The Brainstem Oscillator for Whisking and the Case for Breathing as the Master Clock for Orofacial Motor Actions

Kleinfeld, David; Moore, Jeffrey D.; Wang, Fan; Deschênes, Martin

doi:10.1101/sqb.2014.79.024794

Cited by 27 publications

(17 citation statements)

References 51 publications

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“…What might be the utility of coordinating the fast, rhythmic motion of the different sensory apparatuses as animals explore their nearby environment? It is an open issue whether the coordination of these motor actions maximizes sensory input [30, 31], such as by sweeping odorants toward the nose. Any source of sensory input that contributes to both touch and olfaction, which are elements of social interactions [32] as well as exploration (Figure 4G), will lead to multisensory input that is likely to be phase-locked to breathing.…”

Section: Discussionmentioning

confidence: 99%

Coordination of Orofacial Motor Actions into Exploratory Behavior by Rat

et al. 2017

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SUMMARY The delineation of sensorimotor circuits that guide exploration begins with an understanding of the pattern of motor outputs [1]. These motor patterns provide a clue to the form of the underlying circuits [2–4] (but see [5]). We focus on the behaviors that rodents use to explore their peripersonal space through goal-directed positioning of their nose, head, and vibrissae. Rodents sniff in response to novel odors, reward expectation, and as part of social interactions [6–12]. Sniffing serves olfaction [13, 14], while whisking synchronized to sniffing serves vibrissa-based touch [6, 15, 16]. We quantify the ethology of exploratory nose and head movements in relation to breathing. We find that sniffing is accompanied by prominent lateral and vertical de-flections of the nose, i.e., twitches, which are driven by activation of the deflector nasi muscles [17]. On the timescale of individual breaths, nose motion is rhythmic and has a maximum deflection following the onset of inspiration. On a longer timescale, excursions of the nose persist for several breaths and are accompanied by an asymmetry in vibrissa positioning toward the same side of the face. Such directed deflections can be triggered by a lateralized source of odor. Lastly, bobbing of the head as the animal cranes and explores is phase-locked to sniffing and to movement of the nose. These data, along with prior results on the resetting of the whisk cycle at the onset of inspiration [15, 16, 18], reveal that the onset of each breath initiates a “snapshot” of the orofacial sensory environment.

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Section: Discussionmentioning

confidence: 99%

Coordination of Orofacial Motor Actions into Exploratory Behavior by Rat

et al. 2017

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“…Multiple cranial nerves are required to dilate or stiffen the nasopharyngeal, oropharyngeal and laryngeal airways maintaining their patency (Abdala et al., ; de Britto & Moraes, ; St‐John, Rudkin, & Leiter, ). Indeed, several studies demonstrated that breathing modulates the nasofacial and oral motor outflows in rats (Kleinfeld, Moore, Wang, & Deschênes, ). Breathing has not only its physiological role in blood gas homeostasis but also serves as a common clock that couples nasofacial and oral senses during exploratory behaviours such as sniffing (Kleinfeld, Deschênes, Wang, & Moore, ).…”

Section: Introductionmentioning

confidence: 99%

Active expiratory oscillator regulates nasofacial and oral motor activities in rats

Britto

Magalhães

Silva

et al. 2020

Experimental Physiology

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New Findings What is the central question of this study?Does the parafacial respiratory group (pFRG), which mediates active expiration, recruit nasofacial and oral motoneurons to coordinate motor activities that engage muscles controlling airways in rats during active expiration. What is the main finding and its importance?Hypercapnia/acidosis or pFRG activation evoked active expiration and stimulated the motoneurons and nerves responsible for the control of nasofacial and oral airways patency simultaneously. Bilateral pFRG inhibition abolished active expiration and the simultaneous nasofacial and oral motor activities induced by hypercapnia/acidosis. The pFRG is more than a rhythmic oscillator for expiratory pump muscles: it also coordinates nasofacial and oral motor commands that engage muscles controlling airways. Abstract Active expiration is mediated by an expiratory oscillator located in the parafacial respiratory group (pFRG). Active expiration requires more than contracting expiratory muscles as multiple cranial nerves are recruited to stabilize the naso‐ and oropharyngeal airways. We tested the hypothesis that activation of the pFRG recruits facial and trigeminal motoneurons to coordinate nasofacial and oral motor activities that engage muscles controlling airways in rats during active expiration. Using a combination of electrophysiological and pharmacological approaches, we identified brainstem circuits that phase‐lock active expiration, nasofacial and oral motor outputs in an in situ preparation of rat. We found that either high chemical drive (hypercapnia/acidosis) or unilateral excitation (glutamate microinjection) of the pFRG evoked active expiration and stimulated motoneurons (facial and trigeminal) and motor nerves responsible for the control of nasofacial (buccal and zygomatic branches of the facial nerve) and oral (mylohyoid nerve) motor outputs simultaneously. Bilateral pharmacological inhibition (GABAergic and glycinergic receptor activation) of the pFRG abolished active expiration and the simultaneous nasofacial and oral motor activities induced by hypercapnia/acidosis. We conclude that the pFRG provides the excitatory drive to phase‐lock rhythmic nasofacial and oral motor circuits during active expiration in rats. Therefore, the pFRG is more than a rhythmic oscillator for expiratory pump muscles: it also coordinates nasofacial and oral motor commands that engage muscles controlling airways in rats during active expiration.

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“…The slow, orienting movements of the nose likely play a role in olfactory navigation since lateral deflections affect air flow between sides of the nasal cavity (Deschênes et al 2016a) and bilateral comparisons improve trail-tracking (Duistermars et al 2009;Louis et al 2008;Martin 1965;Porter et al 2007;Steck et al 2010). Synchronization of movement on a breath-bybreath cycle is seen in many types of orofacial movement and may play a role in binding multimodal sensory inputs (Heck et al 2017;Kepecs et al 2006;Kleinfeld et al 2014aKleinfeld et al , 2014bMoore et al 2013;Ranade et al 2013;Sirotin et al 2014;Wachowiak 2011;Welker 1964).…”

Section: Introductionmentioning

confidence: 99%

Functional brain stem circuits for control of nose motion

Kurnikova

Deschênes

Kleinfeld

2019

Journal of Neurophysiology

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Rodents shift their nose from side to side when they actively explore and lateralize odors in the space. This motor action is driven by a pair of muscles, the deflector nasi. We studied the premotor control of this motion. We used replication-competent rabies virus to transsynaptically label inputs to the deflector nasi muscle and find putative premotor labeling throughout the parvocellular, intermediate, and gigantocellular reticular formations, as well as the trigeminal nuclei, pontine reticular formation, midbrain reticular formation, red nucleus, and superior colliculus. Two areas with extensive labeling were analyzed for their impact on nose movement. One area is in the reticular formation caudal to the facial motor nucleus and is denoted the nose retrofacial area. The second is in the caudal part of the intermediate reticular region near the oscillator for whisking (the nose IRt). Functionally, we find that optogenetic activation of glutamatergic cells in both areas drives deflection of the nose. Ablation of cells in the nose retrofacial area, but not the nose IRt, impairs movement of the nose in response to the presentation of odorants but otherwise leaves movement unaffected. These data suggest that the nose retrofacial area is a conduit for a sensory-driven orofacial motor action. Furthermore, we find labeling of neurons that are immediately upstream of premotor neurons in the preBötzinger complex that presumably synchronizes a small, rhythmic component of nose motion to breathing. NEW & NOTEWORTHY We identify two previously undescribed premotor areas in the medulla that control deflection of the nose. This includes a pathway for directed motion of the nose in response to an odorant.

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The Brainstem Oscillator for Whisking and the Case for Breathing as the Master Clock for Orofacial Motor Actions

Cited by 27 publications

References 51 publications

Coordination of Orofacial Motor Actions into Exploratory Behavior by Rat

Coordination of Orofacial Motor Actions into Exploratory Behavior by Rat

Active expiratory oscillator regulates nasofacial and oral motor activities in rats

Functional brain stem circuits for control of nose motion

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