Whereas visuomotor behaviors and visual object recognition have been studied in detail, we know relatively little about tactile object representations. We investigate a new model system for the tactile guidance of behavior, namely prey (cricket) capture by one of the smallest mammals, the Etruscan shrew, Suncus etruscus. Because of their high metabolic rate and nocturnal lifestyle, Etruscan shrews are forced to detect, overwhelm, and kill prey in large numbers in darkness. Crickets are exquisitely mechanosensitive, fast-moving prey, almost as big as the shrew itself. Shrews succeed in hunting by lateralized, precise, and fast attacks. Removal experiments demonstrate that both macrovibrissae and microvibrissae are required for prey capture, with the macrovibrissae being involved in attack targeting. Experiments with artificial prey replica show that tactile shape cues are both necessary and sufficient for evoking attacks. Prey representations are motion-and sizeinvariant. Shrews distinguish and memorize prey features. Corrective maneuvers and cricket shape manipulation experiments indicate that shrew behavior is guided by Gestalt-like prey descriptions. Thus, tactile object recognition in Etruscan shrews shares characteristics of human visual object recognition, but it proceeds faster and occurs in a 20,000-times-smaller brain.active touch ͉ barrel cortex ͉ object recognition ͉ Suncus etruscus ͉ whisker

The Etruscan shrew, Suncus etruscus, is one of the smallest mammals. Etruscan shrews can recognize prey shape with amazing speed and accuracy, based on whisker-mediated tactile cues. Because of its small size, quantitative analysis of the Etruscan shrew cortex is more tractable than in other animals. To quantitatively assess the anatomy of the Etruscan shrew's brain, we sectioned brains and applied Nissl staining and NeuN (neuronal nuclei) antibody staining. On the basis of these stains, we estimated the number of neurons of 10 cortical hemispheres by using Stereoinvestigator and Neurolucida (MBF Bioscience) software. On average, the neuron number per hemisphere was found to be ~1 million. We also measured cortical surface area and found an average of 11.1 mm² (n = 7) and an average volume of 5.3 mm³ (n = 10) per hemisphere. We identified 13 cortical regions by cytoarchitectonic boundaries in coronal, sagittal, and tangential sections processed for Nissl substance, myelin, cytochrome oxidase, ionic zinc, neurofilaments, and vesicular glutamate transporter 2 (VGluT2). The Etruscan shrew is a highly tactile animal with a large somatosensory cortex, which contains a barrel field, but the barrels are much less clearly defined than in rodents. The anatomically derived cortical partitioning scheme roughly corresponds to physiologically derived maps of neocortical sensory areas.

The Etruscan shrew, Suncus etruscus, is not only the smallest terrestrial mammal, but also one of the fastest and most tactile hunters described to date. The shrew's skeletal muscle consists entirely of fast-twitch types and lacks slow fibres. Etruscan shrews detect, overwhelm, and kill insect prey in large numbers in darkness. The cricket prey is exquisitely mechanosensitive and fast-moving, and is as big as the shrew itself. Experiments with prey replica show that shape cues are both necessary and sufficient for evoking attacks. Shrew attacks are whisker guided by motion- and size-invariant Gestalt-like prey representations. Shrews often attack their prey prior to any signs of evasive manoeuvres. Shrews whisk at frequencies of approximately 14 Hz and can react with latencies as short as 25–30 ms to prey movement. The speed of attacks suggests that shrews identify and classify prey with a single touch. Large parts of the shrew's brain respond to vibrissal touch, which is represented in at least four cortical areas comprising collectively about a third of the cortical volume. Etruscan shrews can enter a torpid state and reduce their body temperature; we observed that cortical response latencies become two to three times longer when body temperature drops from 36°C to 24°C, suggesting that endothermy contributes to the animal's high-speed sensorimotor performance. We argue that small size, high-speed behaviour and extreme dependence on touch are not coincidental, but reflect an evolutionary strategy, in which the metabolic costs of small body size are outweighed by the advantages of being a short-range high-speed touch and kill predator.

Cortical organization in the Etruscan shrew is of comparative interest because of its small size and because the Etruscan shrew is an amazing tactile hunter. Here we investigated cortical organization in Etruscan shrews by electrophysiological mapping. We developed an anesthesia protocol for this very small mammal in which we combined massive application of local anesthesia, very slow induction of general anesthesia, and passive cooling. Under this anesthesia regime, we characterized auditory, visual, and somatosensory cortical responses. We found that large parts of shrew cortex respond to such stimuli. Of the responsive sites, a small fraction (∼14%) responded to visual stimuli in a caudally located region. Another small fraction of sites (∼11%) responded to auditory stimuli in a centrally located region. The majority of sites (∼75%) responded to tactile stimuli. We identified two topographically organized somatosensory areas with small receptive fields referred to as putative primary somatosensory cortex and putative secondary somatosensory cortex. In a posterior-lateral region that partially overlaps with piriform cortex, we observed large somatosensory receptive fields and often polysensory responses. In an anterior-lateral region that partially overlaps with piriform cortex, we observed large unimodal somatosensory receptive fields. Our findings demonstrate a remarkable degree of tactile specialization in Etruscan shrew cortex.

A crucial role of tactile experience for the maturation of neural response properties in the somatosensory system is well established, but little is known about the role of tactile experience in the development of tactile behaviors. Here we study how tactile experience affects prey capture behavior in Etruscan shrews, Suncus etruscus. Prey capture in adult shrews is a high-speed behavior that relies on precise attacks guided by tactile Gestalt cues. We studied the role of tactile experience by three different approaches. First, we analyzed the hunting skills of young shrews' right after weaning. We found that prey capture in young animals in most, but not all, aspects is similar to that of adults. Second, we performed whisker trimming for 3–4 weeks after birth. Such deprivation resulted in a lasting disruption of prey capture even after whisker re-growth: attacks lacked precise targeting and had a lower success rate. Third, we presented adult shrews with an entirely novel prey species, the giant cockroach. The shape of this roach is very different from the shrew's normal (cricket) prey and the thorax—the preferred point of attack in crickets—is protected by a heavy cuticle. Initially shrews attacked giant roaches the same way they attack crickets and targeted the thoracic region. With progressive experience, however, shrews adopted a new attack strategy targeting legs and underside of the roaches while avoiding other body parts. Speed and efficiency of attacks improved. These data suggest that tactile experience shapes prey capture behavior.