touch has not been in the focus of these studies. Another fascinating mollusc model system is the Octopus, that has long been known for its cognitive abilities. A number of behavioural studies on tactile discrimination and tactile shape recognition have been conducted, largely following an animal psychology approach, in combination with ablation studies (e.g., Young, 1983). As a result, touch-related behaviour in Octopus has been analysed at a different level of description than in other invertebrate groups. A review of the touch-related behavioural repertoire in Octopus is given by Grasso and Wells (2013).

The Arthropod tactile hair

Compared to the soft-bodied animals mentioned above, animals with a skeleton no longer work as hydrostats in which body deformation is best monitored by deformation of the surface, i.e., the integument. In contrast to a hydrostat, skeletons require the formation of joints, thus "focussing" any change in posture on a limited set of locations. As a consequence, skeletons impose a physical limit to the number of degrees of freedom of movement. With regard to touch, this is important because mechanoreceptors may be dedicated to "strategically relevant locations" across the body, i.e., locations where displacement is most likely to occur. In proprioception, such strategically relevant locations are the joints themselves (and/or the muscles and tendons actuating them). In touch, strategically relevant locations are surface areas where contact with external objects is most likely to occur. Arthropods (that is the group comprising spiders, Crustaceans, insects and their relatives) appear to exploit such strategically relevant locations in two ways: In proprioception, they often use patches of hairs, so-called hair fields or hair plates, to sense displacement of two adjoining body segments. In touch, they use very much the same kind of hairs, too, but at various locations on the body, with particularly high "hair density" at places where contacts are most likely to occur and/or most relevant to detect.

These arthropod hairs are not like mammalian hairs at all: The Arthropod tactile hair is a cone-shaped cuticular structure, filled with fluid and equipped with a number of cells as the base. At least one of these cells is a ciliated mechanoreceptor that encodes the deflection of the cuticular structure (Thurm, 1964). Arthropods have a large variety of such sensory hairs (called seta or, more generally, sensillum; plural: setae and sensilla). Their information encoding properties have been described in different ways (e.g., see French, 2009). Apart from various mechanoreceptors (the basic type being the Sensillum trichoideum), there are also variants with chemoreceptors, subserving gustation and olfaction.

Both spiders and insects use hair sensilla also in proprioception and, as a consequence, in active touch sensing, where the active movement of a limb needs to be monitored. To date, a number of such proprioceptive hair fields have been characterised functionally (e.g., French and Wong, 1976). As part of this encyclopedia, tactile hairs are the key sensory elements in three chapters, one dealing with the functional properties and behavioural relevance of tactile hairs in spiders (Barth, 2015), and two more dealing with tactile hairs on dedicated sensory organs in insects—the antennae (Okada, 2009; Dürr, 2014).

The Arthropod antenna: elaborate touch in invertebrates

Among the living Arthropods, only the Myriapods (millipedes, etc.), Crustaceans and insects carry antennae (singular: antenna). Antennae are commonly called feelers, which is appropriate given the fact that they are dedicated sensory limbs (Staudacher et al., 2005). As such, they are equipped with a particularly large number of sensilla, and the density of sensilla per unit surface area is much higher than on most other parts of the body. With regard to touch this means that the antennae are the major sensory organ of touch, although all other body parts that carry tactile hairs may contribute tactile information as well.

During evolution of the Arthropoda, several body segments have fused to form the head. For example, in insects, the common view is that the head has developed from six body segments, three of which carry the mouthparts, and another three that carry the main sensory organs of the head: the eyes and the antennae (or feelers). In Crustaceans, there are two pairs of antennae: the smaller, anterior pair - the Antennules (or 1st antennae) - are known to have important functions in chemoreception (as in an underwater sense of smell). The larger, posterior pair (the 2nd antennae) is known to serve the sense of touch. Tactually mediated behaviour in Crustaceans has mostly been studied in lobsters, crayfish and other large, decapod Crustaceans (Staudacher et al., 2005). Given the fact that the Decapoda represent only a small fraction of the morphological, behavioural, and ecological diversity of Crustaceans, it is very likely that antennal touch works differently in different taxa. An example for a reasonably well-studied Crustacean with regard to touch is the Australian crayfish Cherax destructor in which both biomechanical and behavioural aspects have been studied (Sandeman, 1985, 1989). Cherax actively explores the environment ahead with its 2nd antennae and shows directed attacks towards objects that it has localised tactually (e.g., Zeil et al., 1985).

Insects carry only one pair of antennae. The common view is that during evolution, insects must have lost the second pair of antennae, such that the insect antenna is homologous to the Crustacean antennule, i.e., both organs have a common evolutionary origin. Like the Crustacean antennule, the insect antenna is the most important sensory organ for olfaction. Other than the Crustacean antennule, the insect antenna is also the most important sensory organ for touch.

Figure 4: An Indian stick insect (Carausius morosus) climbs a rung that it has detected by tactile contact with its antennae. Location of the rung is highlighted in the leftmost frame. From left to right, frames show instants of (i) missing the rung with the antennae, (ii) touching the rung with the left antenna during upstroke, (iii) touching the rung again during the subsequent downstroke, (iv) first foot contact with the rung and (v) climbing the rung. Numbers indicate the time in [s] relative to the first antennal contact with the rung.

Tactually mediated behaviour in insects has been studied in great detail in a number of species, most notably in cockroaches, crickets, stick insects and bees (Staudacher et al., 2005). Antennal touch has been shown to be important for near-range sensing during locomotion, for example in tactually mediated course control (Camhi and Johnson, 1999). In many cases, the relevant mechanoreceptors have been identified, for example the antennal hair fields in touch-mediated turning towards an object (Okada and Toh, 2000). In the past, sensors involved in course control have mostly been viewed as passive systems that do not require active movement for acquiring information. In some behavioural paradigms, such as tactile wall following, antennae are thought to be used passively. However, active movement of antennae is a key feature of active tactile exploration during locomotion. Antennal contact events may trigger decisions between mutually exclusive behavioural actions (e.g., Harley et al., 2009) or goal-directed motor actions such as tactually elicited reaching movements of the front legs (Schütz and Dürr, 2011).

As a higher-order aspect to active tactile exploration, antennal movements are also involved in attentive behaviour such as visually guided pointing in crickets (e.g., Honegger, 1981) and touch-related motor learning in the honeybee (Erber et al., 1997). In addition to non-associative motor learning, honeybees have also been demonstrated to show different associative learning behaviours (with regard to touch). For example, it is possible to condition them to different surface patterns (e.g., Erber et al. 1998) but also to condition antennal sampling movements as such in an operant conditioning paradigm (Erber et al., 2000).

The antennal mechanosensory system of insects has also been studied electrophysiologically, in particular with respect to the information transfer from the head to the ganglia of the ventral nerve cord. Owing to the fact that insect neurons can be identified and labelled individually, there is hope that some aspects of tactually mediated behaviour will be understood at the level of neuronal networks as research progresses. Today, the collection of identified antennal mechanosensitive neurons comprises descending interneurons in the brain (e.g., Gebhardt and Honegger, 2001) and in the suboesophageal (or gnathal) ganglion (e.g., Ache et al., 2015).

As part of the present collection of articles, two insect model organisms are presented in more detail: the cockroach (Okada, 2009) and the stick insect (Dürr, 2014).

Touch in vertebrates

The lateral line system of fish and amphibians

Figure 5: The fish lateral line system provides a sensitive organ for detecting hydrodynamic stimuli. In the Rainbow Trout (Oncorhynchus mykiss), pictured here, the position of the lateral line is marked by the distinctive pink coloring. Photograph by Liquid Art (CC 4.0).

In fish and amphibians, vertebrate mechanoreceptor organs, known as neuromasts, are arranged in lines on the body, head and tail, either free-standing on the skin or inside fluid-filled canals. In many fish species, a line of neuromasts within a canal that lies on the center line of each flank forms what is known as the lateral line system (Bleckmann and Zelick 2009). The number of neuromasts can vary between species from a few dozen to several thousand. The main sensory structure in each neuromast is a bundle of hair cells that respond to hydrodynamic stimuli resulting from water displacement or changes in water pressure. The lateral line system therefore provides a refined sensory system for detecting remote causes of water movement such as the behavior of predator or prey animals, water currents, and topographical features of the underwater environment. The lateral line, in effect, provides a form of remote or distal touch. A remnant of the lateral line system in mammals (including humans) are the liquid-filled (semicircular) canals of the inner ear, a structure informing us about rotational movements of the head.

Evolutionary origins of mammalian hair and skin

Figure 6: The naked mole rat (Heterocephalus glaber) has lost all of its pelagic hair but retains tactile hair across its body surface. Photograph by Trisha Shears.

Skin serves many functions, including to house and protect the organs and internal body parts, and to act as the body’s largest sensory organ sensitive to tactile, thermal, and chemical stimuli (Chuong, Nickoloff et al. 2002). Mammalian skin has evolved from the integument of earlier vertebrates via a complex path that is still only partially charted (Maderson 1972, Maderson 2003). What is clear, however, is that hair evolved anew in early mammals, or in their therapsid reptilian ancestors, as a specialization of the outer epidermal layers of the integument (Sarko, Rice et al. 2011). Whereas dense or pelagic hair serves an obvious thermoregulatory function, the evolution of mammalian hair cannot be explained by the need to improve maintenance of body temperature. Rather, the first hairs almost certainly had a largely tactile function, and their subsequent proliferation allowed hair to gain a secondary role as an insulator. The primary sensory role of hair is retained in the tactile hair, or vibrissae, found on all therian mammals (marsupials and placentals) except humans (Prescott, Mitchinson et al. 2011). In the naked mole rat, an animal that has lost all of its pelage, tactile hair has been retained across the whole body surface for its value in supporting the sense of touch (Crish, Crish et al. 2015).

Many mammals have also evolved areas of non-hairy, glabrous skin. In humans, these include the skin areas on the lips, hands and fingertips and the soles of the feet. These are the parts of the body that are most important when physically interacting with the world and where accurate tactile discrimination is most critical; unsurprisingly, then, glabrous skin has a high density of mechanosensory receptors including Meissner corpuscles, Pacinian corpuscles, Merkel-cell neurite complexes and Ruffini endings (Moayedi, Nakatani et al. 2015). The same mechanoreceptor types are also found in hairy skin alongside hair follicles and a system of unmyelinated low threshold C-tactile (CT) mechanoreceptors (Loken, Wessberg et al. 2009). The CT fibers are particularly sensitive to light 'stroking' touch and thus are thought to underlie an affective, or social, touch capacity that may be unique to mammals (McGlone, Wessberg et al. 2014).

Figure 7: The CT fiber system in mammalian hairy skin appears to be part of an affective system that encourages social touch and promotes bonding in mammals. Photograph by Jim Champion (CC 3.0).

Glabrous skin forms the basis for specialized sensory organs in a variety of animals including the electroreceptive bill of the platypus and the unusual tactile snout of the star-nosed mole (see below). A notable feature of mammalian tactile sensing systems is the presence of somatotopic maps of the skin surface in primary somatosensory cortex (S1) (Kaas 1997) (Wilson and Moore 2015). These maps are organized to match the topographic layout of the periphery but in a distorted manner, such that skin areas that have a higher density of receptors, greater receptor innervation, or that are functionally more important to the animal, have a proportionately larger representation in cortex. The human sensory "homunculus" described by Penfield and Boldrey (1937) is probably the best known of these maps, and the "barrel" field of rat and mice somatosensory cortex, first described by Woolsey and van der Loos (1970), the best studied. However, maps whose size, shape and organisation reflect the sensory specialization of the species have also now been described for a wide range of mammals (Krubitzer, Manger et al. 1995, Catania and Henry 2006).

Mechanosensation in monotremes

Figure 8: Monotremes, such as the duck-billed platypus, combine mechanosensing through their unique "pushrod" system, with electroreception, to search for prey underwater or beneath the ground. Photograph from Brisbane City Council (CC 2.0).

Sensing in the monotremes, or egg-laying mammals, is perhaps most remarkable for the sensitive electroreceptive capability of the platypus (Scheich, Langner et al. 1986). However, all three monotreme species (the platypus and both species of spiny anteater—echidna) also possess a distinctive tactile sensing system, quite different from the vibrissae of the therian mammals. Specifically, all monotremes have mechanoreceptive structures on the snout or bill known as “pushrods” (Proske, Gregory et al. 1998). These are compact, rigid columns of cells embedded in the skin that are able to move relative to the surrounding tissue. Most of the rod structure is below the skin surface with a convex tip raised slightly above it. The tissues of the pushrods are associated with four types of nerve ending including Merkel cells, and the structure has been compared to the Eimer organs of moles (see below). In platypus, up to 50,000 pushrods are scattered across surface and along the edges of the bill. The bill also contains an extensive venous system that can be engorged with blood, possibly boosting the acuity of the pushrod system. In platypus the electroreceptive system provides a strongly directional sense for detecting and orienting to prey animals; the pushrods might then assist targeting of prey in the final attack phase. In echidna the pushrod system might similarly be important when the animal probes the ground with its snout looking for insect prey.

Mammalian vibrissal systems

Long facial whiskers, or macrovibrissae, are found in many mammalian species, projecting outwards and forwards from the snout of the animal to form a tactile sensory array that surrounds the head (Pocock 1914, Brecht, Preilowski et al. 1997, Mitchinson, Grant et al. 2011). Pocock (1914) examined example specimens from all of the principal mammalian orders, concluding that facial vibrissae were present in at least some species in all orders except the monotremes, and that species that lacked whiskers, or in which the whiskers were less evident, were usually the more derived members of their order. He concluded that the possession of facial whiskers was a primitive mammalian trait. Each vibrissa, also known as a sinus hair, is composed of a flexible hair shaft that emerges from an intricate mechanosensory structure known as a follicle-sinus complex (FSC), containing six distinct populations of receptors, and that differs in structure, and is more richly innervated, than the simpler follicle of a pelagic hair (Rice, Mance et al. 1986). Many terrestrial mammals, particularly ones that are nocturnal, inhabit poorly-lit spaces, or that are tree-climbing (scansorial), have evolved highly specialized vibrissal sensing systems. Research has focused on several such animals— rodents such the common rat, the common mouse, and the golden hamster, insectivores such as the Etruscan shrew (Roth-Alpermann and Brecht 2009) and the marsupial short-tailed Brazilian opossum (Grant, Haidarliu et al. 2013).

Figure 9: Many terrestrial mammals have prominent vibrissae the evolution of which predates pelagic hair. Many species also actively control their whiskers using their facial musculature. TopLeft: The short-tailed Brazilian Opossum (Monodelphis domestica). BottomLeft: South American river rat (Myocastor coypus). TopCentre: Brazilian Porcupine (Coendou prehensilis). BottomCentre: European water vole (Arvicola amphibius). TopRight: African hedgehog tenrec (Echinops telfairi). BottomRight: Eurasian water shrew (Neomys fodiens). Photographs by Tony Prescott (top row) and Sarah Prescott (bottom row) used with permission.

The configuration of the facial whiskers varies substantially amongst rodents (Sokolov and Kulikov 1987) though the rat serves as a suitable example. In rats, the macrovibrissae form a two-dimensional grid of five rows on each side of the snout, each row containing between five and nine whiskers ranging between ~15 and ~50 mm in length (Brecht, Preilowski et al. 1997). During exploration and many other behaviors, these whiskers are swept back and forth at rates of up to 25 Hz, and in bouts that can last many seconds, in a behavior known as "whisking". The kinematics of each whisker is partly determined by its own intrinsic muscle (Berg and Kleinfeld (2003); see also (Knutsen 2015; Haidarliu 2015)). These movements of the whiskers are also closely coordinated with those of the head and body, allowing the animal to locate interesting stimuli through whisker contact, then investigate them further using both the macrovibrissae and an array of shorter, non-actuated microvibrissae on the chin and lips.

Much of the neurobiological research on the rodent vibrissal system has focused on its accessibility, given the ease of use of rats and mice as laboratory animals, as a model of mammalian neural processing in general, and of cortical processing in particular, rather than as a target for understanding tactile sensing per se. Nevertheless, this research has revealed a great deal about neural processing for somatosensation, demonstrating, in particular, that it involves multiple closed sensorimotor loops at different levels of the neuraxis (Ahissar and Kleinfeld (2003), see also Ahissar, Shinde et al. (2015)). Interest in the rodent vibrissal system as an active sensing system in its own right began with Vincent’s 1912 monograph on “The function of the vibrissae in the behavior of the white rat” and has seen significant growth in recent decades spurred by the availability of high-speed digital video recorders for accurate detection of vibrissal movement (for reviews see Hartmann (2001), Kleinfeld, Ahissar et al. (2006), Mitchinson, Grant et al. (2011)).

The refined vibrissal sense of aquatic mammals

Figure 10: Aquatic mammals such as the Harbor seals have highly developed vibrissal sensing that they employ to detect hydrodynamic flows left by fish. Photograph by Barbara Walsh (CC 2.0).

Some of the most successful and intelligent aquatic animals are the pinnipeds—seals and walruses—sea mammals that evolved when bear-like ancestors returned to the oceans more than twenty million years ago (Berta, Sumich et al. 2006). A striking feature of these animals is that they have well-developed and sensitive vibrissal (whisker) sensory systems (Hanke and Dehnhardt 2015). In some species of seal, the vibrissae have adapted to be able to detect the disturbances left in the water by swimming fish. By measuring these hydrodynamic flow fields these animals are able to track and capture fast-moving prey in total darkness (Dehnhardt, Mauck et al. 2001). Pinnipeds that find food at the bottom of the ocean, such as the bearded seal and the walrus, have evolved a very different form of vibrissal adaptation optimized for efficient foraging for clams and other invertebrates in the muddy substrates of the seafloor (Ray, McCormick-Ray et al. 2006). The numerous, densely-packed, and moveable vibrissae of these animals form a sensitive tactile “rake” that allow them to recognize and consume prey animals at remarkably fast rates (up to 9 clams per minute has been estimated for the walrus).

In addition to the ocean-going pinnipeds, facial vibrissae are well-developed in many other aquatic mammalian species including manatees, otters, water shrews, water voles, and water rats. In manatees, vibrissae are found distributed across the entire body apparently as a compensation for the reduced availability of visual information in the natural habitat of these animals. The manatee’s ability to navigate effectively in turgid water indicates a whole body capacity to detect hydrodynamic signals using vibrissal sensing that has interesting similarities to the fish lateral line (Sarko, Reep et al. 2007, Gaspard, Bauer et al. 2013; Reep and Sarko 2009).

In small aquatic mammals whisker touch appears to be important in predation. For instance, the sensitivity and fast responsiveness of the vibrissae for underwater hunting has been demonstrated for the American water shrew using high-speed video data (Catania, Hare et al. 2008). These animals show no significant capacity for following hydrodynamic trials, but display a very rapid and precise attack response when they make direct contact with a prey animal or when there is nearby movement of the water generated by a possible prey. Attacks are initiated within 25ms of first contact and usually completed with 1 second. The Etruscan shrew, the world's smallest terrestrial animal, has shown as similar facility for short-latency, high-precision attacks on insect prey in air, guided purely by vibrissal touch (Anjum, Turni et al. 2006; Roth-Alpermann and Brecht, 2009).

The specialization of mammals to aquatic environments has been accompanied by adaption to the sensory innervation of the vibrissae. In a comparison of an aquatic (ringed seal), semi-aquatic (European otter) and terrestrial (pole cat) mammal species, the latter two being of the same mammalian family (Mustelidae), a marked increase was found in innervation by the deep vibrissal nerve in the semi-aquatic (4x terrestrial) and aquatic (10x terrestrial) animals (Hyvarinen, Palviainen et al. 2009). The form and structure of the whiskers also varies quite markedly between species. For instance, in terrestrial mammals, a typical vibrissal hair shaft is tapered and has a round cross-section, while those of eared seals and walruses are typically non-tapered and oval. These differences in hair structure are associated with a different response to tactile stimulation (Hanke, Witte et al. 2010), in particular their vibratory properties. These adaptations point to the increased importance of vibrissal touch sensing in the ecology of many aquatic mammals.

Active sensing strategies and the unusual case of the star-nosed mole

Figure 11: The nose of the star-nosed mole (Condylura cristata) has evolved twenty-two fleshy appendages that together constitute a unique active touch sensing system for rapid detection of invertebrate prey. Photograph from the US National Park Service.

Millions of years of tunneling in damp soil has given rise to the intriguing active-touch organ that is the “star” of the star-nosed mole (Catania and Kaas 1995, Catania 1999, Catania and Remple 2005, Catania 2011). In this animal, the glabrous skin of the snout has expanded and diversified into twenty-two movable fleshy fingers, called rays, controlled by tendons connected to the facial musculature. Each ray is covered with thousands of Eimer organs (over 25 000 across the whole star), distributed in a honeycomb pattern. The Eimer organ is a narrow column of skin tissue and nerve endings capped with a 30 μm dome, that sits atop one slowly adapting (Merkel) and one rapidly adapting (lamellated corpuscle) mechanoreceptor. Eimer organs are found in the snouts of all species of mole so far investigated and are known to be very sensitive to light touch.

The unusual structure of the star is thought to be a consequence of the mole’s subterranean lifestyle (Catania and Remple 2005). Although many mole species tunnel in the ground and prey on small invertebrates, the star-nosed mole stands out for the speed at which it can detect and consume small prey animals—handling time, from detection to consumption, can be as little as 120ms. The evolution of the star may thus have allowed the mole to specialize towards smaller and smaller prey sizes. To achieve this feat of speed foraging, touch is actively controlled. Specifically, as the animal searches for food, the rays of the star lightly palpate the surface of the substrate many times per second. If a potential prey item is detected the star is oriented to allow more extensive exploration with ray 11, a shorter ray at the center and bottom of the star. Ray 11 has been proposed to be a tactile fovea, with the orienting movements of the star likened to visual saccades (Catania 1999). Interestingly, ray 11 does not have higher Eimer organ density than other rays but it does have significantly higher innervation density (70% higher than other rays), and a massively enlarged representation in somatosensory cortex (25% of the S1 cortical area associated with the entire star). Enlarged cortical representation cannot be explained by increased innervation alone so likely reflects the central role of ray 11 in the mole’s predatory behavior. That is, it may have expanded to provide the mole with enhanced discrimination of tactile features relevant to prey identification and capture, whereas other rays are principally concerned with detection of possible prey.

In terms of its active sensing behavior, there appears to be an interesting convergence between control of its rays by the star-nosed mole, and of the vibrissae in terrestrial whisker specialists such as rats, mice, and hamsters. Each animal makes rapid palpations of a broad area around the snout with long protuberances, before homing in for a fine-grained investigation of regions of special interest with a tactile fovea, composed of the densely congregated microvibrissae, in the case of the rat, and ray 11 in the case of the mole. Note that although neurobiological investigations of S1 cortex in rats and mice have mainly focused on the prominent macrovibrissal "barrels", the microvibrissae on the lips and chin also map to individual barrel-like cell aggregates. Indeed, overall the area of S1 dedicated to representing the microvibrissae is larger than that for the longer macrovibrissae (see, e.g. Woolsey, Welker et al. (1975) and Figure 2 in Wilson and Moore (2015)), this is consistent with the notion of the microvibrissal array as a foveal region for the whisker sense (Brecht, Preilowski et al. 1997).

Varieties of human touch sensing

In the womb, an unborn baby will be able to sense her surroundings through touch from as early as eight weeks. From sixteen weeks she will begin to move around inside the womb, exploring through touch—hand to face, one hand to the other, foot to other leg. In this way the unborn child begins to discover her own body. Indeed by the time she is born she will be able to distinguish self-touch from touch by someone else, a process that helps to establish the sense of self (Rochat and Hespos 1997).

Within the first few weeks of life, the mouth evolves from being a mechanism for gaining nutrition by sucking to being the infant’s chief means for finding out about objects in her world. An infant will use her hands to transport an object to the mouth and then explore it by mouthing in a manner that is dependent on object properties (Rochat 1991). From the start of life, then, we engage in active tactile perception (Prescott, Diamond et al. 2011, Lepora 2015) to understand and interrogate our world. Whereas the mouth and lips are the initial focus for exploration, as we grow older our haptic attention shifts to our hands. Indeed, it is no surprise that humans have lost their facial whiskers during the course of evolution, as our hands more than compensate as devices for tactile exploration of nearby space whilst doubling up as manipulators for dextrous grasping and precise control. When tactile acuity is examined, for instance using Weber’s (1834/1978) “two point discrimination” test, the lips, tongue, and fingertips stand out as the locations on the body with the greatest sensitivity to touch. In each place we are typically able to distinguish points that are as little as one or two millimeters apart (Weber 1834/1978, Weinstein 1968). At the other extreme, in the middle of the back, for instance, the two points can be centimeters apart yet you might still feel them as one, indicating a much lower concentration of tactile sensory afferents. Similar estimates can be made for other measures of sensitivity such as orientation, pressure, point localization and vibration detection. These differences in sensitivity at the periphery are also reflected in the proportions of the human somatosensory homunculus which has huge hands and lips and large feet.

Discriminative touch as a self-structuring sensorimotor activity

To understand active tactile sensing in humans, as in other animals, we need to think of touch as a co-ordinated sensorimotor activity with sensory feedback being a key determinant of future movement and sensory input. Crucially, the dynamic coupling of the sensorimotor system with the environment during active touch alters, or “self-structures”, the flow of information between its different components (sensory, neural and motor) (Barlow 2001, Clark 2013). This can optimize the flow of information in measurable ways, for instance by reducing entropy (disorder) and by increasing mutual information (Lungarella 2005, Pfeifer, Lungarella et al. 2007) making the challenge of understanding the world through touch significantly more tractable.

Self-structuring is evident in the exploratory procedures we engage during haptic tasks (Lederman and Klatzky 1993) (Klatzky and Reed 2009). Each procedure is shaped by the goal (what it is we wish to find out), by the environmental structure, and by the morphology of the hand. The result is a pattern of behavior that is characterizable but not stereotyped, and that isolates and enhances (Gibson 1962) the object properties of interest. For instance, as illustrated in see Figure 12, you might stroke a surface to judge texture (Bensmaia 2009) by applying even pressure with your fingertip, your finger tracing a trajectory that naturally follows the contour of the surface. By contrast, you might squeeze an object between two fingers to assess hardness, or repeatedly enclose it within the hand to determine shape (Kappers and Tiest 2014).

Figure 12: Examples of exploratory procedures in haptic touch for discrimination of texture, hardness, and shape. Photographs by Ben Mitchinson, reproduced with permission.

The notion of perception as inference due to Helmholtz (1866/1962) and Gregory (1980) (for more recent accounts see e.g. Kersten et al., 2004; Friston, Adams et al. 2012), is also important for understanding how the brain can make sense of the fragmentary and often fleeting signals we receive through touch. For instance, encountering a cool, hard surface in your pocket, you might manipulate the object with your fingers to determine the denomination of the coin. Encountering a straight-line edge, during this process, another hypothesis springs to mind—this could be a key. The ambiguity inherent in tactile signals requires the use of expectations (priors) to resolve a cloud of indeterminate stimuli into a specific and concrete percept. Fox, Evans et al. (2012) used an approach of this kind, employing strong top-down Bayesian priors, to construct spatial maps from sparse tactile sense data, Lepora et al. (2013) propose a similar Bayesian approach for simultaneous object localization and identification (SOLID) in fingertip touch.

Naturally, our understanding of tactile signals is also informed by information from other modalities, evidence of how and where this happens is shown in the activation of visual cortical areas during touch (Lacey and Sathian 2015). Being visually-impaired, on the other hand, does not always put you at a disadvantage. Indeed, congenitally blind individuals outperform those with intact vision on many haptic tasks as a consequence of “sensory compensation” thought to involve the recruitment of anatomically visual areas to enhance tactile processing (Heller and Ballesteros 2012).

The gentler side of touch: affect, sociality and sensuality

Although discrimination and the detection of affordances are critical tasks for tactile sensing, we should not overlook the central role of touch in human emotion. The slow CT fiber system found in other mammals is also present in humans and projects, not to the somatosensory cortices, but to the insula region (Olausson, Lamarre et al. 2002)—part of the Papez circuit for emotion and a gateway to the processing of reward and feeling in the frontal cortex. The soft stroking of the skin, to which the CT afferents are specifically sensitive, can promote release of endogenous opiates and the hormone oxytocin known to be important in pair bonding and in sexual behavior (Uvnäs-Moberg, Arn et al. 2005, Olausson, Wessberg et al. 2010).

The CT fiber system likely mediates the known benefits of gentle social touch which include reducing stress and blood pressure, and raising pain thresholds. The interpersonal effects of social touch may bypass conscious awareness. A light touch on the hand or the shoulder, can induce you to give a waiter a larger tip without realizing why (Crusco and Wetzel 1984)—the astute waiter is tapping in to a subliminal mammalian channel for bonding via touch. Social touch also plays a notable role in communicating affect. For instance, Hertenstein, Holmes et al. (2009) asked people to send emotional signals in the way they touched one another (no speaking or eye contact allowed). They found that people could communicate up to eight different emotions—fear, anger, disgust, sadness, gratitude, sympathy, happiness, and love—through touch alone, and with an accuracy of nearly eighty percent. Although CT fibers do not appear to penetrate glabrous skin, it is undoubtedly true that touch on surfaces such as the fingers and lips is often reported as pleasant. One possibility, suggested by McGlone, Olausson et al. (2012) is that sensing in glabrous skin is primarily discriminatory, but that we learn to associate certain patterns of stimulation with positive affect.

Touch is also hugely important to human sexual behavior (see e.g. Gallace and Spence 2014), although research on sensual touch is somewhat limited owing to social taboos. We know, however (and this is no surprise), that some of the most sensitive areas for touch on the human body are in the genitals, particularly, the male penis glans and the female clitoris (Soderquist 2002). Both sites have the same mechanoreceptors and sensory nerve endings found in other areas of the skin rather than having any specialized receptor types. Projections travel to at least two areas of S1 cortex, to secondary somatosensory cortex, and to the posterior insula, the latter presumably being key for processing the affective aspects of genital stimulation (Cazala, Vienney et al. 2015).

Research on genital touch has important social and medical consequences. For instance, a number of studies have found reduced sensitivity in the circumcised penis, compared to uncircumcised (Bronselaer, Schober et al. 2013, Gallace and Spence 2014) raising questions about the use of circumcision as a surgical treatment and as a cultural practice. Research on female tactile sensitivity has failed to find support for a distinct erogenous zone on the vaginal wall, sometimes known as the G spot, helping to demystify our understanding of female sexual arousal (Hines, 2001).

Whilst touch is clearly of great importance to human sexual response we should also note that its arousing effects strongly depend upon perception in other modalities, and on the broader psychological, social and cultural context. The flip-side of pleasurable touch is pain. Again specific neural pathways are involved (Derbyshire 2014), but as with pleasure, how and where in the wider brain these signals are processed, and what other contextual signals are present, will be critical to how there are subjectively experienced. Neither pleasure nor pain, is, in the end, simply the result of this or that kind of stimulus, or of activation in a particular kind of nerve fibre; both are, in a more holistic way, states of mind and body.

The benefits to personal well-being of affective touch are reflected in the universal interest in the therapeutic or healing potential of tactile stimulation. Beyond the immediately rewarding and restorative effects noted above for gentle stroking touch, there is evidence for some longer-term benefits, for instance in relieving chronic pain. A possible mechanism that could underlie such a lasting impact involves the reorganization of distorted somatotopic maps through gentle repeated stimulation (Kerr, Wasserman et al. 2007). The idea of using stimulation to unlearn a distorted brain map has also led to treatments such as mirror visual feedback for phantom limb pain (Ramachandran and Brang 2009), and could potentially lead to therapies for a wider range of touch disorders (van Stralen and Dijkerman 2011).

Synthetic touch for haptic interfaces, robots, prostheses and virtual worlds

Touch sensing was a relatively slow starter in the realm of consumer electronics. Although we can think of the electronic keyboard as tactile input device, in its original manifestation this was essentially a bank of on-off switches. All that changed, however, with devices such as track pads for laptop computers and touch screens for phones and tablets. Since the turn of the century, haptic interfaces have become commonplace. Every smart-phone and tablet, and many computers now have a touch sensitive screen (Zhai, Kristensson et al. 2012), and laptops now replace the conventional mouse with an intelligent track-pad. These devices distinguish single from multiple touch, and track the direction and speed of motion, and possibly pressure. The remarkable speed with which haptic interfaces have been adopted is an indication of how natural it seems for people to interact with objects in this way—our electronic devices are at last catching up with the human predilection for fast and precise object manipulation and our ability to communicate intention through a simple touch (Vincent, Oliver et al. 2004).

In robotics, touch was also, for a long time, the sensor system of last resort—a warning that something unexpected has happened. However, the latest generation of tactile sensing devices suggest that we are finally starting to catch up with nature which has always used touch as key modality for finding out about the world. Tactile sensing for robotics does not appear to be converging on a specific preferred transducer type, rather, as in animal integument, there are many different types of sensor each one having benefits and limitations that make it suited to some sensing challenges and not others (Martinez-Hernandez 2015). A significant driver of technology development has been biomimetics—the goal to create an artificial fingertip or covering with the tactile sensitivity of human skin. Within the last decade many fingertip-like sensors have been developed for robot hands and grippers (see, e.g. figure 13) although matching the human hand for the range of stimulus types it can recognise, and for its sensitivity and resolution is still some way off. Biomimetics is also looking to other species, and tactile systems found in nature. For instance, sensors that resemble insect antennae have been developed for a variety of wheeled and legged-robots (Russell 1985, Kaneko, Kanayama et al. 1998, Lewinger, Harley et al. 2005, Lee, Sponberg et al. 2008), and artificial vibrissae have been investigated both for robots operating in air, and those immersed in water (Prescott, Pearson et al. 2009, Eberhardt, Shakhsheer et al. 2011, Pipe and Pearson 2015).

Figure 13: Shadow Dexterous Robot Hand holding a lightbulb. Robot hands, such as the Shadow, are typically able to sense forces, micro-vibrations, and temperature, at multiple positions (taxels). Photograph by Richard Greenhill/Hugo Elias (CC 3.0).

One of the most important roles for touch is likely to be in human-machine interfaces. A key technology will be tactile sensing for prosthetics (Clement, Bugler et al., 2011). Whilst prosthetic hands are already being fitted with fingertip-like transducers, research to interface the outputs of these to the human nervous system, in a way that will allow users to experience a natural feeling of touch, is still in its infancy (but see Raspopovic, Capogrosso et al. 2014; Tan, Schiefer et al. 2014). A non-invasive means to provide such an interface could be through the development of haptic display technologies that are evolving rapidly as a means to deliver complex stimulus patterns to areas of skin (Visell 2009, Kim and Harders 2015), taking advantage of the capacity of the human nervous system to discover meaning in novel patterns of peripheral stimulation. Haptic displays have long been a focus of research in sensory substitution, or sensory augmentation, beginning with the Polish ophthalmologist Kazimierz Noiszewski who, in the 1880s, invented a device to convert light energy into patterns of tactile stimulation called the electroftalm, or “artificial eye”. Other pioneering devices, created by Starkiewicz and Kuliszewski (1963) and by Bach-y-Rita (1972) also took visual images and displayed them as a pattern of vibration on the skin of the user. Research into sensory augmentation has discovered the importance of mapping into the sensing bandwidth, resolution, and psychophysics of the modality into which a signal is being converted. For instance, when going from vision to touch it is important to consider that tactile sensing in the human skin cannot match the spatial resolution of the eye, but that it does have good temporal resolution.

Some of the most effective augmentation or substitution devices operate by tapping into the active nature of human tactile sensing—allowing the human user to direct what might be a relatively low resolution device to explore areas of particular interest (Kra, Arieli et al. 2015). A related idea, originating from the enactive perspective (e.g. Varela, Thompson et al., 1993), is to seek to make the interface device “experientially transparent” (Froese, McGann et al. 2012) such that the goal-directed behavior of the user naturally incorporates properties of the artifact including its capacity to transform from one sensory modality to another. Examples of effective devices adopting this approach include the enactive torch (Froese, McGann et al. 2012) that gives the user an augmented distance sense, and the feelspace belt (Nagel, Carl et al. 2005) that provides the wearer with a novel compass sense via touch.

Figure 14: The Electroftalm developed by Starkiewicz and Kuliszewski in the 1960s was one of a number of pioneering attempts to create a sensory substitution device for the visually-impaired that mapped the visual scene to a pattern of vibration on the surface of the skin.

Just as touch screens and trackpads have accelerated the developing of tactile sensors, telecommunication and virtual reality applications are beginning to drive the development of a new generation of haptic displays, that can enable, for instance, remote affective communication through the internet (Cheok and Pradana 2015). The possibility of immersive virtual reality in which tactile experience comes close to anything that can happen in the real world is far off, however, the importance of touch to our species is such that technologies that even crudely approximate a feeling of touch could have far-ranging applications, from touch-assisted key-hole surgery, to accurate manipulation of objects with robot hands, to a virtual handshake with a person in another country. The possibilities for synthetic touch are vast, and like much of the world of biological touch, we are only just beginning, so to speak, to feel our way.

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Internal References

• Ahissar, E; Shinde, N and Haidarliu, S (2015). Systems neuroscience of touch. Scholarpedia 10: 32785. http://www.scholarpedia.org/article/Systems_Neuroscience_of_Touch. (see also pages mmm-nnn of this book)

• Barth, F G (2015). A spider's tactile hairs. Scholarpedia 10(3): 7267. http://www.scholarpedia.org/article/A_spider%27s_tactile_hairs. (see also pages mmm-nnn of this book)

• Bensmaia, S (2009). Texture from touch. Scholarpedia 4(8): 7956. http://www.scholarpedia.org/article/Texture_from_touch. (see also pages mmm-nnn of this book)

• Brembs, B (2014). Aplysia operant conditioning. Scholarpedia 9(1): 4097. http://www.scholarpedia.org/article/Aplysia_operant_conditioning.

• Cheok, A and Pradana, G A (2015). Virtual touch. Scholarpedia 10: 32679. http://www.scholarpedia.org/article/Virtual_touch. (see also pages mmm-nnn of this book)

• Crish, C M; Crish, S D and Comer, C M (2015). Tactile sensing in the naked mole rat. Scholarpedia 10(3): 7164. http://www.scholarpedia.org/article/Tactile_sensing_in_the_naked_mole_rat. (see also pages mmm-nnn of this book)

• Derbyshire, S (2014). Painful touch. Scholarpedia 9(3): 7962. http://www.scholarpedia.org/article/Painful_touch. (see also pages mmm-nnn of this book)

• Dürr, V (2014). Stick insect antennae. Scholarpedia 9(2): 6829. http://www.scholarpedia.org/article/Stick_Insect_Antennae. (see also pages mmm-nnn of this book)

• Grasso, F and Wells, M (2013). Tactile sensing in the octopus. Scholarpedia 8(6): 7165. http://www.scholarpedia.org/article/Tactile_sensing_in_the_octopus. (see also pages mmm-nnn of this book)

• Haidarliu, S (2015). Whisking musculature. Scholarpedia 10(4): 32331. http://www.scholarpedia.org/article/Whisking_musculature. (see also pages mmm-nnn of this book)

• Hanke, W and Dehnhardt, G (2015). Vibrissal touch in pinnipeds. Scholarpedia 10(3): 6828. http://www.scholarpedia.org/article/Vibrissal_touch_in_pinnipeds. (see also pages mmm-nnn of this book)

• Heller, M and Ballesteros, S (2012). Visually-impaired touch. Scholarpedia 7(11): 8240. http://www.scholarpedia.org/article/Visually-impaired_touch. (see also pages mmm-nnn of this book)

• Kappers, A and Bergmann Tiest, W (2014). Shape from touch. Scholarpedia 9(1): 7945. http://www.scholarpedia.org/article/Shape_from_touch. (see also pages mmm-nnn of this book)

• Kim, Y and Harders, M (2015). Haptic displays. Scholarpedia 10: 32376. http://www.scholarpedia.org/article/Haptic_Displays. (see also pages mmm-nnn of this book)

• Klatzky, R and Reed, C L (2009). Haptic exploration. Scholarpedia 4(8): 7941. http://www.scholarpedia.org/article/Haptic_exploration. (see also pages mmm-nnn of this book)

• Knutsen, P (2015). Whisking kinematics. Scholarpedia 10: 7280. http://www.scholarpedia.org/article/Whisking_kinematics. (see also pages mmm-nnn of this book)

• Kra, Y; Arieli, A and Ahissar, E (2015). Tactile substitution for vision. Scholarpedia 10: 32457. http://www.scholarpedia.org/article/Tactile_Substitution_for_Vision. (see also pages mmm-nnn of this book)

• Lacey, S and Sathian, K (2015). Crossmodal and multisensory interactions between vision and touch. Scholarpedia 10(3): 7957. http://www.scholarpedia.org/article/Crossmodal_and_multisensory_interactions_between_vision_and_touch. (see also pages mmm-nnn of this book)

• Lepora, N (2015). Active tactile perception. Scholarpedia 10: 32364. http://www.scholarpedia.org/article/Active_tactile_perception. (see also pages mmm-nnn of this book)

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• Moayedi, Y; Nakatani, M and Lumpkin, E (2015). Mammalian mechanoreception. Scholarpedia 10: 7265. http://www.scholarpedia.org/article/Mammalian_mechanoreception. (see also pages mmm-nnn of this book)

• Okada, J (2009). Cockroach antennae. Scholarpedia 4(10): 6842. http://www.scholarpedia.org/article/Cockroach_antennae. (see also pages mmm-nnn of this book)

• Pipe, T and Pearson, M (2015). Whiskered robots. Scholarpedia 10: 6641. http://www.scholarpedia.org/article/Whiskered_robots. (see also pages mmm-nnn of this book)

• Prescott, T J; Mitchinson, B and Grant, R A (2011). Vibrissal behavior and function. Scholarpedia 6(10): 6642. http://www.scholarpedia.org/article/Vibrissal_behavior_and_function. (see also pages mmm-nnn of this book)

• Ramachandran, V S and Brang, D (2009). Phantom touch. Scholarpedia 4(10): 8244. http://www.scholarpedia.org/article/Phantom_touch. (see also pages mmm-nnn of this book)

• Reep, R and Sarko, D K (2009). Tactile hair in manatees. Scholarpedia 4(4): 6831. http://www.scholarpedia.org/article/Tactile_hair_in_Manatees. (see also pages mmm-nnn of this book)

• Roth-Alpermann, C and Brecht, M (2009). Vibrissal touch in the Etruscan shrew. Scholarpedia 4(11): 6830. http://www.scholarpedia.org/article/Vibrissal_touch_in_the_Etruscan_shrew. (see also pages mmm-nnn of this book)

• van Stralen, H and Dijkerman, C (2011). Central touch disorders. Scholarpedia 6(10): 8243. http://www.scholarpedia.org/article/Central_touch_disorders. (see also pages mmm-nnn of this book)

• Wilson, S and Moore, C (2015). S1 somatotopic maps. Scholarpedia 10: 8574. http://www.scholarpedia.org/article/S1_somatotopic_maps. (see also pages mmm-nnn of this book)

Sponsored by: Prof. Ehud Ahissar, Department of Neurobiology, The Weizmann Institute, Rehovot

Reviewed by: Prof. Ehud Ahissar, Department of Neurobiology, The Weizmann Institute, Rehovot

Reviewed by: Dr. Nathan Lepora, University of Bristol, Bristol, United Kingdom

Accepted on: 2015-04-24 12:13:15 GMT