What is It Like to Be a Rat Rat Sensory Perception

Review

What is it like to be a rat? Rat sensory perception

and its implications for experimental design

and rat welfare

Charlotte C. Burn

Department of Clinical Veterinary Science, University of Bristol, Bristol BS40 5DU, UK

Accepted 21 February 2008

Available online 10 April 2008

Abstract

This review of rat sensory perception spans eight decades of work conducted across diverse research

fields. It covers rat vision, audition, olfaction, gustation, and somatosensation, and describes how rat

perception differs from and coincides with ours. As Nagel’s seminal work (1974) implies, we cannot truly

know what it is like to be a rat, but we can identify and acknowledge their perceptual biases. These primarily

nocturnal rodents are extremely sensitive to light, with artificial lighting frequently causing retinal

degeneration, and their vision extends into the ultraviolet. Their olfactory sensitivity and ultrasonic hearing

means they are influenced by environmental factors and conspecific signals that we cannot perceive. Rat and

human gustation are similar, being opportunistic omnivores, yet this sense becomes largely redundant in the

laboratory, where rodents typically consume a single homogenous diet. Rat somatosensation differs from

ours in their thigmotactic tendencies and highly sensitive, specialised vibrissae. Knowledge of species-

specific perceptual abilities can enhance experimental designs, target resources, and improve animal

welfare. Furthermore, the sensory environment has influences from neurone to behaviour, so it can not only

affect the senses directly, but also behaviour, health, physiology, and neurophysiology. Research shows that

environmental enrichment is necessary for normal visual, auditory, and somatosensory development.

Laboratory rats are not quite the simple, convenient models they are sometimes taken for; although very

adaptable, they are complex mammals existing in an environment they are not evolutionarily adapted for.

Here, many important implications of rat perception are highlighted, and suggestions are made for refining

experiments and housing.

# 2008 Elsevier B.V. All rights reserved.

Keywords: Animal welfare; Communication; Olfaction; Perception; Rats; Refinement; Vision

www.elsevier.com/locate/applanim

Available online at www.sciencedirect.com

Applied Animal Behaviour Science 112 (2008) 1–32

E-mail address: [email protected].

0168-1591/$ – see front matter # 2008 Elsevier B.V. All rights reserved.

doi:10.1016/j.applanim.2008.02.007

mailto:[email protected]

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Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

2. Vision. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

2.1. Sensitivity to light . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

2.2. Colour vision . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

2.2.1. Emitted light . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

2.2.2. Colour in the environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7

2.3. Periodicity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8

2.4. Acuity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8

3. Audition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

3.1. Audiogenic damage in the laboratory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

3.2. Vocalisations and communication . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

3.3. Perception of the human voice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

3.4. Sound recordings and playbacks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

3.5. Echolocation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

4. Olfaction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

4.1. Overview of rat olfactory communication . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

4.2. Scent and reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

4.3. Olfactory modulation of aggression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

4.4. Communication about experiences . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

4.5. Communication about food . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15

4.6. Scents in the laboratory. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15

5. Gustation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

5.1. Taste in the laboratory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17

5.2. Nutritional regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17

5.3. Refinement within the homecage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18

5.3.1. Nutritional content . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18

5.3.2. Flavour . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18

5.3.3. Physical presentation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19

5.4. Refinement of experiments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19

6. Somatosensation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20

6.1. Environmental enrichment and somatosensation . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

6.2. Vibrissae and the laboratory environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

7. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

8. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22

Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22

1. Introduction

The stimuli that an animal can perceive depend on the available sensory apparatus, while the

way stimuli are evaluated in terms of their biological relevance depends on the animal’s innate

biases, cognitive abilities and experiences. Perception is therefore a subjective distortion of

reality, differing between species and even between individuals within a species. Since rats and

mice, which have similar perceptual abilities to each other, constitute over 80% of all research

animals in the European Union (Commission of the European Communities, 2003), and they

have been bred for research since the late 1800s (Krinke, 2000; Whishaw and Kolb, 2005), much

C.C. Burn / Applied Animal Behaviour Science 112 (2008) 1–322

is known about their perceptual biases. However, the information is scattered through time and

across different research fields, so it is not easily available to researchers, rat caretakers, and other

rat specialists. The resulting lack of awareness can have serious implications, sometimes leading

to poorly designed experiments and harming rat welfare. This review brings current information

together, to help inform and refine rodent experiments and housing.

The review concentrates on the laboratory rat, Rattus norvegicus, since summaries of mouse

sensory perception are included within several other review papers (Sherwin, 2002; Olsson et al.,

2003; Latham and Mason, 2004). Much of the information will also be true for mice and other

rodents, but care should still be taken if extrapolating between species. The species’ natural

ecology – such as whether they are diurnal or nocturnal, social or solitary, arboreal, burrowing or

terrestrial – will profoundly affect their sensory perception. These ethological considerations are

highly relevant in laboratory rats despite their domestication; adult laboratory rats retain so many

of their wild instincts that, when released into a naturalistic habitat, their resulting community

and behaviour rapidly resembles that of their wild relatives (Berdoy, 2002).

This review is organised around the classic ‘five senses’: vision, audition, olfaction, gustation

and somatosensation. It should be remembered that these are actually not the only senses; indeed

rats may even possess a magnetic compass, like mice (Muheim et al., 2006) and hamsters

(Deutschlander et al., 2003), but most published information currently covers the aforementioned

five senses. For each sense, the rat’s sensory biases relative to humans are first described, then

some practical implications of its perception with respect to welfare and experimental design are

discussed. This is an applied review, focussing on the known or suspected implications of each

sense, and aiming to provide enough information to allow readers to extrapolate to their own

situations. The review cannot be completely comprehensive, and it will become clear that in

many cases, rat sensory perception is still poorly understood.

2. Vision

An obvious difference between human and rat vision is that rats’ eyes are located on the sides

of their heads, rather than the front. They therefore have a wider field of view, but less binocular

overlap than us: wild rats have a binocular overlap of 358, domestic rats 768, and humans 1058(Heffner and Heffner, 1992a).

Wild rats usually inhabit burrows or other enclosed environments, and tend to be nocturnal or

crepuscular, so most of their activities occur under low-light conditions (e.g. Calhoun, 1963).

Consequently, rats rely relatively little on vision, but they are dramatically more sensitive to dim

light than we are, able to discriminate tiny increments in intensity, indiscernible to us, including

discriminating ‘total darkness’ from 0.107 lx (Campbell and Messing, 1969).

Rats, especially albinos, have much poorer visual acuity (Lashley, 1938; Creel et al., 1970;

Prusky et al., 2002) and narrower depth perception than humans (O’Sullivan and Spear, 1964;

Routtenberg and Glickman, 1964). For example, human acuity can be around 30 cycles per

degree (c/d, a measure of spatial resolution accounting for stimulus size and distance), while

pigmented rats’ acuities are only 1–1.5 c/d and albino strains have even lower acuities of 0.5 c/d

(Prusky et al., 2002). This presumably gives an extremely blurred image by human standards

(Fig. 1, reprinted from Prusky et al., 2002). Poor acuity in rats is probably partly due to their eyes’

relatively small size, and partly because their eyes appear to have very limited abilities to focus

light from different distances or angles compared with human eyes (Artal et al., 1998). Rats often

bob their heads which may help them gain motion cues about the distance of objects (Legg and

Lambert, 1990).

C.C. Burn / Applied Animal Behaviour Science 112 (2008) 1–32 3

Experiments in the 1930s suggested that, contrary to popular belief, rats possess colour

vision (e.g. Munn and Collins, 1936; Walton and Bornemeier, 1938), which has recently been

confirmed through electroretinograms and quantitative behavioural tests (Jacobs et al., 2001).

Rod cells comprise 99% of rat photoreceptors, but rats also have two cone cell types (Szel and

Rohlich, 1992). Around 93% of the cones respond maximally to blue-green light (around

510 nm), while the remaining 7% respond to ultraviolet (UV) (around 360 nm) (Jacobs et al.,

2001; Akula et al., 2003). Cone responses are normally distributed, so rats actually perceive

hues ranging from ultraviolet (400 nm) to orange-red (around 635 nm) (Jacobs et al., 2001),

but they are most responsive to colours near their peak sensitivities (Jacobs et al., 2001; Akula

et al., 2003).

Flicker fusion thresholds (when emitted light flickers rapidly enough to appear constant) for

rats are not yet known, but are relevant for their perception of video images and artificial lighting

(D’Eath, 1998). Flicker fusion thresholds decrease with high light intensity, and increase with

fatigue. Animals with high proportions of rod cells, like rats, generally have high-flicker fusion

thresholds, so rats might perceive videos, computer monitors, and some fluorescent lighting as

flickering (Jarvis et al., 2003).

Discussion of the implications of rat vision is separated according to sensitivity to light

generally, colour vision, periodicity, and acuity.


Fig. 1. Visual perception of rat strains in visual-based behavioral tasks, reprinted from Prusky et al. (2002) (with

permission from Elsevier and the authors). The original image (top-left) has been blurred to model the perception of rats

with acuities of 1.5 c/d (top-right; Fisher–Norway), 1.0 c/d (bottom-left; Dark Agouti, Long-Evans, wild) and 0.5 c/d

(bottom-right; Fisher-344, Sprague–Dawley, Wistar) when the image subtends 108. This approximates the size of the

image if it were used as a visual cue in a typical visuo-behavioral task (see Prusky et al., 2002 for details).

2.1. Sensitivity to light

The sensitivity of rats to light (Campbell and Messing, 1969) means that light levels

comfortable for humans can rapidly cause retinal atrophy (reviewed in Schlingmann et al.,

1993a,b) and cataract formation in rats (Rao, 1991). Albinos are particularly susceptible because

they lack protective melanin in the iris and retinal epithelium, and the entire eyeball is slightly

transparent (Schlingmann et al., 1993b). Consequently, even when the iris contracts in bright

light, most of the light still enters the eye (Williams et al., 1985). In fact, albino rats may be the

most susceptible of all laboratory animals to light-induced retinal degeneration (Bellhorn, 1980).

To illustrate the relevant range of light intensities, the UK code of practice for the care and use

of laboratory animals suggests that ‘‘350–400 lx at bench level is adequate for routine

experimental and laboratory activities’’ (Home Office, 1989). Light intensities within cages are

commonly between about 150 and 550 lx (Schlingmann et al., 1993c), but are higher in

laboratory rooms, with upper limits approaching 10,000 lx due to current technological

limitations (e.g. Light Therapy ProductsTM, 2006; Outside In Ltd., 2006). Humans can tolerate

still higher intensities—outdoors on sunny days light often exceeds 50,000 lx, and only at this

order of magnitude are discomfort and potential retinal damage likely in humans.

Light intensities of only 65 lx can cause retinal degeneration in albino rats, even on a 12 h

light–dark cycle (Semple-Rowland and Dawson, 1987). Half the photoreceptors were

permanently damaged after just 3 days at 133 lx in albinos, but pigmented rats were less

susceptible, with equivalent damage occurring at 950 lx (Williams et al., 1985). Rod cells are

particularly vulnerable to light destruction, but cones often survive even after all rods have been

destroyed (Cicerone, 1976; La Vail, 1976). Long-term cyclical light intensities of about 500 lx

within an animal room can also cause cataracts in albino rats (Rao, 1991). These problems are

worst in rats housed closest to the light source, usually those highest in the rack (Rao, 1991; Perez

and Perentes, 1994).

Surprisingly, some vision can remain after constant long-term light exposure, even when no

intact photoreceptor cells can be observed (e.g. Lemmon and Anderson, 1979). This might be

conferred by a few remaining cones that may be so sparse that they were undetectable by the

quantitative techniques used (Cicerone, 1976; La Vail, 1976). Even so, under ‘ordinary’ laboratory

conditions, visual impairments can confound some tests. For example, in the Morris water maze – a

test of cognitive function – rats with incidental light-induced retinal damage perform as poorly as

rats with cognitive deficits, both groups displaying difficulties locating the platform (Osteen et al.,

1995; Lindner et al., 1997). Also, in commonly used ‘anxiety’ tests, such as open field tests and

light–dark boxes, visually impaired individuals might venture into the exposed/light areas more

than fully sighted ones, through their lesser ability to discriminate light from dark, but this requires

experimental confirmation. Therefore, light-induced retinopathy should be controlled for in such

tests, or non-visual tests used alongside the established visual ones.

Welfare problems might arise at even lower light levels than those causing retinal damage,

because of motivation to hide, as well as to avoid ocular discomfort (Schlingmann et al., 1993c).

Rats, especially albinos, reliably choose the lowest light intensities available, even when all the

choices are very dim, appearing indistinguishable to humans (Campbell and Messing, 1969;

Woodhouse and Greenfeld, 1985; Blom et al., 1995). Rats’ aversion to light was clearly

demonstrated in a study showing that sleeping pigmented and albino rats awoke and moved to

areas of lower illumination at thresholds of only 60 and 25 lx, respectively (Schlingmann et al.,

1993c). Consistent with such behaviour, chromodacryorrhoea, an aversion-related secretion from

the Harderian gland (e.g. Mason et al., 2004), increases with brighter light (Hugo et al., 1987).


There is clearly a conflict between human workers needing adequate light to inspect rats, for

example for signs of illness, and rats needing to avoid damaging or aversive light levels.

Schlingmann et al. (1993a) therefore stressed the importance of providing shelters within cages,

allowing rats some control over their light exposure. As described below, coloured shelters exist

that allow humans to see rodents, while it supposedly appears dark to the rodents inside the

shelter, although their efficacy requires confirmation.

Light levels affect commonly used psychological tests, such as elevated plus-mazes in which

exploration of the exposed arms is taken to indicate reduced anxiety; rats explore the exposed

arms more in dim than bright light (Cardenas et al., 2001; Garcia et al., 2005). Moreover, some

effects are only found under certain light conditions. For example, the anxiolytic effects of

gentling only show in brightly lit open fields (Hirsjarvi and Valiaho, 1995), and some drug effects

are influenced by plus-maze illumination (Clenet et al., 2006). Therefore, some control and

careful description of lighting conditions during these tests is necessary to account for its

influence on psychological measures.

Surgery presents a difficult situation because good lighting is essential for delicate operations,

but the anaesthetised, unblinking rat is unable to protect its eyes from that light. Care should

therefore be taken, not only to keep the eyes hydrated, but also to protect them from prolonged

bright light. Interestingly, the anaesthetic agent, halothane, prevents retinal degeneration (Keller

et al., 2001); other anaesthetics have not yet been investigated. This protection is afforded under

white, but not blue, light.

Despite the above evidence that bright light is harmful to rats, this aspect of their biology is not

always considered in some fields of research. An example is the use of rats as models for seasonal

affective disorder in humans, exploring whether bright light therapy (up to 11,500 lx for 2 weeks)

can cure depression in rats (e.g. Dilsaver and Majchrzak, 1988; Giroux et al., 1991; Humpel et al.,

1992; Overstreet et al., 1995). Unsurprisingly, the depression was not cured, and the one study that

considered the effects of light on rat vision discovered massive destruction of the albinos’

photoreceptors (Humpel et al., 1992). These examples illustrate how crucial knowledge of species-

specific perception is for generating reasonable hypotheses and preventing animal suffering.

2.2. Colour vision

Rats are not colour-blind (Muenzinger and Reynolds, 1936; Munn and Collins, 1936; Walton

and Bornemeier, 1938; Lemmon and Anderson, 1979; Jacobs et al., 2001). However, relative to

humans, they perform poorly when discriminating between colours of similar wavelengths

(Walton, 1933), and they take longer to learn colour discriminations than light intensity ones

(Jacobs et al., 2001).

To discuss the implications of rats’ colour sensitivity, the implications for emitted light and

that reflected by objects in the environment will be dealt with separately, as their effects are quite

distinct.

2.2.1. Emitted light

Standard artificial lighting rarely emits UV wavelengths (e.g. Bellhorn, 1980; Latham and

Mason, 2004), since human cones are insensitive to it. To date, no studies have apparently

investigated the effects of UV-deficient light on rats. In some birds, UV light is important for their

welfare (Moinard and Sherwin, 1999; Maddocks et al., 2001) and normal behaviour (Bennett and

Cuthill, 1994), but laboratory mice appear to have, if anything, a slight aversion to it (C.M.

Sherwin, personal communication). Also, high levels of UV can cause cataracts in mice (in


Bellhorn, 1980), and can affect reproductive and circadian rhythms in rats (reviewed in Brainard

et al., 1994). In fact, the colour composition of artificial light can have large effects. In rats, blue

light (around 490 nm) caused more retinal degeneration (reviewed in Schlingmann et al., 1993b),

and also more disruption to fertility (Tong and Goh, 2000) than any other wavelengths tested; UV

light was not included in these studies, but is of a shorter wavelength than blue light so may be

more harmful.

At the opposite end of the spectrum, dim red light is sometimes used to observe nocturnal

behaviour in rats, because it is on the upper edge of the wavelengths visible as colour to them

(Jacobs et al., 2001). However, rats’ rod cells are stimulated by similar wavelengths to human rod

cells, including red light (Akula et al., 2003). This means that, provided some rod cells remain

intact, rats can see red light, even if only as light and dark contrast. This may not be a problem in

experiments if rats are habituated to it, since moonlight would provide illumination in the wild.

As an alternative to red light, sodium lamps, which emit very narrow peaks of yellow-orange (589

and 589.6 nm) light, can be used (McLennan and Taylor-Jeffs, 2004). Not only is it more visible

to humans than red light, but also there were no significant long-term differences between the

activity levels of mice when illuminated by this lamp or in darkness. However, in studies

unequivocally requiring rats to behave as if in pitch darkness, infrared light and the necessary

viewing equipment should be used.

It is also worth noting that most video equipment and computer monitors, which create images

using emitted light, include no UV emissions and the colour balance is optimised for human

vision (D’Eath, 1998). Even in black-and-white images and light from white artificial light bulbs,

‘white’ is composed of red, green and blue light adjusted for humans, and so would not appear as

white to rats. Therefore, any such images presented to species with different colour sensitivities,

particularly UV-sensitive animals, could lack important information.

2.2.2. Colour in the environment

Caution is required when presenting images to rats in discrimination tests, even if the cues

reflect rather than emit light. Different inks have different spectral properties that may be

invisible to the human eye, and some might even reflect UV. Moreover, different pigments might

differ in their olfactory qualities, which could be more salient to rats than their visual qualities.

Even if this does not harm the experimental purpose, it can make standardisation between

experiments difficult.

Outside experimental situations, there are also some relevant implications of rodent colour

vision within the homecage. In recent years, manufacturers of rodent environmental enrichments

have produced transparent shelters in various colours (e.g. Robbins, 2004; Datesand Ltd., 2005).

The idea behind them is that, while rodents – supposedly blind to the shelter’s colour – perceive

themselves as being sheltered in a dark environment, human carers can inspect them without

disturbing them. However, these shelters seem not to have been independently evaluated for their

efficacy. Red transparent material might make a suitable shelter, being the least visible colour to

rats (Jacobs et al., 2001), but as explained earlier, it would still stimulate rod cells and possibly

some cones.

The colour of the homecage itself might also affect rats. Sherwin and Glen (2003) housed mice in

different coloured cages and found that they had significantly different preferences for cage-

colours. Moreover, the colour affected their food-to-body mass conversion rates and their elevated

plus-maze anxiety. Assuming these effects were due to the colours directly (rather than the scents,

tastes, or textures of the dyes used), this study shows that environmental colour can have

surprisingly strong effects on mouse behaviour and physiology, and so possibly that of rats too.


2.3. Periodicity

Rats tend to be most active at dusk and dawn, although their circadian rhythms are relatively

flexible (e.g. Calhoun, 1963). Because we are diurnal, many rodent experiments are carried out in

the light, so much of our knowledge of this species comes from individuals awakened during their

resting period, and tested under much brighter conditions than they would voluntarily

experience. The implications of this can be profound, but time-shifted experiments are still rare

in some fields. The brain state changes radically between sleep and activity, with whole

populations of neurons shifting between activity and inactivity (Hobson, 2005; Saper et al.,

2005). The time of testing can strongly influence the variables of interest in experiments. For

example, during the light phase, rats’ cardiovascular responses to various stressors are more

pronounced (Schnecko et al., 1998), and they show less exploratory behaviour in an elevated

plus-maze than in the dark phase (Andrade et al., 2003).

For most experiments, rats will be in a wakeful state provided they have sufficient time to

awaken, but little published information is available on how long rodents require to fully awaken

(i.e. be in the same state as during the active phase). Any conclusions drawn from light phase

studies of rats as human models could suffer from interpretive problems, because it is unclear

whether the observed state would reflect a similar state in our light (active) phase or our (dark)

resting phase.

Time-shifted experiments and husbandry can be made possible by using red or sodium

illumination as described above, and also by feeding rats only during the phase when we wish

them to be active (cited in Saper et al., 2005); a situation that sometimes occurs in the wild

(Calhoun, 1963).

2.4. Acuity

As described above, rats have very poor acuity (Fig. 1). Their image resolution is at least 20

times poorer than ours (Artal et al., 1998). Note though that the studies investigating rat visual

acuity (Lashley, 1938; Creel et al., 1970; Artal et al., 1998; Robinson et al., 2001; Prusky et al.,

2002) have used laboratory rats, whose acuity might have been further reduced by their

artificially lit environments.

Apart from the damaging effects of light itself, several other factors can affect rat vision,

including the early environment. Complete lack of light impairs rats’ visual development

(Fagiolini et al., 1994), but providing environmental enrichment to these dark-reared animals can

eliminate this effect (Bartoletti et al., 2004). In mice, enriched environments during rearing

accelerate visual development and improve adult acuity (Prusky et al., 2000; Cancedda et al.,

2004).

Also, diet has a large influence on vision (Berson, 2000). For example, caloric restriction can

prevent cataracts (e.g. Wolf et al., 2000), and antioxidant intake and consumption of certain

vitamins can prevent retinal damage (Li et al., 1985; Berson, 2000). Dietary composition is

discussed in more detail in Section 5.

The research implications of rats’ poor visual acuity depends on the experiment in question,

but if visual cues are used they should be relatively large and high contrast, but not too bright as to

be aversive. Also, visual cues may not be as salient to rats as cues in other modalities. Few

experiments have tested this directly, but rats do remember auditory associations for longer than

equivalent visual ones (Wallace et al., 1980), and can more rapidly learn discriminations using

multimodal stimuli (floor surfaces differing in appearance, smell, and texture: Dymond, 1995;


Dymond et al., 1996) or olfactory or tactile cues (Birrell and Brown, 2000). However, vision is

often the most appropriate sense for guiding rats in water mazes (Prusky and Douglas, 2005), for

comparison with past studies, and for certain models of human activities.

3. Audition

Sound can be described in terms including its frequency, intensity, timbre (frequency

spectrum) and envelope (shape of sound pressure through time). While young humans hear

frequencies from about 0.02 to 20 kHz (Moore, 2003), hearing in rats is shifted upwards to

include the ultrasonic range (Kelly and Masterton, 1977). The lowest frequency rats have been

reported to hear is 0.25 kHz and the highest is 80 kHz (Kelly and Masterton, 1977; Heffner and

Heffner, 1992b; Heffner et al., 1994). They can also detect lower sound frequencies (Petounis

et al., 1977), probably through contact with vibrating surfaces, and can even perceive low-

frequency sounds using their vibrissae (Neimark et al., 2003) (see Section 6).

Auditory sensitivity decreases near the extremes of the detectable frequencies, so sounds at

the lower and higher extremes must be louder before rats can detect them. The rat’s peak

sensitivity is estimated to lie between about 8 and 50 kHz (Kelly and Masterton, 1977; Heffner

and Heffner, 1992b), although estimates vary, probably due to factors including strain, age, and

background noise. Even whether the homecages of rats are barren or environmentally enriched

can greatly affect hearing sensitivity; auditory neurone performance is vastly improved by

environmental enrichment (Engineer et al., 2004).

The implications of rat auditory perception include what sound characteristics are harmful,

vocal communication between rats, perception of the human voice, and experimental use of

sound cues. There has also been debate about whether rats can echolocate.

3.1. Audiogenic damage in the laboratory

Interactions between sound intensity and frequency (Fleshler, 1965; Voipio et al., 1998; Bjork

et al., 2000) make it difficult to determine detection- and safety-thresholds for sound intensities.

The decibel (dB) scale is logarithmic, so even small numerical increases represent large increases

in the actual intensity. European Union legislation (2003) states that advice and hearing-

protection must be provided for human workers frequently exposed to sounds of 80 dB or more.

Above about 150 dB, auditory damage is inevitable with most perceivable sounds (Gamble,

1982). Equivalent thresholds are unknown for rats, but young rats are more sensitive to sounds

than older ones, and permanent audiogenic damage is most likely in pups between about 12 and

22 days of age (Voipio, 1997).

In the laboratory, audible sounds as loud as 80–90 dB have been recorded; 50–75 dB for

ultrasound (Milligan et al., 1993), so conceivably, audiogenic damage could occur in both

humans and rats. Husbandry procedures cause the loudest sounds, especially if metallic

equipment is involved or if the work is performed in a hurried manner (Gamble and Clough,

1976; Milligan et al., 1993; Sales et al., 1999; Voipio et al., 2006). Filling metal food hoppers

made 80–90 dB of (mostly ultrasonic) sound, which would occur about once a week for the rats’

lifetimes (Sales et al., 1999; Voipio et al., 2006). This was measured from a distance of 50 cm,

approximately the furthest that a caged rat could get from the sound.

Many apparently silent activities or devices actually produce high levels of ultrasound (Sales

et al., 1988, 1999). Examples include computer monitors, making 68–84 dB of broadband

ultrasound (Sales et al., 1988), and some fluorescent lighting (G.J. Mason personal


communication and personal observation). Cage washers, hoses, running taps, squeaky chairs,

and rotating glass stoppers (Sales et al., 1988) produce both ultrasound and audible sound, as do

some air-flow hoods worn to prevent allergy in human workers (Picciotto et al., 1999). Similarly,

standard fire alarms produce loud high- and low-frequency sounds, which laboratory animals

cannot escape, so laboratories can be fitted with fire alarms that only emit sound audible to

humans but not rodents (Home Office, 1989); although note that even frequencies below rats’

audible range can affect them (Petounis et al., 1977).

Whether common laboratory sounds affect rodent welfare has not been investigated directly,

but loud noises generally can trigger seizures, reduce fertility, and cause diverse metabolic

changes (Sales et al., 1988; Milligan et al., 1993). Repeated short bursts of 2 kHz sound at 120 dB

caused ‘behavioural despair’ in rats (Bulduk and Canbeyli, 2004). Longer lasting sounds can also

affect animals, although that has apparently not been tested in rats. In pigs, 90 dB prolonged or

intermittent broadband noise increased cortisol, ACTH, noradrenaline:adrenaline ratios and time

lying down, and decreased growth and social interactions (Otten et al., 2004). Conceivably then,

a fluorescent light emitting loud ultrasound could cause significant stress in rats housed near it.

The envelopes and timbres of sounds also determine how aversive or damaging they are.

Noise-type sounds, e.g. white noise or the sound of tearing paper, cause stronger fear reactions in

rats than equivalent harmonic or pure tones, or audible rat vocalisations (Voipio, 1997). Sudden

sounds are probably also more startling than those with gradual onsets. It should be noted that

avoidance of sound occurs at still lower thresholds than those causing startle reactions (in

Fleshler, 1965), or physical damage.

Ultrasound detectors (e.g. bat detectors), which represent ultrasounds in a form that humans

can hear or visualise, would be useful as standard pieces of laboratory equipment to regularly

check whether ultrasound of certain frequencies is being emitted in the animal rooms and to test

experimental setups. Few experimenters would choose to carry out experiments during loud

building work, for example, because of potential effects on the animals’ performances, and the

same meticulousness should apply to ultrasound. Indeed, background noise levels during

behavioural experiments do affect the apparent learning abilities of rats, with louder white noise

leading to faster completion of a maze task (Prior, 2006). Moreover, even loud infrasound affects

rat behaviour, reducing their activity and triggering sleep (Petounis et al., 1977).

3.2. Vocalisations and communication

As well as audible ‘squeaks’, rats produce at least three types of ultrasonic vocalisations. First,

juvenile rats produce a 40–50 kHz vocalisation (Noirot, 1968), which together with olfactory

cues, causes pup retrieval by the mother (e.g. Allin and Banks, 1972; Farrell and Alberts, 2002).

The second ultrasonic vocalisation is the ‘22 kHz long-call’, which occurs mainly in aversive

situations and might therefore indicate negative affect (Knutson et al., 2002). Examples of such

situations include social defeat (Van der Poel and Miczek, 1991), exposure to cat odour

(Blanchard et al., 1991), administration of naloxone or lithium chloride (Burgdorf et al., 2001),

arthritic pain without analgesia (Calvino et al., 1996), acute pain (Jourdan et al., 1995), acoustic

startle (Kaltwasser, 1990) and electric shocks (Kaltwasser, 1991). However, male rats make a

similar vocalisation after ejaculation (Van der Poel and Miczek, 1991), so this call might occur in

two subtly different forms, or might not reliably indicate negative affect.

The third ultrasonic vocalisation is the ‘50 kHz chirp’, which is apparently associated with

positive events (Knutson et al., 2002), and has even been suggested as a form of laughter

(Panksepp and Burgdorf, 2000). It occurs in anticipation of positive social contact (Knutson et al.,


1998; Brudzynski and Pniak, 2002), rewarding ‘tickling’ by humans (Panksepp and Burgdorf,

2000; Burgdorf and Panksepp, 2001; Panksepp, 2006), amphetamine or morphine administration

(Knutson et al., 1999), and feeding or rewarding electrical stimulation of the brain (Burgdorf

et al., 2000), and also during play (Knutson et al., 1998; Brudzynski and Pniak, 2002; Burn,

2006). However, again, this vocalisation does not reliably indicate positive affect because it

occurs in some aversive situations, e.g. during morphine withdrawal (Vivian and Miczek, 1991),

aggression (Sales, 1972), and in certain painful situations (Hawkins et al., 2005).

Surprisingly little work has investigated the audible squeak. There may in fact be several

different types of squeak, because subjectively there is variation in the quality of sounds

produced (O.H.P. Burman, personal communication; personal observation). Pups and their

mothers make audible squeaks in the nest (e.g. Voipio, 1997), but this may be different from

squeaking in other contexts. Squeaks occur during nociception but they persist even when central

nervous system analgesics are given, which might suggest that they are detached from the

emotional experience of pain (Jourdan et al., 1995). They also occur during playing and fighting

(Voipio, 1997; Burn et al., 2006a), and sometimes during handling, especially alongside

struggling behaviour (van Driel et al., 2004; Burn, 2006). They generally seem to indicate

negative affect, but do not necessarily occur alongside the 22 kHz long-call, so there must be

some qualitative or quantitative difference between the motivations behind the two call types.

All of these vocalisations could have practical implications. Procedures or environments that

cause rats to vocalise could affect the behaviour and physiology of all neighbouring rats within

audible range. For example, playbacks of 22 kHz long-calls caused freezing and decreased

activity (Sales, 1991; Brudzynski and Chiu, 1995) and increased latencies to emerge into an arena

(Burman et al., 2007). Playbacks of audible squeaks also caused conspecifics to orientate towards

the speaker and occasionally to squeak themselves (Voipio, 1997).

3.3. Perception of the human voice

An awareness that rats can hear our voices is important, because of affects on experimental

results and rat welfare. Rats can hear and discriminate many elements of the humanvoice (e.g. Pons,

2006), and pet rats can learn to respond to verbal commands (e.g. Fox, 1997). In fact, rats can

distinguish between some languages (Toro et al., 2003), so the pitches, rhythms and accents of

different human workers could be at least partly responsible for rats being able to distinguish

between individual humans (McCall et al., 1969; Morlock et al., 1971; Davis et al., 1997; van Driel

and Talling, 2005). Shouting causes stress responses in farm animals (Hemsworth, 2003), so this

may also be true for laboratory rats, especially because when humans speak with more emotional

content, the higher pitched and ultrasonic content of our speech increases (Mason, 1969).

3.4. Sound recordings and playbacks

By default, most standard recording devices and speakers include no ultrasound, so specialised

equipment is necessary, such as ‘tweeter’ speakers and ultrasonic microphones (Bjork et al., 2000).

White noise, although aversive to rats (Voipio, 1997), is commonly used to standardise background

noise in experiments, but different speakers differ in their ultrasonic output, so comparisons across

studies might sometimes be invalid. Even a study that specifically investigated how background

noise affected rat behaviour in a maze, neither mentioned their ultrasonic hearing abilities, nor used

specialist equipment to produce the experimental white noise (Prior, 2006), indicating that

awareness of these auditory issues may be lacking in some fields.


3.5. Echolocation

There has been some debate about whether rats can echolocate (e.g. Rosenzweig et al., 1955;

Riley and Rosenzweig, 1957; Kaltwasser and Schnitzler, 1981; Forsman and Malmquist, 1988).

Blind rats can use self-generated sounds, reflected off solid objects, to guide them in mazes

(Rosenzweig et al., 1955; Riley and Rosenzweig, 1957). Also, sighted rats in darkness can

discriminate between shelves close enough to jump to and those too far away, but not if they are

deafened (Chase, 1980). Some studies described quiet ultrasonic ‘clicks’ (Chase, 1980; Graver

et al., 2004), which were produced more in darkness than in light, more before rats jumped to the

platform than after, and the decision to jump was faster in rats that clicked more (Graver et al.,

2004). However, rats seem not to have anything like the specialised echolocation abilities of

mammals such as bats or cetaceans. Indeed, some blind and blindfolded humans can ‘echolocate’

using reflected sound, similar to rats (in Riley and Rosenzweig, 1957), but there is no evidence

that either species can use sound to build up a detailed picture of their environment, as bats or

cetaceans can.

4. Olfaction

Rats rely heavily on olfaction (e.g. Doty, 1986). They can quickly associate olfactory cues

with food rewards (Le Magnen, 1999a; Birrell and Brown, 2000), with this ability even making

them a suitable alternative to ‘sniffer’ dogs for locating contraband substances (Otto et al., 2002).

Rats can locate the direction of odorants, without moving their heads, three orders of magnitude

more quickly than we can (Rajan et al., 2006). It is sometimes stated that albinism dampens

olfaction, because albinos show weaker avoidance of garlic than pigmented rats do (Keeler,

1942), but of course they might simply be less averse to the scent.

Humans are unusual mammals because a much smaller proportion of our genome is devoted to

olfaction, than other species (Gilad et al., 2003; Emes et al., 2004; Rat Genome Sequencing

Project Consortium, 2004; Quignon et al., 2005), and our vomeronasal organ is vestigial or non-

existent (e.g. Brennan and Keverne, 2004). In contrast, rats not only possess main olfactory

epithelia, but also well-developed vomeronasal organs. Although the two systems overlap

(reviewed in Shepherd, 2006), the vomeronasal organ seems specialised for instinctive

recognition of pheromones and evolutionarily relevant compounds (Dulac, 1997; Holy et al.,

2000; Brennan and Keverne, 2004), while the olfactory epithelium is specialised for learned

associations between volatile scents and their implications (Dulac, 1997). The vomeronasal

system detects relatively non-volatile compounds, requiring the rat to lick or imbibe some

compounds before it can detect them (Brennan and Keverne, 2004). Here ‘olfaction’ includes

both systems, because in most cases the specific odorant or detection mechanism is currently

unknown. The focus is on olfactory communication, but some significant scents within

laboratory environments are also discussed.

4.1. Overview of rat olfactory communication

Rat olfactory communication is well developed, yet remains little understood by humans.

Much communication is mediated through urine, but rats have many scent glands, including the

sebaceous, preputial, clitoral, perineal, salivary, anal, plantar, and Harderian glands. Through

scent, rats can gain information about each others’ gender (Alberts and Galef, 1973; Moore,

1985; Brown, 1992; Garcia-Brull et al., 1993), reproductive state (Gawienowski et al., 1975;


Manzo et al., 2002; Zala et al., 2004), genetic relatedness (Wills, 1983; Hurst et al., 2005),

dominance (Krames et al., 1969), health status (Zala et al., 2004), and individual identity (Hopp

et al., 1985; Gheusi et al., 1997). Rats also recognise familiar conspecifics using olfaction

(Burman and Mendl, 2003), not through a shared ‘colony scent’, but through remembering

individual odours (Alberts and Galef, 1973; Carr et al., 1976). These odours can be determined

genetically or be acquired from the environment (Schellinck et al., 1991; Schellinck and Brown,

2000; Hurst et al., 2005).

Laboratory rats may not be completely isolated from conspecifics even when individually

housed, because scents from neighbouring cages, or experimental apparatus and instruments can

influence them (unless they are in individually ventilated cages). These scents can profoundly

affect rats, as described below, although it should be mentioned that isolation itself also affects

these social animals (e.g. Day et al., 1982; Hurst et al., 1997; Sharp et al., 2002; Westenbroek

et al., 2005).

4.2. Scent and reproduction

Much sexual behaviour in rodents is olfactorily mediated. The ‘Bruce effect’, whereby female

mice abort their offspring upon encountering the volatile scent of unfamiliar males (Bruce and

Parrott, 1960), seems not to occur in rats. However, the ‘Whitten effect’, in which volatile male

scents trigger oestrus in females (Whitten, 1959), and the ‘Lee–Boot effect’, when females

housed without males show suppressed, irregular oestrus cycles (Van Der Lee and Boot, 1956) do

occur relatively weakly in rats. In rats and mice, male odour accelerates the onset of puberty in

females, in a phenomenon labelled the ‘Vandenbergh effect’ (Vandenbergh, 1969, 1976).

The scent of female rats, especially those in oestrus, stimulates not only male sexual

behaviour, but also urinary-marking (Manzo et al., 2002) and competitive aggression (Alberts

and Galef, 1973). It is possible therefore, that housing males where they can smell females could

affect their physiology and behaviour, affecting research, and might affect their welfare either

way. The vomeronasal system, probably responsible for detecting these scents, habituates to

stimuli less easily than most sensory systems (Holy et al., 2000), so the effects might be

persistent. However, since the vomeronasal organ requires direct physical contact to detect some

pheromones (Brennan and Keverne, 2004), the problem might only exist if the scent is volatile.

Other important scents here include those mediating the mother–pup relationship. For

example, diodecyl proprionate, a pup preputial gland pheromone, induces maternal licking

(Brouettelahlou et al., 1991). Mother rats produce various odours aiding pup survival, including

those guiding pups to the nipples, and those deposited in the bedding that reduce pup activity,

keeping them in the nest (Porter and Winberg, 1999). Also, pregnant females release a non-

volatile pheromone that prevents infanticide by cohabiting males (Mennella and Moltz, 1988).

Perhaps it is the removal of these scents that increases the likelihood of pups being cannibalised

when rats’ cages are cleaned within the first few days of birth (Burn and Mason, in press).

4.3. Olfactory modulation of aggression

Aggression in male rodents can be triggered by novel (usually male) scents, so rats rendered

anosmic show little aggression in resident–intruder tests (Alberts and Galef, 1973). Habituation to

familiar or self-scents plays a large role in reducing aggression between familiar or related

individuals. For example, aggression is reduced between more familiar individuals (Alberts and

Galef, 1973; Garcia-Brull et al., 1993) and between more closely related individuals (Nevison et al.,


2003). Some inbred mouse strains cannot discriminate between familiar and unfamiliar conspecific

odours, resulting in reduced aggression (Nevison et al., 2003). This could also be true for rats.

In fact, unfamiliar male scents not only stimulate aggression, but also defensive behaviour in

subordinate males encountering dominant male odours. Rats defeated by an alpha-male,

subsequently show avoidance and fear behaviour upon encountering the scent of other alpha-

males (Williams and Groux, 1993; Williams, 1999).

This said, while cage-cleaning – which removes scent marks – provokes aggression in male

mice (Gray and Hurst, 1995; Van Loo et al., 2000), in familiar rats it merely provokes non-

aggressive skirmishing (Burn et al., 2006a,b); perhaps for this reason cage-cleaning frequency

seemingly has no long-term effects on male rat welfare.

When unfamiliar rats are to be housed together, exposing them to each other’s scents for a few

days before allowing physical contact may prevent aggression (e.g. Bulla, 1999). Alternatively,

aggression can sometimes be prevented by masking unfamiliar conspecifics using another

unfamiliar, neutral scent. In rats evidence is anecdotal, but in a controlled study of mice,

chocolate or sheep’s wool odours reduced resident–intruder aggression (Kemble et al., 1995).

Finally, it is worth mentioning that odour-mediated aggression does not only occur between

males. For example, mother rats able to smell their own pups show aggression towards

intruders—neither visual, tactile, nor auditory cues from the pups elicit this aggression (Ferreira

and Hansen, 1986).

4.4. Communication about experiences

Rats are generally attracted to areas smelling of conspecifics (e.g. Galef and Heiber, 1976;

Mackay-Sim and Laing, 1980), but scents released during negative or positive experiences, can

make those areas aversive or more attractive, respectively.

Rats produce ‘alarm’ odour when they experience electric shocks (Mackay-Sim and Laing,

1980; Abel and Bilitzke, 1990; Williams and Groux, 1993; Kiyokawa et al., 2004), transport

between rooms (Beynen, 1992), and the events and disturbances accompanying carbon dioxide

euthanasia (Ware and Mason, 2003). They probably also produce it in forced-swim tests (Abel

and Bilitzke, 1990), but no unstressed controls were used so rats may simply have been

responding to odours left by an unfamiliar male. Alarm odour is more powerful with more severe

stressors (Mackay-Sim and Laing, 1980). The molecule(s) involved have not yet been identified,

but a candidate is 2-heptanone; more of this is present in urine from stressed rats, but diazepam

during the stressor does not reduce the amount produced (Gutierrez-Garcıa et al., 2006).

In recipients, alarm odour increases freezing behaviour (Williams, 1999; Kikusui et al., 2001),

activity (Mackay-Sim and Laing, 1980; Abel and Bilitzke, 1990; Kikusui et al., 2001; Ware and

Mason, 2003), body temperature (Kikusui et al., 2001), hypothalamic–pituitary–adrenal activity

(Takahashi et al., 1990; but see Mackay-Sim and Laing, 1980), urination (Stevens and Koster,

1972), and latency to approach rewards (Mackay-Sim and Laing, 1981; Ware and Mason, 2003).

It also causes avoidance compared with the scent of unstressed conspecifics (Mackay-Sim and

Laing, 1980). Experience can affect responses to alarm odour, with rats avoiding the odour of

shocked rats more if they have experienced shock themselves, but not necessarily if they have

experienced defeat by an alpha-male (Williams and Groux, 1993).

A somewhat separate body of literature describes ‘frustration’ or ‘non-reward’ odour, produced

when anticipated rewards are withheld (Collerain and Ludvigson, 1972; Ludvigson et al., 1985;

Taylor and Ludvigson, 1987). Again this odour causes avoidance, but unlike alarm odour, no fear

responses to it have been reported. It seems not to exist in urine (Collerain and Ludvigson, 1972),


unlike alarm odour (Mackay-Sim and Laing, 1981), but both are also produced from other bodily

sources yet to be identified (Mackay-Sim and Laing, 1981; Weaver et al., 1982).

Rats probably also produce a ‘reward’ odour, although this has mainly been tested against non-

reward situations (i.e. frustration odour), with no neutral rat odour control. Nevertheless, a rat’s trail

is more attractive if laid down after the rat receives a reward than before (Galef and Buckley, 1996),

and when it perceives a signal that reliably predicts reward (Ludvigson et al., 1985). However, the

attraction of rats to reward odour is much weaker than the avoidance of frustration odour, when

compared against the same ‘no odour’ control (Taylor and Ludvigson, 1980).

The release of alarm odour means that rat welfare and experimental aims might be

compromised if neighbouring conspecifics are distressed by illness, injury, or experimental

procedures (Beynen, 1992). Any of these odours can bias rats’ decisions in choice tests (Collerain

and Ludvigson, 1972; Aoyama and Okaichi, 1994; Mitchell et al., 1999), increase ‘baseline’

stress in subsequently tested rats or supposed control ones (Beynen, 1992; Kikusui et al., 2001),

and alter behaviour in tests such as swim tests (Abel and Bilitzke, 1990), and open field or novelty

tests (Mackay-Sim and Laing, 1981; Takahashi et al., 1990; Ware and Mason, 2003).

There has apparently been no evaluation of effective ways to clean experimental apparatus;

various cleaning agents are used, which probably vary in efficacy and may have intrinsic odours

that affect rats. Alcohol is commonly used, but in pigs, its volatile components can reduce

cortisol levels in open field tests (Thodberg et al., 2006).

4.5. Communication about food

Rats can learn about specific foods from conspecific odours. Carbon disulphide, present in

rats’ breath (Galef et al., 1988), causes rats to strongly prefer novel foods eaten by their

cagemates versus other novel foods (e.g. Strupp and Levitsky, 1984). The preferences can persist

for at least 30 days, even without opportunity to sample the foods during that time (Galef and

Whiskin, 2003b).

Aversion to novel foods can be caused by the ‘poisoned partner effect’ (Lavin et al., 1980).

Here if a novel food is eaten by a rat, which then encounters the odour of a poisoned conspecific,

the healthy rat will subsequently avoid the novel food, even if the poisoned rat did not eat it

(Stierhoff and Lavin, 1982). Strangely, the healthy rat only avoids food that it itself has eaten,

rather than that eaten by the poisoned rat, and therefore not necessarily the poisonous food (Galef

et al., 1990). In fact, exactly as described above, the healthy rat actually prefers novel food after

smelling it on the poisoned rat’s breath (Galef et al., 1990).

Lactating rats also avoid novel foods ingested just before their pups become ill, because of an

odour released by pups with gastrointestinal illness (Gemberling, 1984). The odour causes no

aversion in males or nulliparous females, and is not released by pups stressed in other ways, so it

seems more specific than the poisoned partner effect.

4.6. Scents in the laboratory

Most of the scents relevant to laboratory rats are those within the cage itself. Apart from those

produced by conspecifics or food, others could include detergent residues, bedding materials, and

microbial products from the breakdown of food or excreta. Cage-cleaning abruptly changes the

olfactory environment, which might contribute to post-cleaning changes in rat behaviour and

physiology (Burn et al., 2006a). Also, like gerbils, rats might more accurately discriminate scents

in a test arena on days when their cages are clean rather than soiled (Dagg et al., 1971).


Another salient source of smell for laboratory rodents might be their human handlers. Rats

respond differently towards different humans (McCall et al., 1969; Morlock et al., 1971;

Davis et al., 1997; van Driel and Talling, 2005), mostly because of differences in odour

(McCall et al., 1969). People smell different due to genetic factors and environmental ones,

such as diet, smoking, perfume, soap, and deodorant. Regular rodent handlers may also be

‘marked’ with odours from previously handled rodents, sometimes including reward or alarm

odours.

Additionally, rats might fear humans carrying scents from their pets, especially if the pet is a

predatory species. Rats innately fear predator odours, including cats and mustelids (reviewed in

Blanchard et al., 2003), but apparently not dogs. Rats cannot easily habituate to predator odours

(Blanchard et al., 1998), showing increased corticosterone, freezing and vigilance, elevated plus-

maze anxiety and endogenous opioid analgesia, and suppressed electric-prod burying, and

impaired working memory (Williams, 1999; Blanchard et al., 2003). Predator odours also elicit

fear-related fast-waves and reduce cell-proliferation in the dentate gyrus (Heale et al., 1994;

Tanapat et al., 2001).

It is even possible that rats would instinctively fear human odour—wild rats usually avoid

close human contact, and any such fear of humans might have escaped our notice because, of

course, it would require a controlled experiment not involving human presence.

Many odours from synthetic products used in laboratories could affect rodents. While several

reviews compare the efficacy of detergents for cleaning animal cages (e.g. Heuschele, 1995),

none discuss their potential olfactory impacts on the animals. Yet, some organic solvents (e.g.

xylene, toluene, diethyl ether, and methyl methacrylate) cause avoidance and fast-waves in the

dentate gyrus, just as predator odours do (Heale et al., 1994). These solvents constitute many

everyday substances, including some inks, glues, and paints; indeed, identification-marking

rodents with inks or dyes can affect their anxiety profiles (Burn et al., 2008) and cause them to

become submissive to unmarked cagemates (Lacey et al., 2007).

Many odorants that smell subjectively pleasant to humans, often therefore being present in

perfumed products or human diets, can also influence hypothalamo-pituitary–adrenal activity

and immune responsiveness, positively or negatively (Komori et al., 2003). Rose oil (de Almeida

et al., 2004) and ‘green odour’, trans-2-hexenal (Nakashima et al., 2004), are anxiolytic to rats.

Citrus oils are analgesic (Aloisi et al., 2002), but can have complex effects on rodent anxiety

(Komori et al., 2003; Ceccarelli et al., 2004). In rat pups, peppermint increases mortality and

decreases activity (Pappas et al., 1982), and rats avoid the scent of garlic (Keeler, 1942) and

rosemary (R.M.J. Deacon, personal communication). Many of these effects could inadvertently

introduce variation between experiments, but some could be used as non-nutritive environmental

enrichments or rewards. Also, anxiolytic scents could be easily administered to rats in mildly

stressful situations (de Almeida et al., 2004; Nakashima et al., 2004).

5. Gustation

Like us, rats are opportunistic omnivores; their ecological niche is characterised by sampling

diverse food substances and remembering their nutritional consequences (e.g. Capaldi, 1996).

They rapidly learn aversions to harmful novel foods, which can be a problem in pest control

situations when they ingest sub-lethal quantities of bait. Rats, particularly wild strains, are

neophobic, being reluctant to consume novel food (Galef and Whiskin, 2003a). They initially

sample only small amounts of novel food (if any at all), but if it proves safe, they later readily

consume it, often in preference to more familiar foods (Calhoun, 1963). Under natural


conditions, this cautious but explorative behaviour might help them obtain a full nutritional

complement, reducing reliance on any one food type, while avoiding poisoning.

Rats detect similar taste dimensions to humans, i.e. sweetness (carbohydrates and artificial

sweeteners), saltiness (sodium salts), sourness (hydrogen ions), bitterness (quinine, caffeine,

most natural toxins, and some others) (Grill and Norgren, 1978), and umami (amino acids, such

as glutamate) (e.g. Smith and Margolskee, 2001). As with humans, sweetness and umami are

rewarding, bitterness is usually aversive, and saltiness and sourness are only pleasant at low

concentrations (Grill and Norgren, 1978; Berridge, 2000). They also initially strongly avoid

capsaicin, the ‘hot’ taste of chilli, but often consume it readily once it becomes familiar (Jensen

et al., 2003). However, rats do not perceive certain artificial sweeteners as being ‘sweet’ (Sclafani

and Abrams, 1986; Dess, 1993; Sclafani and Clare, 2004), and they may have separate receptors

for sugars and starch (Sclafani, 1987). Their bitterness thresholds for some compounds differ

from ours (Glendinning, 1994; Mueller et al., 2005), allowing denatonium benzoate – which

tastes less bitter to rats than to humans and some other animals – to be added to baits to prevent its

consumption by non-target species (Hansen et al., 1993). There are also some strain and sex

differences in rat gustation (Boakes et al., 2000; Clarke et al., 2001).

In fact, ‘flavour’ involves not only gustation, but also olfaction and tactile sensations (Smith

and Margolskee, 2001). For completeness, these senses are not separated here when discussing

the practical implications of rat gustatory biases.

5.1. Taste in the laboratory

Laboratory rodents usually have no opportunity to sample different foods, typically being fed

a palatable, dry, nutritionally complete diet, in powder form or as pellets. These diets are easily

stored, inexpensive, and require little preparation (Lane-Petter, 1975), and they aid

standardisation between experiments. Laboratory rats will also taste their mothers’ milk,

bodily secretions from themselves or conspecifics (if socially housed), their cage surfaces, and

perhaps human hands or gloves, and bedding material (if provided). Hence, scope for learning

taste–nutrient associations is very limited, rendering the gustatory sense largely redundant in

laboratories.

For other sensory modalities, sensory deprivation reduces the volume and functioning of the

associated brain regions. For example, the visual cortices of rats reared in darkness are

permanently underdeveloped (Fagiolini et al., 1994), while sensory deprivation only temporarily

limits olfactory bulb (Cummings et al., 1997) and barrel cortex development (Polley et al., 2004;

but see Rema et al., 2003). However, despite rats frequently being used as models in taste

research, precisely because their gustatory perception is supposedly similar to ours, the effects of

gustatory deprivation on the brain and behaviour are apparently unknown. The effects may be

minimal if taste is tightly genetically controlled, but alternatively, lack of gustatory experience

could, for example, exaggerate rats’ neophobia or diminish their gustatory learning abilities.

5.2. Nutritional regulation

It is unclear whether rats can appropriately self-regulate their nutritional intake, given the

opportunity. Most discrepancies between findings are probably due to differences between the

diets offered to rats (Naim et al., 1985; Sclafani, 1987; Prats et al., 1989), and circadian variations

in intake patterns (Larue-Achagiotis et al., 1992). Rats generally do select foods appropriate for

their changing nutritional needs, but like humans, they are biased towards sugary or fatty foods.


They are consequently also prone to obesity if offered palatable, calorific diets (Naim et al., 1985;

Sclafani, 1987; Prats et al., 1989).

Because laboratory rodent diets are homogenous, they allow no qualitative nutritional

regulation. Generally, this is unproblematic because the diets have sustained rodent populations

for many decades, without apparent negative effects on breeding, health, or longevity. However,

although special formulations are available, many widely used diets cover all age and sex

categories: oestrus females, weanling pups, and elderly males alike. Moreover, they are often

common to rats and mice. Thus, within this diversity, individuals might sometimes have different

nutritional requirements from that provided. In standardising diets to this extent, we might

inadvertently increase, rather than decrease, variation in rodents’ internal nutritional states

because they have no opportunity to regulate them.

Some dietary supplements can enhance laboratory rat health, calling into question the

completeness of homogenous diets. For example, blueberries, high in antioxidants, prevent

cognitive deficits in aging rats (Casadesus et al., 2004), and as mentioned previously, other dietary

supplements prevent retinal damage (Li et al., 1985). Also, in hamsters, supplementation with seeds

and rabbit chow increased pup growth, and reduced cannibalism by the mothers (Day et al., 2002).

5.3. Refinement within the homecage

Palatable diets may provide rats with ‘enjoyment’ (Lane-Petter, 1975) or hedonic experiences,

with palatable and unpalatable foods eliciting distinctive behavioural expressions that are

homologous to human gustatory expressions (Berridge, 2000). Most welfare efforts concentrate

on reducing negative welfare, but facilitating positive welfare, such as pleasure from food or

foraging, should not be neglected (e.g. Balcombe, 2005). Food-related environmental

enrichments might be particularly relevant for generalists, like rats, because their natural

ecology incorporates diverse food types, varying through time and space. However, the idea of

food-related enrichment has been little explored for laboratory rats, and yet it could improve their

welfare (Johnson and Patterson Kane, 2003), provided obesity is avoided (e.g. Mattson, 2005).

There are three main aspects of food that could be varied for enrichment purposes: nutritional

content, flavour, and physical presentation.

5.3.1. Nutritional content

Providing rodents with very nutritionally diverse diets may be undesirable for practical

reasons (Lane-Petter, 1975; Key, 2004), and because they encourage obesity (Mattson, 2005),

and may increase variation. Nevertheless, offering some opportunity to nutritionally self-regulate

could be beneficial, as suggested above. In some animal facilities, seeds and nuts are scattered

onto rats’ bedding; rats become very active upon hearing them being scattered in neighbouring

cages, and continue foraging for many hours (Key, 2004). Since the seeds would constitute only a

very small proportion of the diet, they are unlikely to impact heavily on nutritional regulation, but

could allow some relevant gustatory stimulation and regular hedonic experiences. Proper

evaluation of the effects is necessary however; the most relevant study so far seems to be one,

mentioned earlier, when seed supplements enhanced hamster pup growth and decreased

cannibalism (Day et al., 2002).

5.3.2. Flavour

Even without nutritional value, gustatory enrichment could be achieved; providing daily

non-nutritional pina-colada flavour treats to breeding mice increased the number of pups


weaned (Inglis et al., 2004), suggesting that the hedonistic aspects alone of scatter-feeding are

beneficial.

Domesticated rats value variety, and will substitute a preferred food that has been their sole

diet for several days for a less preferred, newly available food (Galef and Whiskin, 2003a, 2005).

They also consume more food if provided as a succession of varied ‘meals’ rather than

homogenous meals (Treit et al., 1983; Clifton et al., 1987; Le Magnen, 1999b). These preferences

exist even when foods differ primarily in flavour not nutritional value, such as when cinnamon,

cocoa, ‘all spice’, or marjoram are added to normal chow (as in the above five studies). These

additives presumably have negligible bioactivity, being common non-nutritive components of

human diets, but confirmation in rats is required. The above studies suggest that obesity might be

a risk because of the increased food consumption, but they were all relatively short-term, so rats

might down-regulate their intake of variable food over time. Le Magnen (1999b) found that if

‘variable days’ were alternated with ‘homogenous days’, rats ate less food than normal on

homogenous days, perhaps compensating for over-eating on variable days.

5.3.3. Physical presentation

Finally, enrichment might be achieved through varying dietary presentation. Soft ‘wet mash’

(chow soaked in water) is often used to help sick or weak rats gain weight, and usually any

healthy cagemates also prefer the mash to freely available pellets. However, it is an impractical

enrichment for healthy rats, being messy and encouraging microbial growth (Lane-Petter, 1975).

Occasionally scattering chow pellets within the cage allows rats to eat in their natural posture,

holding the pellet in their forepaws (Bruce, 1965), and they more readily consume these pellets

than those in the hopper (personal observation).

Captive rats also ‘contra-freeload’, choosing food that requires handling and preparation, even

when prepared food is available (Carder and Berkowitz, 1970). This may be because most of a

wild rat’s time and effort would be devoted to foraging (Johnson and Patterson Kane, 2003).

Scattering small food items, such as the aforementioned seed mixes or chow pellets, in bedding

allows rats to forage, which may be rewarding in itself. Scatter-feeding rarely triggers

competitive aggression because the food is spatially distributed. Commercially available rodent

puzzle-feeders are also available, although they are uncommon in laboratories and are not always

easily sourced.

5.4. Refinement of experiments

The generalist feeding habits of rats can be exploited in research, improving experiments

ethically, enhancing rats’ cooperation, and reducing interference from stress. Drugs and

inoculants are often delivered by gavage, a tube inserted via the mouth into the stomach,

which can be technically difficult, and causes stress, respiratory distress, and occasionally

even death (Balcombe et al., 2004). However, substances can be successfully delivered within

palatable vehicles that rats will voluntarily consume, provided there is no interference with

the active ingredient. Fruit- or beef-flavoured gelatine is commonly used but some rats only

reluctantly consume it, so it can be worth trying several alternatives (Hawkins et al., 2004).

Another example is to use small amounts of chocolate (Huang-Brown and Guhad, 2002).

Taste aversion can develop if the vehicle becomes associated with illness, but giving rats

prior experience with the unadulterated food can prevent this. Some substances can also be

microencapsulated and added to chow for long-term studies (Melnick et al., 1987; Dieter

et al., 1993; Yuan et al., 1993).


Preferred rewards can often be used to motivate rats to perform tasks in experiments, rather

than using punishments or prior deprivation. Deprivation is a powerful motivator, but can

undesirably affect behaviour, physiology, neurochemistry, and drug efficacy (Slawecki and

Roth, 2005). Moreover, it is sometimes unnecessary, because undeprived rats will often work –

albeit to a limited extent – for preferred rewards, including commercially available reward

pellets, sucrose solution (Slawecki and Roth, 2005), or breakfast cereals (e.g. Ellis, 1984). Prats

et al. (1989) found that rats did not readily consume cheese, chocolate or fruit-candy, and instead

preferred other foods offered, including banana, cookies, standard chow pellets, and liver pate.

Large quantities of dairy products (DiBattista, 1990) and chocolate (Huang-Brown and Guhad,

2002) should be avoided as they harm rodent health. Undeprived rats are particularly motivated

to earn rewards if experiments coincide with their active period (Hyman and Rawson, 2001),

with a shifted light cycle enabling practical working hours (see Section 2). Neophobia can be

eliminated by providing the palatable incentive in the homecages of rats several days before

experiments.

Finally, food must often be withheld overnight before surgery or intraperitoneal injections.

This deprivation causes weight loss, and reduced hepatic weight and blood glucose, and

potentially, emotional distress from hunger. However, providing sugar cubes to the rats can

prevent these problems, while gastrointestinal volume is still reduced, as required (Levine and

Saltzman, 1998).

6. Somatosensation

Rat somatosensation could be considered from many different angles. Here, the focus is on that

relating to the ability of rats to explore and interact with their environments. In the rat

somatosensory cortex, the vibrissae (sensory whiskers), nose and mouth, forepaws, and sinus hairs

on the wrists, are particularly well represented. In fact, the forepaws are represented twice each, and

the whiskers and sinus hairs have specialised granular aggregates devoted to them (Hermer-

Vazquez et al., 2005). In general, rat and human somatosensation seem similar, but there are two

main differences that noticeably affect rat behaviour. First, rats’ vibrissae are extremely sensitive

(Arabzadeh et al., 2005), being comparable to primate fingertips (Carvell and Simons, 1990). Rats

can whisk them independently of each other across surfaces to make fine tactile discriminations

(Guic-Robles et al., 1989; Carvell and Simons, 1990). In a study investigating rats’ numerical

competencies, subjects could not discriminate between two, three or four tactile stimuli delivered to

the body, but they succeeded when the stimuli were delivered to a single vibrissal hair (Davis et al.,

1989). The vibrissae also detect differences in mechanical resonant frequencies, with the shorter

anterior vibrissae detecting higher frequencies than the longer posterior ones (Neimark et al., 2003).

The second obvious difference from humans relates to thigmotaxis; the bias of rats towards

maintaining physical contact with vertical surfaces. In fact, thigmotaxis underlies many tests of

‘anxiety’ (Treit and Fundytus, 1988), because when rats perceive environments as threatening,

they stay closer to vertical surfaces, such as the boundaries of open field arenas, or the closed

arms of elevated plus-mazes. The thigmotactic bias may not be strictly somatosensory, perhaps

also incorporating visual preferences for avoiding light exposure. Rats that lack vibrissae on one

side prefer to maintain wall contact on their intact side, suggesting the vibrissae play a role

(Meyer and Meyer, 1992).

The implications of rat somatosensation include the impact of environmental enrichment on

rat somatosensory development generally, and implications of the vibrissal sense for experiments

and housing.


6.1. Environmental enrichment and somatosensation

Environmental enrichment profoundly affects the somatosensory and barrel cortices. In rats

kept in enriched rather than barren environments, the primary somatosensory cortex representing

the forepaws becomes 1.5 times larger (Xerri et al., 1996; Coq and Xerri, 1998, 2001). The barren

cages in these studies contained bedding, exerting their effect despite rats being able to dig with

their forepaws, so the difference might be even more pronounced in rats housed on wire floors.

Environmental enrichment seemingly does not enhance textural discrimination abilities, but it

does increase the rate of learning such discriminations (Bourgeon et al., 2004). Enrichment can

also counteract age-related declines in hind-paw representation in the somatosensory cortex,

which is otherwise associated with impaired walking in aged rats (Godde et al., 2002). Finally, in

naturalistic environments, the representation of each whisker in the barrel cortex becomes

dramatically more well defined compared with standard cages (Polley et al., 2004).

The above studies combined several enrichment types, including social contact, foraging

opportunities, structural features and novelty, so it is unclear what relative contributions were

made by each enrichment type. It is lack of tactile contact with conspecifics that apparently leads

to the self-biting and tail manipulation seen in isolated rats (Day et al., 1982; Hurst et al., 1997).

6.2. Vibrissae and the laboratory environment

The sensitivity of the vibrissal sense (Davis et al., 1989; Guic-Robles et al., 1989; Carvell and

Simons, 1990; Arabzadeh et al., 2005) is probably under exploited in learning tasks, where less

salient visual cues are currently morewidely used (Dymond, 1995; Dymond et al., 1996; Birrell and

Brown, 2000). However, laboratory rats can sometimes lack vibrissae for various reasons, including

‘barbering’, when hairs and often whiskers are removed by conspecifics (Garner et al., 2004). This

occurs in rats, albeit to a much lesser extent than in mice (Bresnahan et al., 1983; Wilson et al.,

1995). Other rats may lack whiskers due to their strain; some nude rodent strains have nowhiskers at

all (e.g. Sundberg et al., 2000), but most have short, kinked whiskers, giving a limited sensory range

(e.g. Festing et al., 1978; Moemeka et al., 1998). Nude strains also lack the sensitive guard hairs

otherwise dispersed through the coat, and which would convey proprioceptive information.

Both vibrissal absence and barrel cortex impairment through lack of environmental

enrichment (as described above), could have practical consequences. Rats lacking vibrissae show

impaired orientation towards tactile stimuli, and – provided they have environmental enrichment

– compensate by orienting towards visual stimuli more than controls do (Symons and Tees,

1990). Whiskers also aid swimming, enabling animals to keep their heads above water (Ahl,

1986; Meyer and Meyer, 1992), and consequently, rats lacking vibrissal sensation can drown in

water mazes and swim tests (Hughes et al., 1978).

Finally, vibrissae are important in social interactions, with whiskerless rats being unable to

avoid bites to their faces during fighting (Blanchard et al., 1977a,b). Because aggression between

familiar rats is uncommon (Burn et al., 2006b), whiskerless rats need not be socially isolated,

except in cases where aggression is observed. However, whiskerless rats may be injured if

introduced to unfamiliar conspecifics, when fighting is more likely.

7. Summary

It is impossible for us to know what it is like to be a ‘rat’ (Nagel, 1974), but knowledge of their

sensory biases allows us to imagine what it might be like, as a human, to have those biases within


a laboratory rat’s environment. This insight, while imperfect, could help predict how rats might

be affected by different situations, improving our experimental design and their welfare. In

summing up then, an overall theoretical picture of a rat’s perception of the laboratory could be as

follows.

The rat’s sensitive eyes, shunning the intense artificial light, provide it with a hazy view in

predominantly grey, ultraviolet and green hues. From within its cage, it hears the chirps, squeaks

and whines of its neighbours, gaining information that we cannot hear unaided and are yet to

understand. Background noise consists of the low babbles and hisses of distinctively scented

humans, and the unregulated drones and blasts of ultrasonic sounds. Scents provide visceral

warnings and enticements, induce new motivations, and inform the rat about social possibilities

outside the cage. The environment wafts a succession of scents, from pleasant, calming fragrances

to the innately alarming odours of intangible predators. The rat tastes little apart from its dry,

satiating homogenous diet. Its vibrissae provide a protective, finely tuned force field to feel the

details of the cage surfaces; with the rat perceiving security from close contact with the solid walls.

8. Conclusion

Knowledge of the sensory gulfs and similarities between ourselves and this commonly used

research animal can improve science and enhance rat welfare. More work is still necessary to

understand rat perception, and even more so for less well-researched species. The aim of this review

is to make current knowledge accessible to researchers, rat caretakers and rodent specialists, in the

hope that it will enable tangible improvements in experimental design and rat welfare.

Acknowledgements

Many thanks to Georgia Mason for her detailed comments and encouragement, and also to

Robert Deacon, Mark Ungless, Jennifer Bizley, and Alex Weir for their comments.

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