Decision letter for "Forebrain projection neurons target functionally diverse respiratory control areas in the midbrain, pons and medulla oblongata"

AbstractEupnea is generated by neural circuits located in the ponto-medullary brainstem, but can be modulated by higher brain inputs which contribute to volitional control of breathing and the expression of orofacial behaviors, such as vocalization, sniffing, coughing and swallowing. Surprisingly, the anatomical organization of descending inputs that connect the forebrain with the brainstem respiratory network remains poorly defined. We hypothesized that descending forebrain projections target multiple distributed respiratory control nuclei across the neuraxis. To test our hypothesis, we made discrete unilateral microinjections of the retrograde tracer Cholera toxin subunit B (CT-B) in the midbrain periaqueductal gray (PAG), the pontine Kölliker-Fuse nucleus (KFn), the medullary Bötzinger complex (BötC), pre-Bötzinger complex (pre-BötC) or caudal midline raphé nuclei. We quantified the regional distribution of retrogradely-labeled neurons in the forebrain 12-14 days post-injection. Overall, our data reveals that descending inputs from cortical areas predominantly target the PAG and KFn. Differential forebrain regions innervating the PAG (prefrontal, cingulate cortices, and lateral septum) and KFn (rhinal, piriform, and somatosensory cortices) imply that volitional motor commands for vocalization are specifically relayed via the PAG, while the KFn may receive commands to coordinate breathing with other orofacial behaviors (e.g. sniffing, swallowing). Additionally, we observed that the limbic or autonomic (interoceptive) systems are connected to broadly distributed downstream bulbar respiratory networks. Collectively, these data provide a neural substrate to explain how volitional, state-dependent, and emotional modulation of breathing is regulated by the forebrain.

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Vagal afferents modulate cytokine-mediated respiratory control at the neonatal medulla oblongata

Respiratory Physiology & Neurobiology ◽

10.1016/j.resp.2011.03.003 ◽

2011 ◽

Vol 178 (3) ◽

pp. 458-464 ◽

Cited By ~ 53

Author(s):

Kannan V. Balan ◽

Prabha Kc ◽

Zana Hoxha ◽

Catherine A. Mayer ◽

Christopher G. Wilson ◽

...

Keyword(s):

Medulla Oblongata ◽

Respiratory Control ◽

Vagal Afferents

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Transitioning between preparatory and precisely sequenced neuronal activity in production of a skilled behavior

eLife ◽

10.7554/elife.43732 ◽

2019 ◽

Vol 8 ◽

Cited By ~ 4

Author(s):

Vamsi K Daliparthi ◽

Ryosuke O Tachibana ◽

Brenton G Cooper ◽

Richard HR Hahnloser ◽

Satoshi Kojima ◽

...

Keyword(s):

Calcium Imaging ◽

Motor Preparation ◽

Projection Neurons ◽

Neuronal Populations ◽

Premotor Neurons ◽

Preparatory Activity ◽

Cell Type Specific ◽

Functionally Diverse ◽

Neural Sequences ◽

The Brain

Precise neural sequences are associated with the production of well-learned skilled behaviors. Yet, how neural sequences arise in the brain remains unclear. In songbirds, premotor projection neurons in the cortical song nucleus HVC are necessary for producing learned song and exhibit precise sequential activity during singing. Using cell-type specific calcium imaging we identify populations of HVC premotor neurons associated with the beginning and ending of singing-related neural sequences. We characterize neurons that bookend singing-related sequences and neuronal populations that transition from sparse preparatory activity prior to song to precise neural sequences during singing. Recordings from downstream premotor neurons or the respiratory system suggest that pre-song activity may be involved in motor preparation to sing. These findings reveal population mechanisms associated with moving from non-vocal to vocal behavioral states and suggest that precise neural sequences begin and end as part of orchestrated activity across functionally diverse populations of cortical premotor neurons.

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Transitioning between preparatory and precisely sequenced neuronal activity in production of a skilled behavior

10.1101/481960 ◽

2018 ◽

Cited By ~ 1

Author(s):

Vamsi K. Daliparthi ◽

Ryosuke O. Tachibana ◽

Brenton G. Cooper ◽

Richard H.R. Hahnloser ◽

Satoshi Kojima ◽

...

Keyword(s):

Calcium Imaging ◽

Motor Preparation ◽

Projection Neurons ◽

Neuronal Populations ◽

Premotor Neurons ◽

Preparatory Activity ◽

Cell Type Specific ◽

Functionally Diverse ◽

Neural Sequences ◽

The Brain

ABSTRACTPrecise neural sequences are associated with the production of well-learned skilled behaviors. Yet, how neural sequences arise in the brain remains unclear. In songbirds, premotor projection neurons in the cortical song nucleus HVC are necessary for producing learned song and exhibit precise sequential activity during singing. Using cell-type specific calcium imaging we identify populations of HVC premotor neurons associated with the beginning and ending of singing-related neural sequences. We discovered neurons that bookend singing-related sequences and neuronal populations that transition from sparse preparatory activity prior to song to precise neural sequences during singing. Recordings from downstream premotor neurons or the respiratory system suggest that pre-song activity may be involved in motor preparation to sing. These findings reveal population mechanisms associated with moving from non-vocal to vocal behavioral states and suggest that precise neural sequences begin and end as part of orchestrated activity across functionally diverse populations of cortical premotor neurons.

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