Sniffing and whisking in rodents
Highlights
► Sniffing and whisking serve to gather sensory information, and occur during reward expectation. ► These rhythmic activities affect both the coding and central processing of sensory inputs. ► As sniffing and whisking exhibit a fixed temporal relationship, they may share a common circuitry.
Introduction
When one observes rodents introduced in a new environment, one immediately notices that they are extremely curious [1]. They run about, stand up on their hind legs, crane their necks forward, and repeatedly explore the whole environment by sniffing and whisking vigorously. Psychologists have described curiosity as a drive like hunger and thirst, which implies that gathering information is rewarding. In experimental studies, sniffing and whisking are commonly considered as motor strategies for rapidly gathering detailed information about the location, texture, and scent of objects. Yet, it is intriguing that decorticated rats, or rats deprived of olfactory and vibrissa afferents, continue to sniff and whisk in a relatively normal manner. Therefore, beyond the obvious intuition that vibrissae are ‘for touch’ and noses ‘for smell’, it is not clear why rhythmic activity is associated with the use of these sensors. Here, we examine the dynamics of rhythmic sniffing and whisking, and how they shape olfactory and tactile sensations in rodents. We place special emphasis on the behavioral significance of the apparent coordination of these patterned activities.
Section snippets
A link between sniffing and whisking
In a now classic paper published in 1964, Welker [2] provided the first descriptive account of the sniffing behavior in rats. Using cinematographic technique, he reported that sniffing consists of an integrated movement sequence involving: (1) bursts of polypnea, (2) recurrent protraction and retraction of mystacial vibrissae, (3) repetitive retraction and protraction of the tip of the snout, and (4) a rapid series of head movements and fixations. These four components occur at rates between 5
Rhythmogenesis of sniffing and whisking
Sniffing in rats is usually defined as rapid, rhythmic respiration [2, 9]. Rats, unlike humans, always breathe nasally, so lower frequencies (1–3 Hz) correspond to basal respiration while higher frequencies (4–12 Hz) correspond to ‘sniffing’ per se. Although rats and mice are commonly used in studies of respiratory rhythmogenesis, the neural mechanisms underlying the generation of sniffing remain unknown. One possibility is that sniffing relies on an increased rate of bursts in the central
The function of the vibrissae in sensation
It is necessary to first consider the anatomical organization and function of the vibrissa sensorimotor plant itself to understand the behavioral significance of whisking. Rats and mice are nocturnal animals with poor visual acuity. They have laterally placed eyes, which allows very little overlap of the visual fields. Panoramic vision gives them a wide field of view, which probably helps them detect predators but provides poor depth discrimination. At close range they rely on sniffing and
Sniffing and whisking shape sensory inputs
Sniffing and whisking affect both the encoding and central processing of sensory inputs. Sniffing and whisking per se, in the absence of odor or touch, modulate the activity of mitral cells and first-order vibrissa afferents respectively [18, 19, 20•, 21] (Figure 3a). Though air flow varies in amplitude, velocity and frequency, individual mitral cells preferentially discharge at a specific phase of the sniffing cycle [21], such that odor evoked responses are normalized to the duration of the
Context-dependent and state-dependent sniffing and whisking modes
There is evidence to suggest that the expression of both whisking and sniffing is dependent on the motivational state and behavioral goals of the animal. Analysis of sniffing in rats performing a go-nogo odor discrimination task reveal two modes of sniffing: a 7–8 Hz sniffing mode associated with odor sampling, and a 10–12 Hz sniffing mode in anticipation of reward delivery [33]. Correspondingly, several other studies report that sniffing is associated with reward anticipation. For example,
Why do rodents sniff and whisk?
Although sniffing clearly subserves olfaction and strongly patterns olfactory processing, several studies reported that basal respiratory rhythm is sufficient for delivering odorants to olfactory receptors, and that rats and mice can perform simple odor discrimination after a single sniff [32•, 43, 44]. Likewise, rodents can locate objects and gauge aperture widths with a single whisk and, rather dramatically, severing the facial nerve to block whisking does not affect performance [45, 46].
Conclusions
Many rhythmic behaviors in rodents have been reported to alternately couple and decouple to breathing. These include whisking and head movements [2], licking, mastication, and swallowing [42]. These rhythmic activities are all generated by pattern generators located in the brainstem. The case of sniffing and whisking is of particular interest as these behaviors often occur spontaneously, are phase locked, and are related to the sensory exploration of the immediate environment. From a practical
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
We thank Adam Kepecs and Dima Rindberg for discussions that shaped this review, and the Canadian Institutes of Health Research (grant MT-5877), the National Institutes of Health (grants NS058668 and NS066664), and the US-Israeli Binational Foundation (grant 2003222) for their support.
References (50)
- et al.
The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units
Brain Res
(1970) - et al.
State dependence of upper airway respiratory motoneurons: functions of the cricothyroid and nasolabial muscles of the unanesthetized rat
EEG Clin Neurophysiol
(1977) - et al.
Respiratory-modulated activities of motor units of the facial nerve
Respir Physiol
(1988) - et al.
Central respiratory modulation of facial motoneurons in rats
Neurosci Lett
(1993) - et al.
A quantitative analysis of sniffing strategies in rats performing odor detection tasks
Physiol Behav
(1987) - et al.
Neural substrates of two different rhythmical vibrissal movements in the rat
Neuroscience
(1984) - et al.
Serotonin regulates rhythmic whisking
Neuron
(2003) - et al.
Functional architecture of the mystacial vibrissae
Behav Brain Res
(1997) - et al.
Responses of trigeminal ganglion neurons during natural whisking behaviors in the awake rat
Neuron
(2007) - et al.
Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb
Neuron
(2010)
Visualizing the cortical representation of whisker touch: voltage-sensitive dye imaging in freely moving mice
Neuron
All in a sniff: olfaction as a model for active sensing
Neuron
The relationship between self-stimulation and sniffing in rats: does a common brain system mediate these behaviors
Behav Brain Res
Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation
J Physiol
Stimulus dependent synchronization of neuronal assemblies
Neural Comput
The sensory contribution of a single vibrissa's cortical barrel
J Neurophysiol
Quantifying the buildup in extent and complexity of free exploration in mice
Proc Natl Acad Sci USA
Analysis of sniffing of the albino rat
Behavior
Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control
J Neurophysiol
Biomechanics of the vibrissa motor plant in rat: rhythmic whisking consists of triphasic neuromuscular activity
J Neurosci
Looking for inspiration: new perspectives on respiratory rhythm
Nat Rev Neurosci
Structural and functional architecture of respiratory networks in the mammalian brainstem
Philos Trans R Soc Lond B Biol Sci
Whisker deafferentation and rodent whisking patterns: behavioral evidence for a central pattern generator
J Neurosci
Social facial touch in rats
Behav Neurosci
Muscle architecture in the mystacial pad of the rat
Anat Rec
Cited by (95)
Neuroanatomical frameworks for volitional control of breathing and orofacial behaviors
2024, Respiratory Physiology and NeurobiologyCuriosity-driven exploration: foundations in neuroscience and computational modeling
2023, Trends in Neurosciences