From the first cry to the last gasp, the respiratory system should never fail to supply sufficient oxygen to meet metabolic demands during every possible event throughout life (Del Negro et al., 2018). The respiratory pattern is not only determined by physical activity, but also reflects the emotional state, and volitional control of respiration can be used to alter affection and reduce stress (Suess et al., 1980; Philippot et al., 2002; Arch and Craske, 2006; Seppälä et al., 2014; Szulczewski, 2019). Indeed, multiple behaviors, such as swimming, playing musical instruments, parturition, or meditation depend on precise respiratory control (Brown and Gerbarg, 2009; Jakovljevic and McConnell, 2009; Bartlett and Leiter, 2012; Holstege, 2014; Sakaguchi and Aiba, 2016), and for many sports and arts, it is often the control of respiration that separates mediocre from top performance (Mahler et al., 1991; Phillips and Aitchison, 1997; Laczika et al., 2013; Salomoni et al., 2016). Thus, indeed, respiratory control affects all aspects of life.

Although control over respiration can be voluntary, most of it is subconscious, even during voluntary respiration. In this review, we discuss the integrated network of brain regions most involved in the control of respiration, their connections, and possible clinical consequences of their pathology. Throughout, we discuss how respiratory control and other motor and non-motor systems interact.

Despite their vast differences in body size and ecological niches, mammals possess similar basic mechanics of ventilation, with some variations between species or sexes (Carvalho and Gonçalves, 2011; Torres-Tamayo et al., 2018). Both lung and tidal volumes scale linearly with body weight, and the higher metabolic rate of smaller mammals is accounted for by a faster respiratory rate (Stahl, 1967; Boggs and Tenney, 1984). The force required for inspiration is delivered by so-called pump muscles that expand the rib cage. The diaphragm and external intercostal muscles are the most prominent inspiratory pump muscles, but also parasternal intercostal, sternocleidomastoid and scalene muscles can act as such (De Troyer and Estenne, 1984; De Troyer et al., 1998; De Troyer et al., 2005; Torres-Tamayo et al., 2018; Welch et al., 2019; LoMauro and Aliverti, 2021). During active expiration, expiratory pump muscles, in particular the internal intercostal and abdominal muscles, are active (De Troyer et al., 2005; Mortola, 2013; Welch et al., 2019). The diaphragm is under control of motor neurons in the phrenic nucleus located in the anterior ramus of the third to sixth cervical vertebrae (Wertheimer, 1886; Hollinshead and Keswani, 1956; Wu et al., 2017). The intercostal and abdominal muscles are innervated from the thoracic spinal cord (Figure 1A–C).

Figure 1

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Valve muscles regulate the air flow by adjusting the resistance of the upper airways. Activity of the facial nucleus can lead to opening of the nasal valve, via the dilator naris anterior muscle and the alar part of the nasal muscle (van Dishoeck, 1937; Strohl, 1985; Vaiman et al., 2003). Contractions of these muscles do not only facilitate inspiration, but can also relate to sniffing (Welker, 1964). Just before the start of inspiration, motor neurons of the hypoglossal nucleus activate tongue muscles, reducing collapsibility of the pharynx (Fuller et al., 1999; Gestreau et al., 2005). Indeed, tongue deformation, for example as a consequence of excessive fat depositions in obesity, can be related to obstructive sleep apnea (Lowe et al., 1986; Kim et al., 2014; Yu et al., 2021). Activation of the trigeminal motor nucleus can contribute to jaw movements (Mong et al., 1988). Finally, contractions of the larynx muscles show a bimodal pattern; initially, they are dilated to allow airflow into the lungs, while at the end of inspiration these muscles contract to reduce the outflow of air, prolonging the period of gas exchange (Gesell and White, 1938; Gautier et al., 1973; Insalaco et al., 1991; Hutchison et al., 1993; Amis et al., 1995; Dutschmann et al., 2014). Laryngeal constriction is controlled by the nucleus ambiguus via the vagus nerve (Dutschmann et al., 2014). The nucleus ambiguus houses also motor neurons controlling swallowing, the control of which is strongly coupled to that of respiration (McFarland and Lund, 1993; Moore et al., 2014).

Respiratory muscles typically serve multiple functions. Rib cage muscles, for instance, control both respiration and arm movements, so that locomotion and respiration are tightly coupled during quadrupedal locomotion. Indeed, one could argue that the change from quadrupedal to bipedal locomotion during hominid evolution paved the way for the intricate breathing control required for human speech (Carrier, 1984; MacLarnon and Hewitt, 1999).

Below, we describe the brain areas most involved in subconscious control of respiration, and their main connections. Most of these pathways are bilateral, but ipsi- and contralateral projections can differ in strength or in their ratio between excitatory and inhibitory fibers, potentially introducing asymmetries in motor activity (Biancardi et al., 2021). As detailed studies on monosynaptic projections are sparse in humans, we base our summary on animal studies, with earlier descriptions mostly concerning cats, and more recent ones often performed in rats or mice (Figure 2, Supplementary file 1). Connections labeled as sparse in the original papers are not included in this overview.

Figure 2

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Many brain regions lack clear borders. In particular when different species are compared, this may lead to some variations in the interpretation of anatomical projections. On top of this, one should also take into account that anatomy and physiology do not always match. For instance, the inspiratory neurons originally considered to be located in the pre-Bötzinger complex are actually distributed around the region of the pre-Bötzinger complex and are partially intermingled with expiratory neurons originally considered to be located in more caudal nuclei (Baertsch et al., 2019). When reading this review, please note that the use of anatomical names is to help orient oneself, but in reality, borders are often fuzzy. Genetic markers may help to define more homogeneous populations of neurons, and when this information was available, we mention that in the text and figures.

Given that the neuronal mechanisms of respiratory rhythm generation are evolutionary well conserved (Cinelli et al., 2013), inter-species differences are expected to be relatively minor (Kastner and Gauthier, 2008). Important exceptions, however, are the elongation of the pharyngeal region, and the development of complex muscle control of pharynx and mouth related to human speech (Duncker, 2001). Since neural control of speech is outside the scope of this review, this will not be further discussed.

Quiet breathing, or eupnea, is a rhythmic alternation between inspiration and passive expiration or post-inspiration (Albaiceta et al., 2005; Figure 1G). During periods with higher metabolic demand, hyperpnea occurs, which entails also active expiration (Pitts et al., 2015; Bellani et al., 2018; Figure 1D–E). It must be noted that the different respiratory muscles cover different aspects of the respiratory cycle. As a result, a clear distinction between passive and active expiration cannot be made. For example, during passive expiration, some of the expiratory muscles can be active, and active expiration encompasses passive elastic contractions as well. In humans, post-inspiration can contribute to longer periods of relatively constant air flow as required for speech or singing (MacLarnon and Hewitt, 1999; Watson et al., 2012; Salomoni et al., 2016; Figure 1F). Here, additional muscles become active that are not active during solely post-inspiration. Thus, to what extent the respiratory cycle within the brainstem can indeed be divided into rhythmogenic phases or whether these phases are just seen at the motor output remains topic of further research. As stated, we discuss in this review multiple mechanisms that modulate the rhythmicity of respiration when confronted with respiratory challenges, such as a change in air pressure or increase in CO₂ concentration (hypercapnia).

During regular breathing, the respiratory cycle is determined by brainstem central pattern generators. Inspiration is triggered by activity of neurons in the pre-Bötzinger complex, most of which fire in phase with inspiration and indirectly drive the inspiratory pump muscles (Smith et al., 1991; Guyenet and Wang, 2001; Moore et al., 2013; Del Negro et al., 2018; Yang and Feldman, 2018). Inspiration may be terminated by activation of the Kölliker-Fuse nucleus, and possibly also the postinspiratory complex can contribute to this (Dutschmann and Herbert, 2006; Anderson et al., 2016). Finally, the lateral parafacial nucleus that is silent during eupnea becomes active during active expiration (Pagliardini et al., 2011; Huckstepp et al., 2015; Del Negro et al., 2018; Figure 3). Without input from the brainstem, the spinal circuitry cannot organize respiration. It does contribute to sequential contraction of thoracic muscles to optimize the inflow of air by adjusting muscle control to body biomechanics (Marckwald, 1889; Porter, 1895; Ellenberger and Feldman, 1988; Butler et al., 2014; Shinozaki et al., 2019; Jensen et al., 2019).

Figure 3

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To adapt the depth of ventilation to the metabolic state, the blood gas balance is continuously monitored. At the same time, sensory systems of the airways and lungs, consisting of thermo-, mechano-, and chemoreceptors, survey ongoing respiration and detect environmental irritants and inflammatory mediators (Sant’Ambrogio et al., 1983; Lee and Yu, 2014). Muscle spindles give feedback on posture and respiratory muscle performance (Nakayama et al., 1998). Altogether, sensory feedback affects ventilatory control, and can trigger respiratory reflexes aimed at maintaining homeostasis upon adverse events. In addition, also hormones can modulate respiratory behavior.

Chemoreception

Chemoreceptors monitor the partial pressures of O₂ (pO₂) and CO₂ (pCO₂) in blood and cerebrospinal fluid. Since CO₂ reacts with water to form HCO₃^- and H⁺, increased pCO₂ leads to acidosis that can cause adverse effects on tissue structures, and may result in headaches, delirium and eventually coma (Cummins et al., 2020). Regulation of pCO₂ is therefore, next to that of pO₂, of great importance, and a major drive for the level of ventilation (Miescher-Rüsch, 1885; Haldane and Priestley, 1905). The concentrations of both gasses are continuously measured by peripheral chemoreceptors in the carotid bodies (Gonzalez et al., 1994; Milsom and Burleson, 2007; Cummins et al., 2020; Ortega-Sáenz and López-Barneo, 2020). The carotid bodies project mainly to the NTS (Claps and Torrealba, 1988; Finley and Katz, 1992; Mifflin, 1992; Zera et al., 2019), but also to the cVRG (Finley and Katz, 1992).

Acidosis can also be caused by inflammation, ischemia or defective acid containment. Consequently, acid sensing is not restricted to respiratory control and has evolved as an important property of neurons with unmyelinated and thinly myelinated fibers (Canning and Spina, 2009). Only those areas that sense pH changes and directly affect ventilation are considered to be central chemoreceptor areas. In this respect, most attention has been given to the retrotrapezoid nucleus, but also the NTS, locus coeruleus, raphe nuclei, lateral hypothalamus, and cerebellar fastigial nucleus are central chemoreceptor areas (Coates et al., 1993; Nattie, 1999; Nattie and Li, 2002; Xu and Frazier, 2002; Putnam et al., 2004; Guyenet et al., 2008; Dean and Putnam, 2010; Li et al., 2013; Figure 4A).

Figure 4

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Cough and expiration reflexes

Coughing is a vital action to clear the airways. Coughing involves first inspiration, then obstruction of airways to build up pressure, and subsequent explosive expulsion of air. Ineffective cough reflexes, for example in patients with dementia, can lead to lethal aspiration pneumonia (Widdicombe, 1995; Mutolo, 2017; Sykes and Morice, 2021). Inversely, the relatively common condition of chronic cough, affecting more than 5% of the adult population, is thought to be caused by hypersensitivity to airway stimulation (Morice et al., 2020).

The cough reflex is typically triggered by stimulation of the cough receptors and possibly also by activation of C fibers in the airways (Ludlow, 2015; Mutolo, 2017). Mechanical stimulation of the vocal cords can trigger the expiration reflex, which resembles cough without the initial inspiration (Korpas and Jakus, 2000; Sant’Ambrogio and Widdicombe, 2001; Tatar et al., 2008; Ludlow, 2015).

Stimulation of irritant receptors in the upper airways can evoke a cough reflex via activation of the paratrigeminal nucleus, and this reflex can be suppressed by the submedial thalamic nucleus and the upstream ventrolateral orbital cortex (Mazzone et al., 2020). In the periaqueductal gray, the excitatory drive from the paratrigeminal nucleus and the inhibitory input from the ventrolateral orbital cortex come together (McGovern et al., 2015b). The periaqueductal gray is hence an important intermediate between the forebrain and the cVRG (Holstege, 1989; Subramanian et al., 2008; Chen et al., 2022). The cVRG itself is essential for the cough reflex (Mutolo, 2017; Cinelli et al., 2020), as it can activate both expiratory motor neurons in the thoracic spinal cord, controlling abdominal muscles, and in the ambiguus nucleus, controlling laryngeal muscles (Figure 5F).

Figure 5

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Stimulation of the lower airways or the lungs activates RAR relay neurons in the NTS. These neurons receive also input from various other sources that can contribute to suppression or facilitation of coughing (Mutolo, 2017). Thalamocortical loops can further modulate coughing and exert voluntary control (Ando et al., 2016). Like the paratrigeminal nucleus, the NTS innervates the cVRG (Gerrits and Holstege, 1996). In addition, the NTS affects also the phrenic nucleus, directly as well as indirectly via the rVRG (Ezure and Tanaka, 1996; Wu et al., 2017). These connections are complemented with direct output to the ambiguus nucleus from both the paratrigeminal nucleus and the NTS (Caous et al., 2001; de Sousa Buck et al., 2001; Kawai, 2018; Figure 5F).

Although direct projections from central pattern generators and respiratory sensory areas to motor neurons do exist, it is likely that indirect pathways via premotor areas are more prominent.

Of the limbic system, the amygdala and hypothalamus are involved in subconscious control of respiration. The former is particularly important for handling fear responses, for example, as a consequence of high levels of CO₂, while the latter is especially important for coupling with the endocrine system, as well as for peptidergic modulation of respiration. The lateral hypothalamus is a central chemoreceptor area, and – although part of the limbic system – discussed in the section on central chemoreception.

On top of the central pattern generators, (pre)motor areas, sensory areas and limbic system, also other brain regions can affect specific aspects of respiration, often to adapt respiration to other behaviors. In fact, few brain regions are completely unrelated to respiration. In the following section, we restrict ourselves to those brain regions of which a non-voluntary respiratory function has been clearly described.

Despite their widespread connectivity and importance for motor control (Roseberry et al., 2016; Lee et al., 2020; Quartarone et al., 2020), the basal ganglia are not typically considered to be part of the respiratory control network. Possibly the best-known consequence of basal gangliar dysfunction is Parkinson’s disease, caused by progressive degeneration of dopaminergic neurons in the substantia nigra (Kalia and Lang, 2015). Patients with Parkinson’s disease can be confronted with respiratory problems, but these may be attributed to degeneration of respiratory muscles, and therefore not directly to respiratory control (Guedes et al., 2012; Baille et al., 2018; Guilherme et al., 2021). Patients with Parkinson’s disease may also experience sleep-disturbed breathing or dyspnea (Docu Axelerad et al., 2021). With a prevalence of 12%, dyspnea is a relatively rare symptom of Parkinson’s disease (Barone et al., 2009), and its cause is unclear (Docu Axelerad et al., 2021). Overall, the basal ganglia, and the substantia nigra in particular, therefore, do not seem to play a major role in respiratory control.

Nevertheless, there are anatomical connections between the substantia nigra and the respiratory control centers, including a direct pathway to the pre-Bötzinger complex (Yang et al., 2020). In a rat model for Parkinson’s disease, modulation of the retrotrapezoid nucleus by the substantia nigra indirectly, via the periaqueductal gray, could contribute to respiratory control (Lima et al., 2018). Given the uncertainty of the impact of the basal ganglia on respiratory control, these outputs of the substantia nigra have been hypothesized to provide respiratory control centers with information on other ongoing movements, to facilitate respiratory control into the behavioral context of the animal (Yang et al., 2020). For this reason, we did not further consider the basal ganglia as control center for the subconscious regulation of respiration.

Breathing is rather unique among the autonomic functions as it can be subjected to volitional control, modulated by the emotional state, adapted to other ongoing behaviors, and vital for vocalizations and human speech. It is quite likely that the cerebral cortex plays an important role in these functions (Herrero et al., 2018). Unlike lesions of the subcortical, and in particular of the medullar respiratory centers, lesions of cortical respiratory areas do not abolish respiration (Ramirez et al., 2011). The anatomical aspects of cortical modulation of respiration have received relatively little attention, and we consider the integration of the thalamocortical system into the anatomical scheme of Figure 7 an important future task.

Figure 7

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There is early evidence for a direct projection from the cat motor cortex to the phrenic nucleus, bypassing the medullary respiratory circuitry (Rikard-Bell et al., 1985). In addition, a wide spectrum of projections from different cortical areas targets subcortical respiratory control areas, with the most numerous projections targeting the periaqueductal gray and the Kölliker-Fuse nucleus, and less abundant projections to the caudal raphe nucleus, Bötzinger and pre-Bötzinger complexes (Trevizan-Baú et al., 2021a). In this study, the Kölliker-Fuse nucleus was predominantly targeted from the (facial) somatosensory, endopiriform and rhinal cortices, and the periaqueductal gray from the insular, cingulate, motor, pre- and infralimbic cortices. In addition, the NTS receives a direct projection form the insular cortex (Torrealba and Müller, 1996; Gasparini et al., 2020).

In the context of the present review, especially the function of the insular cortex is relevant. It appears to be the prime cortical target area of visceral input, and it has a viscerotopic organization (Cechetto and Saper, 1987; Bagaev and Aleksandrov, 2006; Livneh and Andermann, 2021). EEG recordings of the insular cortex revealed coherence with breathing (Herrero et al., 2018). Depending on the location within the insular cortex, microstimulation could either increase or decrease the respiratory rate (Bagaev and Aleksandrov, 2006), suggesting that the insular cortex can affect respiration in response to vagal sensory input.

The cerebellum is composed of a cortex surrounding the fastigial, interposed and dentate nuclei. The output of the cerebellar cortex is formed by Purkinje cells that predominantly target the cerebellar nuclei (Voogd and Glickstein, 1998), although direct connections to the vestibular nuclei, locus coeruleus, and lateral and medial parabrachial nuclei exist as well (Zeeuw and Berrebi, 1995; Sadakane et al., 2000; Sugihara et al., 2009; Schwarz et al., 2015; Hashimoto et al., 2018; Novello et al., 2022). From the cerebellar nuclei, there are projections back to the cerebellar cortex (Tolbert et al., 1977; Gao et al., 2016), inhibitory projections to the inferior olive (Voogd and Glickstein, 1998), and excitatory projections to the MDJ (De Zeeuw and Ruigrok, 1994; Wang et al., 2022) and many brain regions relevant for respiratory control.

Strikingly, there are no direct connections to the phrenic nucleus (Lois et al., 2009), nor to the pre-Bötzinger complex (Yang et al., 2020). Instead, diaphragmatic activity can be affected by a direct projection to the premotor rVRG (Gaytán and Pásaro, 1998). Although there are direct projections from the cerebellum to the trigeminal motor nucleus, affecting upper airway muscles (Judd et al., 2021), facial nucleus (Moolenaar and Rucker, 1976; Fujita et al., 2020), and hypoglossal nucleus (Guo et al., 2020; Judd et al., 2021), these direct projections to motor nuclei are typically relatively sparse so that indirect projections, for example, via the reticular formation, are probably much more abundant (Novello et al., 2022).

Other cerebellar projections that can be relevant for respiratory control target the Kölliker-Fuse nucleus (Fujita et al., 2020), locus coeruleus (Teune et al., 2000; Schwarz et al., 2015), dorsal raphe nuclei (Teune et al., 2000; Çavdar et al., 2018b), periaqueductal gray (Teune et al., 2000; Frontera et al., 2020; Fujita et al., 2020; Judd et al., 2021), lateral and paraventricular hypothalamus (Dietrichs et al., 1994; Zhu et al., 2006). Many of these areas, in particular the Kölliker-Fuse nucleus, have profound projections to medullary respiratory circuit, so that these projections can explain how the cerebellum can affect respiratory control.

Despite the absence of strong pathways from the cerebellum to the respiratory pattern generators and motor nuclei, cerebellar activity can profoundly modulate respiration. Functional brain imaging of healthy human subjects revealed that the cerebellum is particularly active during coping with respiratory challenges: broad activation during hypoxia and slow breathing (Critchley et al., 2015), and specific activation in lobules V and VI during hypercapnia (Colebatch et al., 1991; Kastrup et al., 1999). Also the cerebellar nuclei are active during hypercapnia and hypoxia (McKay et al., 2010), as well as during volitional expiration (Ramsay et al., 1993). Changes in environmental air pressure can trigger cerebellar activity as well (Isaev et al., 2002; Raux et al., 2013; Figure 6G–J).

The notion that the cerebellum is particularly relevant for deviating from rhythmic breathing is corroborated by the finding that mice suffering from a complete lack of output from the cerebellar cortex or from a partial loss of cerebellar output neurons display overly regular breathing at rest (Liu et al., 2020; Taylor et al., 2022; Figure 6F). Stimulation of the fastigial nucleus in cats can affect phrenic nerve activity, and in particular terminate expiratory activity when stimulated during expiration (Zhang et al., 1999), analogous to optogenetic stimulation experiments of Purkinje cells (Romano et al., 2020; Figure 6E). And indeed, Lurcher mice that suffer from a complete loss of Purkinje cells during their development, demonstrated impaired responses to hypercapnic and hypoxic challenges (Calton et al., 2014; Calton et al., 2016). Neuronal activity of the cerebellar cortex and the fastigial nucleus is linked to respiration (Lutherer et al., 1989; Gruart and Delgado-García, 1992; Cao et al., 2012b; Lu et al., 2013; Romano et al., 2020; Figure 6C–D). At rest, modulation of the activity of Purkinje cell occurs without phase lead or lag relative to the respiratory cycle (Romano et al., 2020), and one could speculate that the cerebellum does not only act to adapt respiration to ongoing behavior, but also facilitates adaptation of other behavior to respiration, in line with observations in cerebellar patients (Ebert et al., 1995).

The cerebellum may, in addition, have a particular role in the regulation of breathing during sleep, which includes different stages with different respiratory and oculomotor dynamics (Canto et al., 2017; De Zeeuw and Canto, 2022; Pujol et al., 2022). Indeed, when shifting from awake to subconscious behavior and vice-versa, different brain structures such as cerebellum, hippocampus and amygdala, are dynamically activated and de-activated in line with changes in breathing (Pujol et al., 2022). Accordingly, the impact of sleep on breathing and its role in the development of diurnal respiratory failure in patients suffering from hypoventilation and/or cerebellar disorders can be overlooked (Piper and Yee, 2014; Canto et al., 2017). It remains to be elucidated which sets of mechanisms are involved in this process, but it should be noted that sleep by itself does not only reduce respiratory drive, but also diminishes responsiveness to hypoxia and hypercapnia. For example, acute increases in CO₂ during rapid eye movement sleep can initiate the process of bicarbonate retention, which further depresses ventilatory responsiveness (Piper and Yee, 2014) and which in turn can affect activity in the cerebellar nuclei (Parsons et al., 2001; Martino et al., 2007).

Cerebellar pathology

Although the role of the cerebellum in respiratory control is not yet settled in clinical settings, several lines of evidence indicate a specific role in respiratory control. For instance, in some developmental disorders, cerebellar abnormalities and respiratory dysfunction co-occur. Arguably, the most explicit example is sudden infant death syndrome (SIDS), the unexplained abrupt death of infants, typically during sleep, and most likely related to respiratory problems (Kelly et al., 1986; Kinney and Thach, 2009). Several studies link SIDS to cerebellar malformations. For instance, post-mortem analyses relate SIDS to the presence of a wide external granular layer, which is a sign of developmental delay of the cerebellum (Cruz-Sánchez et al., 1997; Lavezzi et al., 2007a). Also malformed and displaced Purkinje cells were observed in several cases (Lavezzi et al., 2013; Matschke et al., 2020). Additionally, the dentate-olivary system can be affected in SIDS (Lavezzi et al., 2007b). Note that malformations of the cerebellum and related structures have been demonstrated only in a subset of cases, as SIDS can have multiple causes (Kinney and Thach, 2009; Figure 8B).

Figure 8

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Nevertheless, respiratory deficiencies and prolonged dependency on assisted or even mechanical ventilation are frequently observed after cerebellar damage (Chen et al., 2005; Tsitsopoulos et al., 2012; Lee et al., 2013; Arnone et al., 2017). Relatively mild aberrations in respiratory functions were also noted in different types of spinocerebellar ataxia (Sriranjini et al., 2010), while in a mouse model for spinocerebellar ataxia type 7 (SCA7) abnormal respiratory patterns were recorded (Figure 8B–C). Distinct types of spinocerebellar ataxia can affect various brain regions relevant for subconscious control of respiration (Figure 8B, Supplementary file 1). Finally, chronic cough may be one of the earliest symptoms of cerebellar ataxia with neuropathy and vestibular areflexia syndrome (CANVAS), and manifests in the absence of any perceived lung abnormalities (Infante et al., 2018).

Lesions, e.g., as a consequence of hemorrhage, at different levels of the brain can result in different patterns of disordered breathing (Figure 8A).

A bilateral hemispheric or diencephalic lesion can lead to Cheyne-Stokes respiration (Brown and Plum, 1961). This is characterized by an undulating pattern of breathing with increasing depth and frequency alternated with waves of shallow, slower breathing (Lorenzi-Filho et al., 1999).

Apneustic breathing, characterized by the absence or extreme delay of the inspiration to expiration switch, has originally been described as the consequence of a lesion at the level of the Kölliker-Fuse nucleus or the surrounding area (Marckwald, 1890; Lumsden, 1923; Caille et al., 1981; Mador and Tobin, 1990).

Biot’s respiration is characterized by irregular periods of apnea alternated by several breaths of identical depth (Farney et al., 2003; Wijdicks, 2007). Although, the irregularity of this breathing pattern has led to the more common term ‘ataxic breathing’, the cerebellum is not primarily involved in this type of respiration (Summ et al., 2022). However, Biot’s respiration pattern can result after a lesion in the medulla (Summ et al., 2022). Biot’s respiration can also be a complication of long-term opioid use (Farney et al., 2003).

Finally, a respiratory arrest can result after damage to the pre-Bötzinger complex or the upper spinal cord (Ramirez et al., 1998; Schwarzacher et al., 2011; Arora et al., 2012).

Animal experiments have demonstrated that a lack of cerebellar output can lead to hyperregular respiration (Liu et al., 2020; Taylor et al., 2022). Cerebellar patients, however, can also display the opposite and present with irregular respiration (Ebert et al., 1995). Both, hyperregular as well as irregular breathing, can be the consequence of impaired coordination of respiration with ongoing behavior, as described for instance by Ebert et al., 1995.

While each of these brain areas result in a specific type of respiratory pattern. It must be noted that a specific respiratory pattern can have multiple causes such as metabolic or cardiopulmonary disorders. In addition, also peripheral diseases, like COPD (Jolley et al., 2009), can cause disordered breathing. COPD is a chronic obstructive pulmonary condition characterized by abnormalities, especially narrowing of the small airways, of the lung which leads to limitation of the airflow.

Throughout this review, we have discussed several behaviors that are tightly coupled to respiration, such as those involved in airway clearance, feeding, and vocalization, as well as adjusting the rate of ventilation to metabolic demands. In addition, also postural control and cardiovascular function are linked to respiration. All pump muscles have dual functions; they do not only enable ventilation but control also posture and movements (Ebert et al., 2000). The coordination between these different tasks can be affected in cerebellar patients, displaying regular breathing at rest, but arhythmic breathing during arm movements (Ebert et al., 1995).

It is an attractive idea to have one or a few central pattern generator areas that control the respiratory rhythm (Moore et al., 2013; Anderson and Ramirez, 2017). In particular, the pre-Bötzinger complex is essential in this respect, as inspiration depends on it (Smith et al., 1991; Ramirez et al., 1998; Gray et al., 2001; Tan et al., 2008; Schwarzacher et al., 2011; Ashhad and Feldman, 2020; Dhingra et al., 2020). In this view, projections organized in a hierarchical fashion pass the respiratory control from the pattern generator(s) to the respiratory motor neurons. Throughout this review we summarize, however, that many other brain regions, including areas like the cerebellum and the limbic system that are not classically considered to be respiratory areas, can affect respiratory control (Figure 8). As all these areas are interconnected (Figure 7), the picture of an integrated network emerges. Thus, depending on specific behavioral needs, these other brain regions may modulate or even overrule the central pattern generators. This does not contradict the idea of central pattern generators being the main players that control rhythmic respiration, but postulates that these pattern generators together with their downstream areas are themselves embedded in a larger network that allows for flexibility within the respiratory control system. We therefore suggest to view the respiratory control system primarily as an integrated network, rather than a hierarchical system. Consequently, we believe that integration of behavioral conditions will add to the pathogenesis of respiratory disease.

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