Introduction

Breathing is an essential function for humans during every waking and sleeping moment to provide movement of air in and out of the lungs (1-3). Our oxygen demands are dynamic and constantly changing depending on our activity level, emotional state, health status, and current behaviors. Because of this, the brain must constantly ensure that our breathing is appropriately matched to our physiological state and behavior. For example, our breathing rate and/or volume changes in anticipation of altered needs for gas exchange and tissue oxygenation during exercise or other physical activities (4). This feed-forward control is critical for maintaining homeostasis because there is no known mechanism for sensing gas exchange in the muscle or lungs. Breathing changes with emotional states as well, as the feelings of stress and fear can cause hyperventilation (5-7). Although the basic pattern of respiration (inspiration, post-inspiration, and expiration phases) is generated by neurons in the brainstem and transmitted to respiratory muscles via spinal circuits (1, 2, 8), these neurons are influenced by other brain regions in order to ensure that breathing is appropriate for the current situation.

Breathing, unlike other autonomic processes such as heart rate and blood pressure, can be modulated voluntarily in addition to autonomically (9-11). For example, singers and musicians that play wind instruments need precise control over their breathing to produce the correct notes and tones. Mindfulness exercises such as meditation and yoga utilize deliberate and precise breathing methods to elicit calming responses from the body, including lowering blood pressure and heart rate. Competitive weightlifters are among a variety of athletes that use methodic breathing techniques such as hyperventilating before their lift to provide sympathetic activation to maximize strength during their lift. Swimmers pace their breathing to ensure that they do not inadvertently inhale water. Thus, intentionally pacing respiration or modulating breathing volume is a tool that humans and animals use to control their own physiology.

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The forebrain is important for the planning and execution of movements, sensory processing, regulating sleep wake states and behavioral responses to emotions such as stress and fear (5, 7). Each of these functions can have an impact on breathing. For example, fear is linked with a variety of respiratory changes- you may gasp if you are startled, you might find yourself holding your breath when scared, or even hyperventilating as your body prepares its fight or flight response. Sleep/wake states strongly influence the control of breathing, with important consequences if this relationship is dysfunctional, such as sleep apnea, congenital central hypoventilation syndrome, sudden infant death syndrome, or sudden unexpected death in epilepsy. Thus, we propose that the forebrain may be important for ensuring that breathing matches current and anticipated emotional, behavioral, and physiological needs. However, the circuits and mechanisms by which the forebrain exerts control over breathing are only partly understood. This review will summarize anatomical and functional evidence implicating forebrain regions in the control of breathing. These regions include the cerebral cortex, extended amygdala, hippocampus, hypothalamus, and thalamus (Figure 1). We will also point out areas where additional research is needed to better understand the specific roles of forebrain regions in the control of breathing.

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