The neurobiology of Etruscan shrew active touch

Abstract

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.

Figure 1.

The Etruscan shrew and its vibrissal system. (a) An Etruscan shrew and a field cricket. The € cent coin is 16.25 mm in diameter. (b) Frontal view of the head of a shrew. (c) Etruscan shrew whisker array; the longest shrew macrovibrissae are ca 12 mm long. The scale shows millimetres. (d) High magnification view of the microvibrissae surrounding the mouth. (e) Schematics of vibrissal sensing volumes [1] (grey) and body size in the Etruscan shrew, the rat (middle) and the harbour seal (bottom). The percentage value refers to the length the longest facial vibrissa and states the percentage of body length that this whisker reaches.

Figure 2.

Precision and speed of shrew attacks. (a,b) Shrew attacks are selectively placed on the thorax of crickets. Modified from Anjum et al. [6]. (a) Attack histogram derived by analysing video sequences (n = 450 shrew attacks on approx. 130 crickets). (b) Bite mark positions (yellow squares superimposed on a cricket photograph (n = 94 bite marks on 25 freshly killed, immobilized or injured crickets)) and bite mark histogram. (c–e) Mid-attack change of direction. Modified from Munz et al. [7]. (c) Still frames from before and at the end of the attack (time lapse between images = 0.23 s) are overlaid. Dots and circles are the head positions of the shrew and cricket, respectively. Dots and circles are colour-coded for simultaneous head positions of the shrew and cricket. (d) Head speed of the cricket (top) and shrew (bottom). Note the 29 ms lapse between the cricket's speed increase and the shrew's speed increase. Black dotted lines represent 0 cm s⁻¹, red-dotted lines represent the thresholds used to determine the time of speed increase. (e) Average of six such attacks. Black dashed lines are linear fits to the baseline acceleration prior to the sudden increase in cricket acceleration (t = 0 ms). Shaded regions represent ±1 s.e. The difference in time between the cricket and the shrew acceleration increase was 27 ms. (e) Brown curve, cricket; blue curve, shrew.

Figure 3.

Periphery of the Etruscan shrew vibrissal system. (a) Pattern of vibrissal follicles shown in a flattened preparation showing six rows (A–F). Each row contains six to nine whiskers. In addition, there are three whiskers not contained in a row or an arc and labelled X, Y and Z. Scale bar applies to (a) and (b). (b) Ventral view of the shrew's brain. The trigeminal nerve is indicated as black arrows and optic nerve as blue arrows. R, rostral; C, caudal.

Figure 4.

Etruscan shrew neurophysiology. (a) Physiologically derived map of the Etruscan shrew cortex. An average map of cortical regions was delineated by electrophysiological mapping experiments. Dotted areas indicate macrovibrissae responses. S1, primary somatosensory cortex; S2, secondary somatosensory cortex; V, visual cortex; A, auditory cortex; S, somatosensory; RF, receptive field. (b) Whisker responses at different shrew body temperatures. Peristimulus time histograms (1 ms bin size) of multi-unit responses to piezoelectric stimulation (approx. 10° deflection and approx. 1 ms rise time) of a single whisker (n = 20 trials per temperature). Neuronal responses were obtained at the same recording site in putative area S1 while the body temperature of the shrew varied from 36°C (top) to 24°C (bottom). Stimulus onset at time point 0, duration of the stimulus 200 ms, as indicated below. Right: same data as left, but zoomed into the time of stimulus onset. Dashed line indicates the time of first response at 36°C. Note the latency changes with temperatures.