Differential Ascending Projections From the Male Rat Caudal Nucleus of the Tractus Solitarius: An Interface Between Local Microcircuits and Global Macrocircuits

Abstract

To integrate and broadcast neural information, local microcircuits and global macrocircuits interact within certain specific nuclei of the central nervous system. The structural and functional architecture of this interaction was determined for the caudal nucleus of the tractus solitarius (NTS) at the level of the area postrema (AP), a relay station of peripheral viscerosensory information that is processed and conveyed to brain regions concerned with autonomic-affective and other interoceptive reflexive functions. Axon collaterals of most small NTS cells (soma <150 μm2) establish excitatory or inhibitory local microcircuits likely to control the activity of nearby NTS cells and to transfer peripheral signals to efferent projection neurons. At least two types of cells that constitute efferent pathways from the caudal NTS (cNTS) were distinguished: (1) a greater numbers of small cells, seemingly forming local excitatory microcircuits via recurrent axon collaterals, that project specifically and unidirectionally to the lateral parabrachial nucleus; and (2) a much smaller numbers of cells likely to establish multiple global connections, mostly via the medial forebrain bundle (MFB) or the dorsal longitudinal fascicle (DLF), with a wide range of brain regions, including the ventrolateral medulla (VLM), hypothalamus, central nucleus of the amygdala (ACe), bed nucleus of the stria terminalis (BNST), spinal cord dorsal horn, brainstem reticular formation, locus coeruleus (LC), periaqueductal gray (PAG) and periventricular diencephalon (including the epithalamus). The evidence presented here suggests that distinct cNTS cell types distinguished by projection pattern and related structural and functional features participate differentially in the computation of viscerosensory information and coordination of global macro-networks in a highly organized manner.

Aldosterone-sensitive HSD2 neurons in mice

“…Cre-conditional tracing eliminates these confounds because only neurons that express Hsd11b2 at or after the time of AAV injection can produce the genetically encoded tracer, so labeled axons emit exclusively from HSD2 neurons. That HSD2 neurons provide minimal (or no) projections within the NTS places them in a previously described class of NTS neurons that lack local, axon-collateral projections (Kawai and Senba, 1996; Kawai, 2018), with important functional implications for HSD2 neurons and, by extension, aldosterone. That is, whether or not HSD2 neurons influence sodium taste detection or any autonomic reflexes, it is highly unlikely that they exert such influence directly within the brain’s first-order gustatory and viscerosensory nucleus, the NTS.…”

Spatiotemporal Structure and Dynamics of Spontaneous Oscillatory Synchrony in the Vagal Complex

“…However, all or a portion of the two oscillator activities would vary according to consciousness level or quality (such as attention or learning) of animals or individuals. These two brainstem oscillators seem to orchestrate neuronal activities of not only the VC but also other wide-ranging brainstem neuronal groups, including catecholaminergic, cholinergic, and serotonergic systems (Kawai, 2018), through a phase-phase coupling mechanism, to perform specific physiological functions. The oscillatory synchrony and the ascending macrocircuits (Kawai, 2018) could represent functional and anatomic substrates for the presumed ascending reticular activating system including the bulbar reticular formation (Moruzzi and Magoun, 1949).…”

“…However, a neuronal population microenvironment close to an electrode tip differs extremely from other brain areas depending on the neuronal size and density. The VC consists mostly of small cells (Yoshioka et al, 2006; Negishi and Kawai, 2011); VC cell size (~10 μm in diameter) and density (~2.0 × 10 5 /mm 3 in numerical density) would make for a far more numerous and denser cell population near the recording electrode tip than in the cerebral cortex or hippocampus (Buzsaki, 2006; Kawai, 2018), allowing any unusual neuronal activity profiles to be revealed, as demonstrated in the present study. That is, recorded neuronal activities in the VC contained not only typical single- or multi-unit spikes but also longer duration LFP-like waves, and in occasion, high-amplitude potential waves (mostly polyphasic), possibly due to a reflection of synchronized activity produced by the spatially compact neuronal population (Figures 2, 3).…”

“…The dynamics of cardiorespiratory cross-frequency coupling revealed in the present study involving the development of synchrony from fluctuating noisy oscillations might have functional roles related to signal amplification and electrical signal transport to distant regions, rather than serving as passive reflections of neuronal activities resulting from cardiorespiratory rhythmogenesis. The cNTS provides divergent efferent systems up to forebrain regions including catecholaminergic and cholinergic neuronal groups (Kawai, 2018). The parasympathetic preganglionic neurons in the dorsal motor nucleus of the vagus send their axons a great length to reach the abdominal viscera (Ramon y Cajal, 1995).…”

Central afferents to the nucleus of the solitary tract in rats and mice

“…Axonal tracing studies have identified output projections from the NTS to a variety of regions in the upper brainstem and forebrain (Gasparini et al, 2019; Geerling & Loewy, 2006b; Herbert et al, 1990; Kawai, 2018; Ricardo & Koh, 1978; Ter Horst, de Boer, Luiten, & van Willigen, 1989). Prominent targets include the parabrachial nucleus (Herbert et al, 1990; Herbert & Saper, 1990), ventrolateral periaqueductal gray matter (Kawai, 2018), hypothalamus (Ter Horst et al, 1989), CeA, and ventrolateral BST (Bienkowski & Rinaman, 2013; Geerling & Loewy, 2006b; Ricardo & Koh, 1978; Shin et al, 2008; Sofroniew, 1983; Terenzi & Ingram, 1995).…”