Role of whiskers in sensorimotor development of C57BL/6 mice

Abstract

The mystacial vibrissae (whiskers) of nocturnal rodents play a major role in their sensorimotor behaviors. Relatively little information exists on the role of whiskers during early development. We characterized the contribution of whiskers to sensorimotor development in postnatal C57BL/6 mice. A comparison between intact and whisker-clipped mice in a battery of behavioral tests from postnatal day (P) 4-17 revealed that both male and female pups develop reflexive motor behavior even when the whiskers are clipped. Daily whisker trimming from P3 onwards results in diminished weight gain by P17, and impairment in whisker sensorimotor coordination behaviors, such as cliff avoidance and littermate huddling from P4 to P17, while facilitation of righting reflex at P4 and grasp response at P12. Since active whisker palpation does not start until 2 weeks of age, passive whisker touch during early neonatal stage must play a role in regulating these behaviors. Around the onset of exploratory behaviors (P12) neonatal whisker-clipped pups also display persistent searching movements when they encounter cage walls as a compensatory mechanism of sensorimotor development. Spontaneous whisker motion (whisking) is distinct from respiratory fluttering of whiskers. It is a symmetrical vibration of whiskers at a rate of approximately ∼8 Hz and begins around P10. Oriented, bundled movements of whiskers at higher frequencies of ∼12 Hz during scanning object surfaces, i.e., palpation whisking, emerges at P14. The establishment of locomotive body coordination before eyes open accompanies palpation whisking, indicating an important role in the guidance of exploratory motor behaviors.

Keywords: Neonatal motor coordination; Sex differences; Somatosensory development; Tactile sensation; Whisking.

Figure 1

Motor performance in male and female B6 mouse pups with (WT) or without (WC) whiskers. Data are expressed as mean ± S.E.M. * indicates significant differences between WT and WC and ^# indicates age differences compared to P4. In the surface righting test, (a) the latencies for righting their body, and the percentage of observation for (b) locomotion and (c) nose rubbing at a wall during a 60-sec test were measured. In the negative geotaxis test, (d) the latencies for body rotation decrease over development. In the grasp test, the ratio of observation for (e) grasp reflex and (f) grasping response were measured.

Figure 2

Whisker and tactile sensory performance in male and female B6 mouse pups with (WT) or without (WC) whiskers. Data are expressed as mean ± S.E.M. * indicates significant differences between WT and WC and ^# indicates age differences compared to P4. (a) The body weight gains in male and female B6 pups with or without whiskers. In the cliff avoidance test, (b) the latencies for avoidance from a cliff edge, and (c) the number of head dipping observed during a session are presented. In the whisker stimulation test, (d) the number of twitching response and (e) head moving response toward a 30 times whisker stimulation were measured. In the tactile stimulation test, (f) the percentage of twitching responses to total 7 stimulation on their body were calculated.

Figure 3

Huddling with a littermate was observed in male and female B6 mouse pups with (WT) or without (WC) whiskers. Data are expressed as mean ± S.E.M. * indicates significant differences between WT and WC and ^# indicates age differences compared to P4. (a) partial huddling, defined as <40% of pup's body contact with a littermate, and (b) full huddling, defined as >40% of pup's body contact with a littermate that was observed from above camera recording are presented.

Figure 4

Development of whisking behavior observed in B6 mouse pups from P7 through P19. Data are expressed as mean ± S.E.M. (a) The ratio of appearance of whisking behavior (dashed line) and the ratio of active whisking in total observed whisking during an object contact (solid line) were calculated. ^# indicates age differences compared to P7; * indicates significant age differences compared to P12. Whisking behavior in B6 pups emerges around P10 and is consolidated by P11. When exploring an object, pups show active whisking after P14 and the appearance ratio increases over ages. (b) The frequencies of whisker movement including respiratory fluctuation (dashed line), symmetry whisking (open square, solid line), and active whisking (closed circle, solid line) were measured. ^# indicates age differences in respiratory fraction compared to P7. * indicates significant age difmferences in symmetry whisking compared to P10; and + indicates frequencies differences between respiratory fraction and symmetry whisking.

Figure 5

A schematic diagram for development of whisker sensation and exploratory motor coordination in C57BL/6 mouse. Tactile reflex is represented by measuring whisker and skin twitch response and grasp reflection. Reflexive body coordination is shown in measuring righting reflex and negative geotaxis. Exploratory behavior is represented by measuring locomotor activity and cliff avoidance.