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Phil. Trans. R. Soc. B (2011) 366, 3037–3048
doi:10.1098/rstb.2011.0156
Research
Active vibrissal sensing in rodents and
marsupials
Ben Mitchinson1, Robyn A. Grant1, Kendra Arkley1, Vladan Rankov1,
Igor Perkon2,3,4 and Tony J. Prescott1,*
1
Active Touch Laboratory (ATL@S), Department of Psychology, The University of Sheffield,
Sheffield S10 2TN, UK
2
Cognitive Neuroscience Sector, International School for Advanced Studies, Trieste, Italy
3
Italian Institute of Technology, SISSA Unit, Trieste, Italy
4
LDOS, Faculty of Electrical Engineering, University of Ljubljana, Ljubljana, Slovenia
In rats, the long facial whiskers (mystacial macrovibrissae) are repetitively and rapidly swept back
and forth during exploration in a behaviour known as ‘whisking’. In this paper, we summarize previous evidence from rats, and present new data for rat, mouse and the marsupial grey short-tailed
opossum (Monodelphis domestica) showing that whisking in all three species is actively controlled
both with respect to movement of the animal’s body and relative to environmental structure.
Using automatic whisker tracking, and Fourier analysis, we first show that the whisking motion
of the mystacial vibrissae, in the horizontal plane, can be approximated as a blend of two sinusoids
at the fundamental frequency (mean 8.5, 11.3 and 7.3 Hz in rat, mouse and opossum, respectively)
and its second harmonic. The oscillation at the second harmonic is particularly strong in mouse
(around 22 Hz) consistent with previous reports of fast whisking in that species. In all three species,
we found evidence of asymmetric whisking during head turning and following unilateral object contacts consistent with active control of whisker movement. We propose that the presence of active
vibrissal touch in both rodents and marsupials suggests that this behavioural capacity emerged at
an early stage in the evolution of therian mammals.
Keywords: active sensing; touch; vibrissae; whisking; Monodelphis domestica
1. INTRODUCTION
Whiskers, or vibrissae, are prominent sinus hairs, found
on nearly all mammals that act as specialized sensory
organs for touch [1–4]. Rodents, such as rats and
mice, have the ability to control the position and movement of their long facial whiskers (the mystacial
microvibrissae) relative to the head [5]. This control is
afforded by a specialized musculature, which includes
dedicated muscles, one per whisker, that are intrinsic
to the whisker pad, as well as muscles external to the
pad that can move all of the whiskers together by shifting
the pad or by transforming its shape [3,6–8]. The
characteristic pattern of rat whisker movement, and
also its principal component when viewed from above
[9], is for all of the macrovibrissae (around 35 on each
side of the snout) to move forward together (protract),
and then be pulled back together (retract). This sweeping or scanning motion, known as ‘whisking’, is repeated
successively, many times per second, for periods lasting
several seconds at a time [7,10–12]. Typically, as the
* Author for correspondence ([email protected]).
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rstb.2011.0156 or via http://rstb.royalsocietypublishing.org.
One contribution of 18 to a Theo Murphy Meeting Issue ‘Active
touch sensing’.
whiskers protract they also, but not always, fan out
along the anterior–posterior axis [9,13] and, at the
same time, rotate around the axis of the whisker shaft
[12]. Rats and mice are capable of whisking at high frequencies (rates of over 20 Hz have been reported in mice
[14,15]), and hence the whisking musculature of these
animals contains a high proportion of type 2B muscle
fibres that can support faster contractions than normal
skeletal muscles [14].
Since rapid movement of the vibrissae consumes
energy, and has required the evolution of specialized
musculature, it can be assumed that whisking conveys
some advantage to the animal. These observations
motivate the proposal that whisking is a form of active
sensing according to the definition used in this theme
issue. That is, that animals whisk, and modulate their
whisking behaviour in specific ways, in order to boost
the acquisition of task-relevant sensory information
[9,16]. To fully evaluate this hypothesis, two further
steps are needed. First, we need to accurately describe
the whisker and head movements of behaving animals
under a range of different experimental conditions,
including circumstances where the motivation of the
animal can be reasonably well inferred (e.g. when it
has been trained to perform some whisker-based tactile
discrimination task). Second, we need to show that the
types of whisker motion observed in animals, in these
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Active vibrissal sensing
different conditions, positively enhance some relevant
aspects of tactile sensing compared with either the
absence of whisker motion, or to whisker motions that
are unlike those that are naturally expressed. Progress
is being made on both of these issues, described in
more detail below. A parallel approach, that allows for
direct measurement of the effects of sensor movement
on vibrissal sensing, is to develop synthetic (robotic)
whisker systems [17,18], then compare whisker control
strategies similar to those seen in the rat, with strategies
that differ in specific ways. A research programme
directed at this challenge is described in a companion
article in this theme issue [19]. Finally, an approach
that allows us to explore the generality of active vibrissal
sensing, and to investigate its appropriateness to the
different adaptive zones exploited by whiskered animals,
is comparative (cross-species) analysis, which is considered at length in this paper. However, before
embarking on this wider investigation, we first briefly
review some of the evidence so far gathered in relation
to the active vibrissal touch in the rat.
(a) Active sensing strategies in rat whisking
Active sensing implies the ability to vary whisker control
according to context. Conditioning studies have shown
that rats can be trained to vary some of the key parameters of whisking, such as amplitude and frequency
in a stimulus- or task-dependent manner [20–24].
Some persuasive evidence of the role of whisker control
in sensing accuracy has been provided by Carvell &
Simons [23] who showed that good and poor performers
on two types of tactile discrimination tasks were distinguishable in terms of spatio-temporal characteristics
of their whisker movements. Measures of whisker movement in that study also showed some consistent taskrelated differences in movement patterns between
microgeometric (texture) and macrogeometric (shape)
discrimination tasks. Zuo et al. [24] have shown that animals whose whiskers are trimmed are able to alter their
whisker movements in order to improve their success
on a texture discrimination task.
Further indicators that whisking is actively controlled are provided by studies of tactile exploration.
High-speed video recordings show that the whisker
movements of freely moving animals often diverge
from the regular, bilaterally symmetric and synchronous
motor patterns that are usually seen in head-restrained
animals. Asymmetries, asynchronies and changes in
whisk amplitude and timing have been noted, some of
which appear likely to boost the amount of useful sensory information obtained by the animal [6,9,16,25].
Forms of whisking modulation that can be considered
to be elements of active sensing control include the
following.
First, it has been shown that during tactile search
behaviour, whisking tends to be biased towards the
direction in which the animal is turning its head [25].
That is, as the head moves in space, whisking movements
appear symmetric around the future orientation of the
head and are consequently asymmetric with respect to
the current head orientation. We henceforth refer to
this experimental observation as head-turning asymmetry
(HTA). Interestingly, during rat neonatal development,
Phil. Trans. R. Soc. B (2011)
the first whisking motions nearly always occur during
turning, and on the side of the animal that is in the direction of the turn [26,27]. Thus, as the infant rat rotates, it
begins to vibrate its whiskers in the direction in which it is
moving, showing a similar anticipatory bias towards the
area of free space into which the animal is moving. This
might be considered to be an immature form of HTA.
Second, unilateral contact with a nearby surface tends
to reduce whisking amplitude on the side of the snout
ipsilateral to that contact and increase amplitude on
the contralateral side [16]. We term this observation contact-induced asymmetry (CIA). CIA appears to function
so as to prevent ipsilateral whiskers from bending hard
against the contacted object, while increasing the
number of contacts made with that object by whiskers
on the contralateral side. CIA is observed in juvenile
rats some time after the onset of bilateral whisking
(typically delayed by a few days), suggesting that this
form of control may be experience-dependent or rely
on relatively late-maturing brain pathways [27].
Third, when the whiskers of the rat contact an
unexpected object they cease to protract within a
very short time period (typically within 15 ms)
[9,16]. This rapid cessation of protraction (RCP) again
serves to make whisker– surface contacts lighter than
they might otherwise have been. In situations where
there are unilateral contacts or where bilateral contacts
are not simultaneous, RCP also appears to induce
asynchronies in the relative timing of whisker movements on the two sides of the snout. Interestingly,
when trained to make a specific discrimination, animals may modify this aspect of control and allow the
whiskers to bend more strongly [28]. Further, when
the whiskers touch a non-attended surface they may
also show more pronounced bending [16], suggesting
that RCP is not simply the consequence of some
low-level reflex, but is related in some way to the
current goals and focus of the animal.
Fourth, rats appear to regulate the angular separation, or spread, between the whisker columns such
that the whiskers are widely spaced when exploring
across a floor or whisking in open space, but are
more closely bunched when the animal is investigating
an object or surface of interest [9]. This bringing
together of the whiskers appears to occur through
differential control of the angular velocities of the
more anterior and posterior whisker columns. Thus,
during protraction in free-space, the more anterior
columns rotate faster than the posterior ones causing
the whiskers to spread out. During focused exploration
of a surface, on the other hand, the anterior and posterior columns move with similar velocities, so that
low angular separation of the columns is maintained
throughout the whisk [9]. This more foveated style of
whisker movement may also be accompanied by a
forward shift in the set-point (average angular position)
of the whiskers [7]. These aspects of control will tend
to increase the number of whiskers that are brought to
bear on an object of interest.
We can summarize the active sensing role of the
whisking modulations described above as follows.
HTA ensures that the manner in which the whiskers
explore the space surrounding the head is biased
towards the direction of travel; the rat preferentially
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Active vibrissal sensing
investigates the area it is moving into next. CIA, RCP
and the ability to create more foveated patterns of
whisking, all appear to be consistent with a strategy
of making contact with surfaces of interest on as
many whiskers as possible, while minimizing bending
(impingement) of those whiskers such that contacts
are made with a light touch. We have therefore proposed that these modulations collectively promote a
minimal impingement/maximal contact (MIMC) active
sensing strategy for environment exploration [16].
While the focus here is on whisker movement, it is
also important to note that the control of head position
is also critical in determining what contacts are made
by the whiskers with nearby surfaces [9]. Thus, for
instance, while locomoting slowly across a smooth
floor, the head is usually tilted down to allow the whiskers to sample the ground plane directly ahead of the
animal. When a raised object is encountered, the
head tilts upwards so that the whiskers are now
better positioned to sample in the vertical plane. On
encountering a novel object with the macrovibrissae,
the rat will also typically perform an orienting head
movement that will allow directed exploration around
the point of contact with the array of shorter, nonactuated microvibrissae on the chin and lips, and
with other sensory systems located around the tip of
the snout, while the macrovibrissae sample regions of
space to either side of the point of interest.
(b) Which other animals whisk?
Bouts of periodic whisker motion are a defining feature
of how the rat deploys its vibrissae during exploration,
but do other whiskered mammals use their vibrissae in
a similar way? Answering this question will help us to
determine how whisking, and whisking modulation,
contribute to vibrissal sensing and in what circumstances
the ability to move the whiskers is particularly important.
All therian mammals (marsupial and placental
mammals), except humans, have tactile hair at some
point in their lives [4], and even humans have recently
been found to have vestigial sinus hair muscles in their
upper lips [29]. Pocock [2] 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 monetremes, and
that species that lacked whiskers, or in which the
whiskers were less evident, were usually the more specialized members of their order. He concluded that the
possession of facial whiskers was a primitive mammalian
trait. He also noted that the vibrissae tended to be more
pronounced in aquatic or semi-aquatic predators, and in
active scansorial (climbing) or burrowing species. Huber
[3], on reviewing the facial musculature of the different
mammalian orders, reached a similar conclusion—that
early mammals will have possessed prominent, mobile
facial vibrissae and that the emergence of the vibrissal
system played an influential role in establishing a
common ground-plan for the mammalian facial musculature and in driving the re-organization and expansion
of the neopallium (cortex).
Whisking certainly appears to be widespread in
rodents. Specifically, in addition to many species of
rats and mice, whisking has been reported by Welker
Phil. Trans. R. Soc. B (2011)
B. Mitchinson et al.
3039
[5] in flying squirrels (Glaucomys), gerbils (Meriones),
chinchillas (Chinchilla) and hamsters (Mesocricetus). We
have also recently filmed whisking in the hazel
dormouse (Muscardinus), the European field and
water voles (Arvicolinae), the coypu (Myocastor) and
the prehensile-tail porcupine (Coendu). However, while
whisking is common in rodents, it is not universal.
For instance, capybara (Hydrochoerus) and gophers
(Geomys) do not appear to whisk [5], and guinea pigs
(Cavia) appear to display only irregular and relatively
short whisking bouts [14]. Current data, therefore,
suggest that the presence of whisking in animals belong
to at least three of the five rodent sub-orders recognized
by Carleton & Musser [30].
Further research is needed to investigate the commonalities between rodents that display vigorous
whisking and those that do not. While phylogenetic
relationships are clearly important, body-size and lifestyle also appear to matter; for instance, vigorous
whisking has been hypothesized to be more common
in nocturnal animals of smaller size [6]. The circumstances in which whisking is expressed also need to
be further investigated. In seeking to elicit whisking
in a range of species, we have found that it is most
easily observed when animals are exploring their
local environment in an unhurried manner. Exploratory behaviour in new surroundings, and towards
novel objects, similar to that described by Shillito
[31] in the short-tailed vole, can be seen in a range
of rodents and is typically accompanied by prolonged
whisking bouts.
Despite the prevalence of movable whiskers in mammals, there are relatively few descriptions of periodic
whisker motion in non-rodents, although it remains
unclear to what extent whisking is absent in other
mammalian orders or simply under-reported. Welker
[5] described observations suggesting the absence of
whisking in a number of terrestrial and aquatic carnivores with prominent vibrissae, while Wineski [6]
classified animals as showing rapid movement (small
rodents), sporadic movement (larger rodents, some carnivores, lagomorphs), or as having relatively stationary
whiskers (canids, chiropterans, ungulates, higher primates, edentates and cetaceans). Prominent vibrissae
appear to be a characteristic of many carnivores, particularly those that are aquatic or semi-aquatic (e.g.
seals and otters) or nocturnal (e.g. cats and martens).
That whisking is not present in these animals, despite
the ability to move the whiskers, suggests that it is not
specifically an adaptation for prey capture. Andrew
[32] describes whisking as being absent in primates
such as lemurs and lorises. Among non-rodents, rapid
motion of the vibrissae has recently been described
in the Etruscan shrew (Suncus etruscus), a member
of the Soricomorpha (shrew-like mammals) [33,34].
Interestingly, this shrew, which is an efficient insectivorous predator, appears to whisk during the searching
phase of its hunting behaviour and not during the
attack phase (once a prey animal has been located).
We have recently filmed rhythmic whisking, during
locomotion and exploration of objects, in an afrosoricidan, the greater hedgehog tenrec (Setifer setosus);
periodic whisker motion has also been noted in the
sengi (Elephantulus) [32]. Rice [35] observed that
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Active vibrissal sensing
whisking is present in two species of marsupial—the
Brazilian short-tailed opossum (Monodelphis domestica),
and the Virginia opossum (Didelphis marsupialis). That
whisking is seen in rodents and at least some Soricomorpha, Afrosoricidae and marsupials suggests the
presence of this behavioural capacity in a common
ancestor (greater than 125 million years ago) of extant
marsupial and placental mammals [36] as proposed by
Huber [3].
To explore possible commonalities in active vibrissal
sensing, we decided to directly compare whisking in
rodents and marsupials. Within rodents, we examined rats (Rattus norwegicus) as the species in which
whisking has been described in most detail, and the
mouse (Mus musculus) as a near-relative of the rat,
but of significantly smaller body-size. Some of the general characteristics of mouse whisking have previously
been described [14,15,28], with evidence of active
sensing modulation of whisking found in gap-crossing
[15] and object localization tasks [28]. For marsupials,
we chose to examine the grey short-tailed opossum
(M. domestica). There are several reasons for the
choice of this animal. First, this small pouchless marsupial is considered to be a useful species from the
perspective of tracing the evolution of modern mammals. Fossil evidence suggests the presence of
opossum-like animals in the early Cretaceous period
(greater than 100 mya) [36]; hence M. domestica may
have many of the traits possessed by a common ancestor of both modern marsupial and placental mammals.
In particular, the opossum brain has a smaller number
of cortical areas than most mammals [37], lacks a distinct motor cortex, and has relatively few corticospinal
neurons [38]. Thus, it may be reasonably representative of an ancestral mammalian brain (motor cortex
and the corticospinal tract are both new in mammals).
Second, Frost et al. [38] showed that movements of the
vibrissae in M. domestica can be induced by microstimulation of sites in somatosensory cortex, and that this is
the only part of the motor system that appears to be sensitive to cortical stimulation. This finding implies that
control of the vibrissal system may have preceded the
evolution of cortical control over the motor periphery,
and that an examination of the vibrissal movement in
this species might therefore cast some light on the evolution of cortical regulation of movement. Finally, like
all marsupials, M. domestica lacks a corpus callosum
[39]. Since the active control strategies described above
in rats often involve differential control of whisking
behaviour on the two sides of the snout, they will necessarily involve transfer of information across the midline
of the brain. In rats, the corpus callosum has a very
substantial whisker representation [40], which could
conceivably be involved in regulating the asymmetries
and asynchronies seen rat exploratory whisking; hence
it would be interesting to observe whether a mammal
lacking this structure is capable of similar forms of
bilateral active whisking control.
2. METHODS
(a) Animals and behavioural methods
The animals studied were RCS dystrophic (n ¼ 12) and
sighted Hooded Lister (n ¼ 7) rats (R. norwegicus), C57
Phil. Trans. R. Soc. B (2011)
(n ¼ 13) mice (M. musculus) and 26 opossums
(M. domestica). The experimental set-up was similar to
that described in Grant et al. [9]. Briefly, a high-speed,
high resolution (1024 1024) digital video camera was
suspended above a transparent viewing arena illuminated
from below. The animal was placed into the arena
through a hinged lid and allowed to explore the space
freely. In some cases, a rectangular object, such as a
Perspex block, was placed in the arena before the
animal in order to elicit object exploration. Recordings
(‘clips’), of 0.6–6 s duration, were made opportunistically by the experimenter, at 250 or 500 fps, until
the camera memory was full or the animal stopped
exploring. From among hundreds of clips, ‘episodes’
(particular sections of clips) were chosen that appeared
to meet the criteria for each analysis as outlined below.
(b) Whisker tracking and extraction of the
naive mean angle
In each episode chosen for analysis, the animal’s snout
and whiskers were tracked semi-automatically using
the BIOTACT Whisker Tracking Tool. The output
of this operation, for each frame, is the orientation of
the snout (direction of the midline), the position of
the snout tip and a set of parametrized curves fitted
to whisker-like objects located adjacent to the snout
[41], from which (presumed) whisker-base angles
(relative to the midline of the head) are derived. For
opossums, the algorithm was tuned to ensure that
only mystacial vibrissae were detected and not the
prominent genal (cheek) vibrissae. Note that while
automatic tracking usually finds a similar set of
whiskers in adjacent frames, there was no specific
tracking of whiskers across frames. Episodes for
which the automatic detection of the whiskers failed,
as judged by visual inspection, were excluded from
further analysis, as were episodes where substantial
head pitch or roll was present.
Our analyses focus on the movement of the entire
macrovibrissal array on each side of the head, rather
than attempting to quantify the movement of single
whiskers or whiskers columns. To this end, we sought
to summarize the rostro-caudal angular position of the
whiskers on each side. Such a summary has been
implemented in previous work using, for example, the
mean angle of the most rostral and most caudal whiskers
[25] or a mean across the five caudal-most columns [9].
Given the nature of the data produced by the automatic
tracker, we follow [41] by using the mean angle across all
detected mystacial whiskers, low-pass filtered to reduce
noise (30 Hz, zero-phase third-order Butterworth). We
refer to this metric as the naive mean angle (NMA)—
naive, because it ignores the fact that whisker detection
is imperfect and variable between frames and between
sides of the head. A comparison of NMA derived
from automatic tracking with summary measures
derived from manual tracking of a handful of episodes
is given in the electronic supplementary material. Briefly,
NMA appears to capture temporal parameters of
periodic whisking (frequency and phase) accurately,
relative spatial parameters (amplitude) slightly less so,
and absolute spatial parameters (set-point) least accurately (though still reasonably well). Episodes in which
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Active vibrissal sensing
the NMA was judged, by visual inspection, to be a poor
summary of the position of the whiskers were excluded
from further analysis.
(c) Analysis methods
In order to provide a general characterization of whisking within a species, we selected a number of episodes
of whisker motion that occurred when the animal was
moving its whiskers periodically without contacting
anything other than the smooth floor (i.e. with a minimum of sources of whisker movement modulation).
We use the term regular whisking (RW) to describe
the patterns of whisker movement observed under
these circumstances.
To obtain estimates of whisker kinematics from
such an episode, we fitted stationary Fourier-type
series models constrained to have the same primary
frequency, fW, on both sides; fW was also restricted
to 2 – 30 Hz. A one-component model, denoted F1,
had four further (unconstrained) parameters (besides
fW), the phase and amplitude of the single sinusoidal
component on each side. A two-component model
denoted F2, had, correspondingly, eight further parameters besides fW. The second component on each
side of F2 was constrained to have a frequency of
2fW—that is, to represent a harmonic of the first component. The model included a pre-pended filter (zerophase third-order Butterworth, cutoff frequency fW/3)
to remove the slow change in whisking set-point, so
that only the periodic part of the motion remained to
be fitted by the Fourier components. Models were
fitted using multi-starting-point least mean square
with some heuristic interventions (see the electronic
supplementary for details). The frequencies of the primary components, bilateral peak-to-peak amplitude of
the multi-component signal and inter-lateral phase
difference between the primary components, are then
used to describe the periodic whisker motion present
in that episode. In §3, we report peak-to-peak amplitude in two ways. The first (model-based) is the
peak-to-peak amplitude of the F2 model. For the
second (data-based), we measured the peak-to-peak
amplitude of the NMA data, as the maximum minus
the minimum across the episode. Set-point is calculated as the simple average of NMA across the episode.
The amplitude and phase of the second harmonic
of F2 can be used to quantify some of the variability
between episodes in the shape of the whisking profiles.
We report the amplitude of the second harmonic as a
fraction of the amplitude of the first (denoted ‘normalized’), and its phase as the number of degrees of phase
of the first harmonic by which the nearest peak of the
second harmonic precedes the peak of the first (hence,
this value varies between 2908 and þ908). To summarize the relative phase of the second harmonic, we
also compute the power (relative amplitude squared)
for each sample, and sum this in bins regularly distributed across phase, to form the ‘normalized power
density’. The relationship between the phase of the
second harmonic on the two sides was assessed using
simple linear regression.
In addition to estimating the parameters of RW
motion we analysed, for each species, the effect of
Phil. Trans. R. Soc. B (2011)
B. Mitchinson et al.
3041
head-turning and of object contact on bilateral whisker
asymmetry (i.e. testing for the presence of HTA and
CIA active sensing control strategies as defined above).
Further details of each of these analyses are given in §3
and in the electronic supplementary material.
3. RESULTS
(a) Regular whisking kinematics
Thirty one, 44 and 52 episodes of RW were identified
(here, and below, numbers are for rat, mouse and opossum, respectively) and used to provide our general
characterization of whisking kinematics in each species.
While whisker movements in many episodes were
broadly periodic, some episodes did not lend themselves
to the fitting of a (stationary) Fourier series model,
reflecting the fact that whisker movement does not
always consist of exclusively periodic motion.
For each episode we first fitted an F1 model with a
single sinusoidal component on each side. Estimates of
whisking frequency, fW, derived from this model fell
into a narrow range for rat, but were strongly bimodal
in mouse, with peaks in the ranges 9– 14 Hz and
20 –26 Hz. Review of the individual traces and fits
suggested that, rather than indicating whisking in
two distinct frequency bands during different episodes, the latter peak was more likely to be indicating
that a second harmonic in the data was sufficiently
strong to be preferentially fitted by the model in
these episodes. Reasoning that F1 therefore was not
an adequate description of the data, we then fitted
F2 models for all episodes, which included a second
component at twice the primary frequency. Estimates
of fW from F2 fell exclusively into a relatively narrow
range in both rat (7 – 10 Hz) and mouse (9 –13 Hz)
episodes. In opossum, frequency displayed a broader
peak, ranging from 3 to 11 Hz, and therefore the distributions returned by the two models were not
clearly distinguished. All results presented below are
derived from F2 (results from F1 are included in the
electronic supplementary material, along with details
of the semi-automatic model fitting process).
Episodes in which the final (F2) model explained
less than 33 per cent of the variance in NMA (1, 7,
4 per species), as well as those less than two whisk
periods in length after model fitting (6, 7, 13), were
excluded from further analysis. This left 24, 30 and
35 episodes for the three species (mean duration
across all species 540 ms). Examples of good F2
model fits are given in figure 1. In general, rat and
opossum data allowed for convincing modelling
(median explained variance 80 and 76%, respectively),
whereas fits for mouse were poorer (median 62%). In
addition, we estimated locomotion speed as the total
distance travelled by the snout tip during the episode
divided by the episode duration.
Summary statistics of whisking frequency and peak-topeak amplitude averaged across the two sides (both databased and model-based measures), interlateral phase
difference and locomotion speed obtained from our analyses
of RW in each species are given in table 1; plots of their
distributions are shown in figure 2. A comparison
between the kinematic variables measured from each
individual in each species set is included in the electronic
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3042
protraction
angle (°)
(a)
B. Mitchinson et al.
Active vibrissal sensing
120
100
80
60
protraction
angle (°)
(b)
140
120
100
protraction
angle (°)
(c)
120
100
80
time (ms)
Figure 1. Examples of the better fitting models included in
the analysis, for (a) rat, (b) mouse and (c) opossum. Pale
grey is raw NMA, blue/green are left/right smooth NMA,
magenta is the set-point trend, and red is the bilateral
sinusoidal model. Scale bars, 50 ms.
supplementary material—broadly, the results for
individual animals are consistent with the results
pooled over each species. Below, we note some of the
most interesting characteristics of these data.
Whisking frequency in both rat and mouse was relatively invariant across episodes; on average, mouse
whisking is faster than that of rat (by approx. 35%), as
might be expected from previous analyses [14].
Frequency in opossum was much more broadly distributed, covering the range observed in rat as well as
including plenty of examples of much slower movement,
leading to a somewhat slower average overall.
Peak-to-peak amplitude estimates derived from the
data were typically 50– 100% higher than those
obtained from the model, primarily reflecting the fact
that they include the movement in set-point during
the episode (e.g. figure 1), and are reasonably similar
to estimates from previous reports (e.g. [14]). We
also provide the model-based estimate because it
focuses on the amplitude of the periodic motion, ignoring lower frequency changes in set-point; the value of
this metric in rat (about 308) is consistent with a previous report [22]. Whisking amplitude based on either
estimate was quite variable within each species; across
species, mean estimates were significantly higher in rat,
though the highest values of amplitude in all three
species, using either estimate, were fairly similar.
Interlateral phase difference was relatively low (almost
exclusively less than 208) in rat and opossum, indicating
strongly synchronous bilateral whisking. Some larger
magnitude values were found in mouse; however, the
lower model fitting scores (median explained variance
62%) and lower amplitude of whisking in mouse
would both be expected to lead to noisier estimates of
this parameter. Further investigation is required to
establish whether bilateral synchrony is significantly
different in these species. A recent description of whisker
Phil. Trans. R. Soc. B (2011)
movements in head-fixed mice performing a localization
task [28] does suggest that the bilateral movement can
become decoupled in these animals.
The whisking set-point (mean angle throughout episode) was higher in mouse than in rat or opossum,
indicating that mouse whiskers were on average more
protracted than the other two species.
Locomotion speed varied significantly across species,
mice being the fastest movers, then rats, then opossums. Whisking behaviour is likely to be affected by
locomotion, although the relationship between body
movement and whisking has yet to be adequately
described. Note that the significant species differences
in whisking kinematics reported in table 1 are after
controlling for the variation in locomotion speed.
The second harmonic components of F2 are further
analysed in figure 3. In both rat and opossum, the
second harmonic was relatively weak (almost exclusively
less than 30% of the amplitude of the first-model
component), indicating that the whisker movements in
our recordings of these species, obtained during free
movement across a smooth floor, are fairly simple waveforms. However, in mouse, variability in movement
shape was very much a feature of the data, and this is
reflected in the high amplitude (almost exclusively
greater than 30%) of the second harmonic in the F2
model. As shown, the phase and amplitude of the
second harmonic, relative to the first, dictate the shape
of the individual whisks. Note that in episodes with
a very strong second harmonic, the data could be
alternatively interpreted as whisking at the frequency
of the second harmonic, as reflected in the frequency
distributions generated by F1 (see the electronic supplementary material). No strong relationship was
found between the phases of the second harmonics on
the two sides in mouse, either in the full set (n ¼ 30,
r 2 ¼ 0.06, p ¼ 0.21) or in a focused set including only
the examples for which the mean second harmonic
amplitude was above the median of the full set (n ¼ 18,
r 2 ¼ 0.01, p ¼ 0.69).
(b) Head-turning asymmetry
Towal & Hartmann [25] reported that rats motivated
to search in free space for a water reward displayed a
very reliable HTA, such that the whiskers led headturning movements (were symmetric around the
future head orientation) by approximately the duration
of one whisk (115 ms, matching the mean whisking
frequency reported above). To assess whether HTA
is expressed under our conditions of unconstrained
exploratory behaviour, we reprised their analysis
exactly, save for the use of automatic tracking.
For this analysis, 17, 29 and 48 episodes were identified for rat, mouse and opossum, respectively, wherein
the animal was executing head turns and its whiskers
were not contacting anything other than the floor.
Estimates of bilateral asymmetry were calculated on
a frame-by-frame basis as the difference (left – right)
between the instantaneous NMAs on the two sides
of the snout. Values close to zero indicate similar
whisk amplitudes on the two sides of the snout, and
positive/negative values biases towards the left/right
sides of the animal. This value was compared with
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frequency (%) frequency (%) frequency (%)
Active vibrissal sensing
B. Mitchinson et al.
3043
60
40
20
60
40
20
60
40
20
4
8
12
frequency (Hz)
10
30
50
model amp. (°)
10
30
50
data amp. (°)
−40
0
40
interlat. phase (°)
80 100 120 0
100
200
set-point (°)
loco. speed (mm s–1)
Figure 2. Kinematic parameters of regular whisking (RW). Distribution of kinematic parameters during RW (rat, mouse and
opossum, from top to bottom). The mean of each distribution is marked as a vertical line.
Table 1. Cross-species comparison of whisking kinematics. Values shown are ‘mean (standard deviation)’. There was a
significant overall difference in measures of regular whisking kinematics after controlling for differences in locomotion speed
(MANCOVA: F10,164 ¼ 16.806, p , 0.001). Differences for specific measures are computed using MANCOVA, with
locomotion speed as a covariate, except for locomotion speed itself (ANOVA). Effect-size measure is partial h-squared, post
hoc comparisons used a Bonferroni test.
species
n
whisking
frequency (Hz)
amplitude
data-based (8)
amplitude
model-based (8)
interlateral phase
difference (8)
set-point
(8)
locomotion
speed (mm s21)
rat (R)
24
8.55 (0.62)
43.19 (7.65)
29.19 (7.14)
1.67 (11.28)
96.65 (9.21)
mouse
(M)
opossum
(O)
F2,89
p
effect size
post hoc
30
11.35 (0.95)
31.25 (11.64)
16.21 (6.49)
1.69 (29.96)
35
7.32 (1.91)
36.04 (9.53)
18.84 (5.10)
21.38 (11.34)
49.311
,0.001
0.537
M.R.O
8.858
,0.001
0.172
R . M,O
31.334
,0.001
0.424
R . M,O
0.076
0.927
0.002
n.a.
100.63
(9.21)
112.53
(6.85)
94.42
(9.01)
20.501
,0.001
0.325
M . R,O
the angular velocity (positive values indicating anticlockwise) of the head at the same instant. Figure 4
displays the results, pooled within each species. Note
that each panel is directly comparable with fig. 6a of
Towal & Hartmann [25] for rat, but for the differences
in experimental paradigm.
All species expressed robust HTA (R 0.40,
p , 0.001) of the expected polarity (i.e. turning to
the left predicted greater protraction on the right, see
inset example in figure 4), but the magnitude of
the response was consistently less strong in all species
than that reported previously (coefficient of linearity is
28 to 35 compared with 115 in Towal & Hartmann
[25]). Thus, while HTA is clearly expressed under
conditions of free exploration, and in all tested species,
the modulation may be less strong than in the tactile
search paradigm employed in the original study. The
apparently lesser strength of HTA modulation in free
exploration may reflect a real reduction owing to the
less focused nature of the task, or it might be due to
confounding with other effects that were less pronounced in the particular condition targeted by
Towal & Hartmann. For instance, contacts with the
Phil. Trans. R. Soc. B (2011)
132.00 (8.24)
71.66 (7.63)
14.47
,0.001
0.252
M . R,O
floor may be a significant driver of whisking behaviour
(in the previously reported condition, there was no
floor present). Our main finding, however, is that all
three species express this effect robustly.
(c) Contact-induced asymmetry
In previous work in our laboratory [16], we reported that
the location of a nearby wall (vertical plane obstacle) was
a strong predictor of whisking asymmetry—that is, a
difference in bilateral whisking amplitude with increased
amplitude, as measured through recordings of mystacial
muscle electromyogram, on the side of the snout furthest
from the wall and reduced amplitude on the side closest
to the wall. That study also showed that an obstacle
directly ahead tended to excite protraction bilaterally.
We reprised this analysis of CIA across the three species
examined in the current study, but using automated
whisker tracking in place of EMG.
Twenty four, 23 and 44 clip regions were identified
for rat, mouse and opossum, respectively, in which the
animal was interacting with one corner of a smooth
rectangular object with the object ahead of the
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B. Mitchinson et al.
Active vibrissal sensing
1>
power (normalized)
(c)
frequency (%)
(a)
1
2
0.5 1.0 1.5
amplitude (norm.)
−60 0 60
phase (°)
3
4
(b)
amplitude (norm.)
protraction angle
3044
2
6
5
1
3
5
4
1
0
−60 −30 0
30
phase (°)
2
6
60
time (ms)
−180 0 180
phase (rad)
Figure 3. Characteristics of the second harmonic. (a) Second harmonic normalized amplitude is usually weak in rat (red) and
opossum (blue), but usually strong in mouse (green). Normalized power density graphs show that the bulk of the second
harmonic power in mouse falls between 08 and 608 prior to the peak of the primary—owing to weak harmonics in rat and
opossum, phase is poorly defined. (b) The location of the second harmonic in phase-amplitude space determines the shape
of the whisker movement. (c) Six examples taken from the data (blue) with overlaid F2 model (red), from different regions
of phase-amplitude space (numbers inset to each panel correspond to numbers in lower left scattergram, showing the parameters of the second harmonic of the model for that example). (Panels to right) Model whisk profile (red) is formed from
the primary (thick grey line) and secondary (thin grey line) components. (c) Panel (1, rat) is an example of a weak second
harmonic, typical for rat and opossum, resulting in a fairly sinusoidal profile. Panels (2, opossum) and (3– 6, mouse) show
the shape of the whisk with the second harmonic in different parts of phase-amplitude space. Panel (6) shows a very strong
second harmonic, swamping the first, such that the whisking could be interpreted as being high frequency (approx. 20 Hz);
however, the best-fit model in this example has a primary frequency of approximately 10 Hz and a secondary at approximately
20 Hz. Scale barsare 50 ms and 108.
animal and no other nearby obstructions, other than
the floor, that could contact the whiskers. The location
of the object was summarized by manual identification
of its corner; this location was then transformed into a
‘head-centric’ x – y coordinate system with the origin at
the snout tip and the animal facing upwards (along
the positive y-axis). Thus, the object ‘moves around’
in the head-space of the animal. The NMA measure
for each side of the snout was low-pass filtered
(zero-phase 500 ms boxcar) to remove the periodic
component and leave only an estimate of set-point.
This number was then normalized by subtracting
from this signal the mean set-point for the species
during RW (table 1) to give the instantaneous relative
set-point for each side of the snout. Thus, we
obtained two numbers for each frame, with positive/
negative indicating more/less protracted whisker
positions on a given side than was typical for RW
episodes recorded for that species. These numbers
were then pooled across all episodes for each species.
Finally, assuming that the animals did not express
any behavioural bias to one side or the other, samples
with the object on the right-hand side of the head were
flipped, so that the object location was always on the
left-hand side—this allows us to consider movements
Phil. Trans. R. Soc. B (2011)
of the two whisker arrays classified as either ipsilateral
or contralateral to the obstruction. Ipsilateral object
location was then binned on a regular grid, and the
average relative set-point calculated for each bin; the
results are displayed in figure 5. Our main finding is
that all tested species robustly displayed the expected
basic pattern of CIA—reduced protraction ipsilaterally, increased contralaterally. Increased protraction,
for objects directly ahead, reported in rats by Mitchinson et al. [16] was apparent in opossum, less so in rat,
and not evident in mouse.
4. DISCUSSION
(a) Describing the movement of vibrissal arrays
The characteristic sweeping motion of mammalian
whisking can be measured in an intact whisker field
by automated processing of high-speed digital video
sequences [41], which extracts the instantaneous
mean angle of the macrovibrissal array. Using data
from RW episodes in two species of rodent and one
marsupial, we have shown (figures 1 – 3) that the
change over time in this measure can be described
with reasonable accuracy using a two-component
Fourier series composed of a fairly invariant
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Active vibrissal sensing
bilateral asymmetry
in NMA (°)
bilateral asymmetry
in NMA (°)
bilateral asymmetry
in NMA (°)
(a)
(b)
40
20
0
−20
−40
40
20
0
−20
−40
40
20
0
−20
−40
−600 −300 0 300 600
angular head velocity (deg. m s–1)
Figure 4. Head-turning asymmetry. (a) Instantaneous bilateral asymmetry in NMA plotted against angular head
velocity for rat (top), mouse (middle) and opossum
(bottom). Solid lines show linear regression, dashed lines
indicate strength of relationship reported by Towal &
Hartmann [25]. A similar trend is observed in all species
(tendency to explore in the direction of head turning), but
is weaker than in the original study that employed a tactile
search paradigm. (b) Three frames from an episode of
HTA in rat showing the asymmetry in the whisking pattern
through a head-turn.
fundamental frequency (in rat and mouse) and its
second harmonic. For mouse data, this two-component series improved the accuracy of fit by 19 per
cent (median R2) compared with fitting a series
based on a single frequency; smaller improvements
in fit (4 and 10%, respectively) were found for whisking in rat and opossum, reflecting the simpler
characteristics of the recorded motions.
Mouse whisking has been described as occurring
at high frequencies with a mean of around 20 Hz
[14,15]; however, whisking at lower frequencies
around or below 10 Hz has also been reported
[42– 44]. Whisking in rat has been described as falling
into two different frequency bands by Berg & Kleinfeld
[7] and characterized as ‘exploratory’ (range 5– 15 Hz)
and ‘foveal’ whisking (15 – 25 Hz), the latter reported
as occurring specifically when animals were trained
to crane across a gap to investigate a food tube. At
the same time, rodent whisking patterns are often
reported to be highly variable [6,22,28,45]. One
form of variability is where multiple (typically two)
peaks are observed to occur within a single forward–
backward sweep; these ‘double pumps’ have been
described in both hamsters [6] and rats [45]. A specific
Phil. Trans. R. Soc. B (2011)
B. Mitchinson et al.
3045
pattern that we have observed in mouse whisking data
(figure 3, traces 4 and 5) and that has also been
described for hamster [6], is an alternating sequence
of larger and smaller pumps. Traces of this type of secondary oscillation can also be seen in other published
mouse whisking profiles (see fig. 3 of [15]) suggesting
that this is not an artefact of our behavioural task or of
our tracking algorithm.
When we modelled the mouse whisker angle series
using a single component model (F1), the distribution
of frequency of the motion was strongly bimodal (see
the electronic supplementary material for results),
with the upper peak at about twice the frequency of
the lower peak, a location consistent with our
interpretation of the high-frequency data as second
harmonics. However, when mouse whisking was modelled using a two component model (F2), we identified
a continuum of profiles that moves through the amplitude-phase space of the second harmonic. Smooth,
almost sinusoidal, whisking lies at one extreme (primary frequency dominant) and whisking that appears
to be at double-frequency at the other (second harmonic dominant). In between, the alternating sequences of
larger and smaller pumps in figure 3 are captured as a
Fourier series consisting of synchronized oscillations
of two harmonics with a primary:secondary amplitude
ratio of around 3 : 2. Other points in the space generate
similarly rich kinematic patterns.
Given that the two-component modelling approach
provides a mechanism for the generation of whisking
at the fundamental frequency, at twice that frequency,
and in various mixed profile patterns consistent with
observed data, it seems parsimonious to posit that
modes with different underlying frequencies are not
present in our mouse data. Indeed, the success of
the F2 model suggests to us that in both mouse and
rat distinct frequency ‘modes’ and different types of
movement profile could be described parsimoniously
as having the same origins. Thus, the ‘underlying’
whisking frequency may remain relatively invariant
(in a band of a few hertz) in both species, with
examples of higher-frequency motion being reinterpreted as owing to a strong second harmonic, rather
than a change in the fundamental frequency. On the
basis of this interpretation, it would be interesting,
for example, to investigate whether rat foveal whisking
shows any evidence of an underlying fundamental frequency in the exploratory whisking range. Data from
Carvell & Simons [22], in a similar task where the
rat is reaching across a gap to investigate a texture,
show significant power at the second harmonic above
a primary frequency of 8 Hz (compare fig. 7a from
[22] with our supplementary figure A9) consistent
with the possibility of a two-component whisking
pattern in rats. Complex movement profiles, such as
double pumps, may also be explicable as arising
from blends of fundamental frequency and second
harmonic at specific phase offsets.
We have so far not observed high-frequency whisking, or whisking with a large second harmonic
component, in opossum (the apparently broad range
of whisking frequencies expressed in opossum might,
in any case, make whisking in different ‘bands’ difficult
or impossible to distinguish). In this context, and in
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3046
B. Mitchinson et al.
(b)
rostro−caudal position (mm)
(a)
Active vibrissal sensing
(i)
ipsi.
cont.
(ii)
ipsi.
cont.
(iii)
40
40
40
20
20
20
0
0
0
−20
−20
−20
−40
−40
−40 −20 0 0 −20 −40
medio−lateral
object position (mm)
ipsi.
cont.
−40
−40 −20 0 0 −20 −40
medio−lateral
object position (mm)
−40 −20 0 0 −20 −40
medio−lateral
object position (mm)
Figure 5. Contact-induced asymmetry. (a) One frame from an episode of CIA in rat showing the asymmetry in the whisking
pattern in the presence of an obstruction. (b) For each species ((i) rat, (ii) mouse and (iii) opossum) there are two grids. The
left-hand grid shows results for the side nearest (ipsilateral) to the object, the right-hand grid shows movement on the opposite
(contralateral) side. The colour of each cell indicates average relative set-point for the ipsilateral/contralateral whisker array for an
ipsilateral object in the indicated 8 mm8 mm region relative to the tip of the snout which is at [0,0]. Red indicates that on
average the whiskers are less protracted than in RW for an obstacle in that location, blue that the whiskers are more protracted,
and white that the set-point is similar to average values. Darker shades indicate limited (n , 10) data points for that cell with
black indicating no data. Colours are fully saturated for relative set-point of +208. Note that for each grid decreasing values
along the x-axis always denote object positions further away from the snout on the ipsilateral side. Plots for all species show
reduced ipsilateral protraction (lower set-point) and increased contralateral protraction (higher set-point), consistent with
previous results in rat alone [16].
order to explore whether the second harmonic component is a later development in evolutionary terms,
it would be useful to investigate opossum whisking
behaviour in similar circumstances to those that elicit
foveal whisking in the rat.
As a descriptive tool, the two-component Fourier
series allows a good characterization of the visibly
rich patterns of whisking seen in different species
using a model with only a small number of parameters.
As such it provides an alternative to the ‘whisk cycle’
as a descriptive element with which to characterize
vibrissal behaviour, and which has proved to be problematic for the analysis of the many whisking profiles
in which the ‘boundaries’ between whisk events are
hard to discern. One of the benefits of such a description may be to assist efforts to identify the pattern
generator mechanisms underlying periodic vibrissal
motion. For instance, in mice this analysis might
prompt us to look for component systems that oscillate
in the lower frequency band and that are then modulated to form drive signals that accentuate the second
harmonic.
We noted no differences between the behaviour of
our RCS and Hooded Lister animals; furthermore,
no evidence of differences in quantitative kinematic
metrics between rat strains has so far been reported
in the wider literature [7,9,22]. Nonetheless, we note
the possibility that both quantitative and qualitative
metrics, including those reported here, may vary
with animal strain.
(b) Whisking as a form of active touch
This theme issue presents the case that active sensing
is not simply about movement of the sensor, but
about control of the sensor in a manner that will
boost task-relevant information. Although further evidence needs to be gathered, a picture is beginning to
Phil. Trans. R. Soc. B (2011)
emerge about the nature of active sensing control in
whisking animals.
A fundamental question is why animals whisk.
Though the circumstances in which whisking occurs
are in need of further characterization, it is possible
to say the following.
Moving the whiskers allows more degrees of freedom
for sensor positioning, the possibility of sampling a larger
volume of space with a given density of whiskers, and the
ability to control the velocity with which the whiskers
contact the surface. Periodic whisker movements allow
control of the frequency of contacts and the possibility
of many distinct contacts per second. Whisking animals
appear to be able to exert significant control over the
area of space selected for exploration by the whiskers,
making it wider or narrower (control of amplitude and
spread), more anterior or more posterior (control of
set-point), dependent on context. Thus, when whisking
to locate objects in free space animals make large amplitude sweeps, when whisking across a gap they shift
the set-point of the whisk forwards, when turning they
bias exploration in the direction of movement, and
when they contact an object unilaterally, the whiskers
on the contralateral side sweep round to gather more
information about the detected object.
Not all animals with prominent whiskers show
periodic whisker motion. The benefits of whisking are
probably enhanced by the need to operate in low or
zero light while negotiating complex terrain; hence the
apparent importance of whiskers and whisking in many
species of nocturnal climbing animals. The benefits
appear to be reduced, though not entirely eliminated
(witness the coypu), in larger animals whose heads are
more distant from the ground. Periodic motion of the
whiskers does not appear to be critical in the final
stages of prey capture. It is notable that whisker movement emerges alongside forward ambulation [27]. This
reinforces the view that whisking is fundamentally a
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Active vibrissal sensing
strategy for exploring nearby space, identifying properties of immediate relevance to the animal, such as the
presence of surfaces that can support locomotion, and
selecting locations that warrant further investigation by
orienting the multi-sensory zone surrounding the tip of
the snout.
(c) The evolution of active vibrissal touch
Based on a comparative analysis of mammalian facial
musculature, Huber [3] proposed that the evolution
of mobile vibrissae shaped not only the evolution of
the face muscles, but also the organization of the trigeminal complex, and played an influential role in
the early evolution of cortex. The data presented in
the current paper lend support to this view. In particular, it seems unlikely—given the evidence of periodic
whisker motion in a diverse range of species including
rodents, Afrotheria and marsupials—that whisking
emerged late on in evolution in a convergent fashion
across multiple animal classes. Rather, the principle
of parsimony would suggest that this was a primary
mode of interaction with the world for an early
common ancestor of therian mammals. If this
common ancestor whisked, it seems likely that it also
actively controlled its whisking movements in the
fashion described above as common to rat, mouse
and opossum, biasing exploration in the direction of
travel and towards surfaces of interest. The vibrissal
system of murid rodents is likely to be more sophisticated than that of opossums and the manner in
which it is so may well be due to the role of motor
cortex and of the corpus callosum, both of which
have large whisker representations and are absent in
the opossum. Interestingly though, our observations
of opossum whisking suggest that neither structure is
critical to the communication of information between
the two halves of the brain that support CIA in bilateral whisking. That is, the commissural connections
at the thalamic or brainstem level of the marsupial
brain appear to be sufficient for the whiskers on one
side of the snout to know something of what those
on the other side are sensing and respond accordingly.
Further behavioural, anatomical and neurophysiological investigations of the marsupial whisker system
should cast valuable light on how our early mammalian
ancestors used their vibrissae to explore the world, and
how this activity shaped and influenced the evolution
of mammalian brains and bodies. What we might
already say, however, is that alongside thermoregulation, the birth of live young and the expansion of
cortex, the emergence of active vibrissal touch was a
further critical milestone along the evolutionary path
to modern therian mammals.
The authors are grateful to Antonello Mallamachi and
Marco Stebel for providing access to the opossum colony
at the University of Trieste animal facility, to Hazel Ryan
and the Wildwood Trust, Canterbury, UK for allowing
access to various native UK rodent species and the coypu,
and to Washington zoo for allowing filming of the coendu
and tenrec. We would like to thank members of the Active
Touch Laboratory at Sheffield University for their advice
and help, particularly Charles Fox, for assisting in the
development of analysis methods, and Mathew Evans and
Stuart Wilson for help in collecting comparative data.
Phil. Trans. R. Soc. B (2011)
B. Mitchinson et al.
3047
Video analysis was performed using the BIOTACT
Whisker Tracking Tool which was jointly created by the
International School of Advanced Studies in Trieste, the
University of Sheffield and the Weizmann Institute in
Rehovot under the auspices of the FP7 BIOTACT project
(ICT 215910), which also funded the study. We are
particularly grateful for the contribution of Goren Gordon
to programming parts of the tracking tool. Kendra Arkley
was supported by an EPSRC doctoral training award.
REFERENCES
1 Vincent, S. B. 1912 The function of the vibrissae in the
behaviour of the white rat. Behav. Monogr. 1, 1 –82.
2 Pocock, R. I. 1914 On the facial vibrissae of mammalia.
Proc. Zool. Soc. Lond. 84, 889– 912. (doi:1111/j.14697998.1914.tb07067.x)
3 Huber, E. 1930 Evolution of the facial musculature and
cutaneous field of the trigeminus. 1. Q. Rev. Biol. 5,
133 –188. (doi:10.1086/394355)
4 Ahl, A. S. 1986 The role of vibrissae in behavior—a
status review. Vet. Res. Commun. 10, 245– 268. (doi:10.
1007/BF02213989)
5 Welker, C. I. 1964 Analysis of sniffing in the albino
rat. Behaviour 22, 223– 244. (doi:10.1163/156853964X
00030)
6 Wineski, L. E. 1983 Movements of the cranial vibrissae in
the golden-hamster (Mesocricetus auratus). J. Zool. 200,
261–280. (doi:10.1111/j.1469-7998.1983.tb05788.x)
7 Berg, R. W. & Kleinfeld, D. 2003 Rhythmic whisking by
rat: retraction as well as protraction of the vibrissae is
under active muscular control. J. Neurophysiol. 89,
104 –117. (doi:10.1152/jn.00600.2002)
8 Haidarliu, S., Simony, E., Golomb, D. & Ahissar, E.
2010 Muscle architecture in the mystacial pad of the
rat. Anat. Rec. (Hoboken). 293, 1192 –1206.
9 Grant, R. A., Mitchinson, B., Fox, C. & Prescott, T. J.
2009 Active touch sensing in the rat: anticipatory and
regulatory control of whisker movements during surface
exploration. J. Neurophysiol. 101, 862–874. (doi:10.
1152/jn.90783.2008)
10 Zucker, E. & Welker, W. I. 1969 Coding of somatic
sensory input by vibrissae neurons in the rat’s trigeminal
ganglion. Brain Res. 12, 138 –156. (doi:10.1016/00068993(69)90061-4)
11 Bermejo, R., Friedman, W. & Zeigler, H. P. 2005 Topography of whisking II: interaction of whisker and pad.
Somatosens. Mot. Res. 22, 213 –220. (doi:10.1080/
08990220500262505)
12 Knutsen, P. M., Biess, A. & Ahissar, E. 2008 Vibrissal
kinematics in 3D: tight coupling of azimuth, elevation
and torsion across different whisking modes. Neuron 59,
35– 42. (doi:10.1016/j.neuron.2008.05.013)
13 Sachdev, R. N., Sato, T. & Ebner, F. F. 2002 Divergent
movement of adjacent whiskers. J. Neurophysiol. 87,
1440 –1448.
14 Jin, T. E., Witzemann, V. & Brecht, M. 2004 Fiber types
of the intrinsic whisker muscle and whisking behavior.
J. Neurosci. 24, 3386–3393. (doi:10.1523/JNEURO
SCI.5151-03.2004)
15 Voigts, J., Sakmann, B. & Celikel, T. 2008 Unsupervised
whisker tracking in unrestrained behaving animals.
J. Neurophysiol. 100, 504– 515. (doi:10.1152/jn.00012.
2008)
16 Mitchinson, B., Martin, C. J., Grant, R. A. & Prescott,
T. J. 2007 Feedback control in active sensing: rat exploratory whisking is modulated by environmental contact.
Proc. R. Soc. B 274, 1035–1041. (doi:10.1098/rspb.
2006.0347)
Downloaded from http://rstb.royalsocietypublishing.org/ on June 17, 2017
3048
B. Mitchinson et al.
Active vibrissal sensing
17 Pearson, M. J., Pipe, A. G., Melhuish, C., Mitchinson,
B. & Prescott, T. J. 2007 Whiskerbot: a robotic active
touch system modeled on the rat whisker sensory
system. Adapt. Behav. 15, 223 –240. (doi:10.1177/
1059712307082089)
18 Prescott, T. J., Pearson, M. J., Mitchinson, B., Sullivan,
J. C. W. & Pipe, A. G. 2009 Whisking with robots:
from rat vibrissae to biomimetic technology for active
touch. IEEE Robot. Autom. Mag. 16, 42– 50. (doi:10.
1109/MRA.2009.933624)
19 Pearson, M. J., Mitchinson, B., Sullivan, J. C., Pipe,
A. G. & Prescott, T. J. 2011 Biomimetic vibrissal sensing
for robots. Phil. Trans. R. Soc. B 366, 3085–3096.
(doi:10.1098/rstb.2011.0164)
20 Bermejo, R., Harvey, M., Gao, P. & Zeigler, H. P. 1996
Conditioned whisking in the rat. Somatosen. Mot. Res. 13,
225– 233. (doi:10.3109/08990229609052578)
21 Gao, P., Ploog, B. O. & Zeigler, H. P. 2003 Whisking as
a ‘voluntary’ response: operant control of whisking parameters and effects of whisker denervation. Somatosens.
Mot. Res. 20, 179–189. (doi:10.1080/0899022031000
1623031-411)
22 Carvell, G. E. & Simons, D. J. 1990 Biometric analyses
of vibrissal tactile discrimination in the rat. J. Neurosci.
10, 2638–2648.
23 Carvell, G. E. & Simons, D. J. 1995 Task- and subjectrelated differences in sensorimotor behavior during
active touch. Somatosens Mot. Res. 12, 1–9. (doi:10.
3109/08990229509063138)
24 Zuo, Y., Perkon, I. & Diamond, M. E. 2011 Whisking
and whisker kinematics during a texture classification
task. Phil. Trans. R. Soc. B 366, 3058–3069. (doi:10.
1098/rstb.2011.0161)
25 Towal, R. B. & Hartmann, M. J. 2006 Right-left asymmetries in the whisking behavior of rats anticipate head
movements. J. Neurosci. 26, 8838 –8846. (doi:10.1523/
JNEUROSCI.0581-06.2006)
26 Landers, M., Haidarliu, S. & Philip Zeigler, H. 2006
Development of rodent macrovibrissae: effects of neonatal whisker denervation and bilateral neonatal
enucleation. Somatosens. Mot. Res. 23, 11–17. (doi:10.
1080/08990220600700784)
27 Grant, R. A., Mitchinson, B. & Prescott, T. J. In press.
The development of whisker control on rats in relation
to locomotion. Dev. Psychobiol.
28 O’Connor, D. H., Clack, N. G., Huber, D., Komiyama,
T., Myers, E. W. & Svoboda, K. 2010 Vibrissa-based
object localization in head-fixed mice. J. Neurosci. 30,
1947–1967. (doi:10.1523/JNEUROSCI.3762-09.2010)
29 Tamatsu, Y., Tsukahara, K., Hotta, M. & Shimada, K.
2007 Vestiges of vibrissal capsular muscles exist in the
human upper lip. Clin. Anat. 20, 628–631. (doi:10.
1002/ca.20497)
30 Carleton, M. D. & Musser, G. G. 2005 Order Rodentia.
In Mammal species of the world: a taxonomic and geographic reference (eds D. E. Wilson & D. M. Reeder),
pp. 745 –752, 3rd edn. Baltimore, MD: Johns Hopkins
University Press.
31 Shillito, E. E. 1963 Exploratory behaviour in the shorttailed vole Microtus agrestis. Behaviour 21, 145 –154.
(doi:10.1163/156853963X00149)
Phil. Trans. R. Soc. B (2011)
32 Andrew, R. J. 1963 The origin and evolution of the calls
and facial expressions of the primates. Behaviour 20,
1– 109. (doi:10.1163/156853963X00220)
33 Anjum, F., Turni, H., Mulder, P. G., van der Burg, J. &
Brecht, M. 2006 Tactile guidance of prey capture in
Etruscan shrews. Proc. Natl Acad. Sci. USA 103,
16 544– 16 549. (doi:10.1073/pnas.0605573103)
34 Munz, M., Brecht, M. & Wolfe, J. 2010 Active touch
during shrew prey capture. Front. Behav. Neurosci. 5, 12.
35 Rice, F. L. 1995 Comparative aspects of barrel structure
and development. In Cerebral cortex, vol. 2: The barrel
cortex of rodents (eds E. G. Jones & I. T. Diamond).
New York, NY: Plenum Press.
36 Ji, Q., Luo, Z. X., Yuan, C. X., Wible, J. R., Zhang, J. P.
& Georgi, J. A. 2002 The earliest known eutherian
mammal. Nature 416, 816– 822. (doi:10.1038/416816a)
37 Wong, P. & Kaas, J. H. 2009 An architectonic study of
the neocortex of the short-tailed opossum (Monodelphis
domestica). Brain Behav. Evol. 73, 206 –228. (doi:10.
1159/000225381)
38 Frost, S. B., Milliken, G. W., Plautz, E. J., Masterton, R.
B. & Nudo, R. J. 2000 Somatosensory and motor representations in cerebral cortex of a primitive mammal
(Monodelphis domestica): a window into the early evolution of sensorimotor cortex. J. Comp. Neurol. 421,
29–51. (doi:10.1002/(SICI)1096-9861(20000522)421:
1,29::AID-CNE3.3.0.CO;2-9)
39 Karlen, S. J. & Krubitzer, L. 2007 The functional and
anatomical organization of marsupial neocortex: evidence for parallel evolution across mammals. Prog.
Neurobiol. 82, 122 –141. (doi:10.1016/j.pneurobio.2007.
03.003)
40 Alloway, K. D., Smith, J. B., Beauchemin, K. J. & Olson,
M. L. 2009 Bilateral projections from rat MI whisker
cortex to the neostriatum, thalamus, and claustrum: forebrain circuits for modulating whisking behavior. J. Comp.
Neurol. 515, 548–564. (doi:10.1002/cne.22073)
41 Perkon, I., Kosir, A., Itskov, P. M., Tasic, J. F. &
Diamond, M. E. 2011 Unsupervised quantification of
whisking and head movement in freely moving rodents.
J. Neurophysiol. 105, 1950– 1962. (doi:10.1152/jn.
00764.2010)
42 Woolsey, T. A., Durham, D., Harris, R., Simons, D. J. &
Valentino, K. 1981 Somatosensory development. In The
development of perception: psychobiological perspectives (eds
R. N. Aslin & D. B. Pisani), pp. 259–292. New York,
NY: Academic Press.
43 Kiryakova, S. et al. 2010 Recovery of whisking function
promoted by manual stimulation of the vibrissal muscles
after facial nerve injury requires insulin-like growth factor
1 (IGF-1). Exp. Neurol. 222, 226 –234. (doi:10.1016/j.
expneurol.2009.12.031)
44 Sohnchen, J. et al. 2010 Recovery of whisking function
after manual stimulation of denervated vibrissal muscles
requires brain-derived neurotrophic factor and its
receptor tyrosine kinase B. Neuroscience 170, 372–380.
(doi:10.1016/j.neuroscience.2010.06.053)
45 Towal, R. B. & Hartmann, M. J. 2008 Variability in velocity profiles during free air whisking behavior of
unrestrained rats. J. Neurophysiol. 100, 740–752.
(doi:10.1152/jn.01295.2007)