Neuropeptides and small-molecule amine transmitters: cooperative signaling in the nervous system

Eiden, Lee E.; Hernández, Vito S.; Jiang, Sunny Zhihong; Zhang, Limei

doi:10.1007/s00018-022-04451-7

Cited by 16 publications

(11 citation statements)

References 273 publications

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“…Cotransmission is ubiquitous and a likely contributor to distinctions between modulatory neuron activation and bath-application. Co-transmitter complements include neuropeptide plus classical and/or amine small molecule transmitters, or multiple small molecule transmitters (Nusbaum et al, 2017;Nässel, 2018;Trudeau and El Mestikawy, 2018;Svensson et al, 2019;Eiden et al, 2022). One or more neuropeptides plus a small molecule transmitter is common in modulatory PNs targeting CPGs (Figure 1A; Schlegel et al, 2016;Nusbaum et al, 2017;Nässel, 2018).…”

Section: Co-transmissionmentioning

confidence: 99%

“…Although neuromodulators are often considered to act via relatively non-specific "volume transmission, " it is becoming increasingly clear that there is also spatial constraint of neuromodulator actions (Disney and Higley, 2020;Liu et al, 2021;Nässel and Zandawala, 2022). Localization of reuptake and degradative machinery, and constrained release/receptor distributions beyond anatomically-defined synapses can limit the sphere of neuromodulator influence (Nusbaum, 2002;Disney and Higley, 2020;Liu et al, 2021;Eiden et al, 2022).…”

Section: Spatial Segregation Of Co-transmitter Actionsmentioning

confidence: 99%

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Neural circuit regulation by identified modulatory projection neurons

Blitz

2023

Front. Neurosci.

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Rhythmic behaviors (e.g., walking, breathing, and chewing) are produced by central pattern generator (CPG) circuits. These circuits are highly dynamic due to a multitude of input they receive from hormones, sensory neurons, and modulatory projection neurons. Such inputs not only turn CPG circuits on and off, but they adjust their synaptic and cellular properties to select behaviorally relevant outputs that last from seconds to hours. Similar to the contributions of fully identified connectomes to establishing general principles of circuit function and flexibility, identified modulatory neurons have enabled key insights into neural circuit modulation. For instance, while bath-applying neuromodulators continues to be an important approach to studying neural circuit modulation, this approach does not always mimic the neural circuit response to neuronal release of the same modulator. There is additional complexity in the actions of neuronally-released modulators due to: (1) the prevalence of co-transmitters, (2) local- and long-distance feedback regulating the timing of (co-)release, and (3) differential regulation of co-transmitter release. Identifying the physiological stimuli (e.g., identified sensory neurons) that activate modulatory projection neurons has demonstrated multiple “modulatory codes” for selecting particular circuit outputs. In some cases, population coding occurs, and in others circuit output is determined by the firing pattern and rate of the modulatory projection neurons. The ability to perform electrophysiological recordings and manipulations of small populations of identified neurons at multiple levels of rhythmic motor systems remains an important approach for determining the cellular and synaptic mechanisms underlying the rapid adaptability of rhythmic neural circuits.

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Section: Co-transmissionmentioning

confidence: 99%

Section: Spatial Segregation Of Co-transmitter Actionsmentioning

confidence: 99%

Neural circuit regulation by identified modulatory projection neurons

Blitz

2023

Front. Neurosci.

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“…Note the clearly visible allocortical feature, three layers of the NLOT clearly visible. Da and Db show two magnocellular neurons, single-stained within the SON, that they emitted 3 main axons from soma or proximal dendrites and coursed medially (1), dorsally (2) and laterally (3) that could be followed and reconstructed using adjacent sections (see Fig. 4A).…”

Section: Figure 3 Anatomical Relationship and Interconnections Betwee...mentioning

confidence: 99%

“…Neuropeptides acting as neurotransmitters in the brain participate in circuits which monitor multiple environmental inputs, and access brain state-related information, in order to produce highly integrated responses that are appropriately tuned to the specifics of a given situation requiring motor decision-making (action) (1) . An area of research relevant to the general question of how multiple-circuit integration leads to specific behaviors occurs, is the study of the microanatomy, neurochemistry, and cellular and behavioral functions of vasopressinergic magnocellular neurosecretory neurons (AVPMNNs) of the mammalian brain.…”

Section: Introductionmentioning

confidence: 99%

Nucleus of the lateral olfactory tract (NLOT): a hub linking water homeostasis-associated SON-AVP circuit and neocortical regions to promote social behavior under osmotic challenge

Hernández‐Pérez

Hernández

Zetter

et al. 2022

Preprint

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Homeostatic challenges increase the drive for social interaction. The neural activity that prompts this motivation remains poorly understood. Here, we identify direct projections from hypothalamic supraoptic nucleus (SON) to the cortico-amygdalar nucleus of the lateral olfactory tract (NLOT). Dual in situ hybridization (DISH) with probes for PACAP, and VGLUT1, VGLUT2, V1a and V1b revealed a population of vasopressin-receptive PACAPergic neurons in NLOT layer 2 (NLOT2). Water deprivation (48 hours, WD48) increased sociability compared to euhydrated subjects, assessed with the three-chamber social interaction test (3CST). Fos expression immunohistochemistry showed NLOT and its main efferent regions had further increases in rats subjected to WD48+3CST. These regions strongly expressed PAC1 mRNA. Microinjections of AVP into NLOT produced similar changes in sociability to water deprivation, and these were reduced by co-injection of V1a or V1b antagonists along with AVP. We conclude that during challenge to water homeostasis, there is a recruitment of a glutamatergic-multi-peptidergic cooperative circuit that promotes social behavior.

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“…Neuropeptides acting as neurotransmitters in the brain participate in circuits that monitor multiple environmental inputs, and access brain state‐related information, to produce highly integrated responses that are appropriately tuned to the specifics of a given situation requiring motor decision‐making (action) 1 . An area of research, relevant to the general question of how multiple‐circuit integration leads to specific behaviors occurs, is the study of the microanatomy, neurochemistry, and cellular and behavioral functions of vasopressinergic magnocellular neurosecretory neurons (AVPMNNs) of the mammalian brain.…”

Section: Introductionmentioning

confidence: 99%

Nucleus of the lateral olfactory tract: A hub linking the water homeostasis‐associated supraoptic nucleus‐arginine vasopressin circuit and neocortical regions to promote social behavior under osmotic challenge

Hernández‐Pérez

Hernández

Zetter

et al. 2022

J Neuroendocrinology

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Homeostatic challenges may alter the drive for social interaction. The neural activity that prompts this motivation remains poorly understood. In the present study, we identify direct projections from the hypothalamic supraoptic nucleus to the cortico‐amygdalar nucleus of the lateral olfactory tract (NLOT). Dual in situ hybridization with probes for pituitary adenylate cyclase‐activating polypeptide (PACAP), as well as vesicular glutamate transporter (VGLUT)1, VGLUT2, V1a and V1b, revealed a population of vasopressin‐receptive PACAPergic neurons in NLOT layer 2 (NLOT2). Water deprivation (48 h, WD48) increased sociability compared to euhydrated subjects, as assessed with the three‐chamber social interaction test (3CST). Fos expression immunohistochemistry showed NLOT and its main efferent regions had further increases in rats subjected to WD48 + 3CST. These regions strongly expressed PAC1 mRNA. Microinjections of arginine vasopressin (AVP) into the NLOT produced similar changes in sociability to water deprivation, and these were reduced by co‐injection of V1a or V1b antagonists along with AVP. We conclude that, during challenge to water homeostasis, there is a recruitment of a glutamatergic‐multi‐peptidergic cooperative circuit that promotes social behavior.

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Neuropeptides and small-molecule amine transmitters: cooperative signaling in the nervous system

Cited by 16 publications

References 273 publications

Neural circuit regulation by identified modulatory projection neurons

Neural circuit regulation by identified modulatory projection neurons

Nucleus of the lateral olfactory tract (NLOT): a hub linking water homeostasis-associated SON-AVP circuit and neocortical regions to promote social behavior under osmotic challenge

Nucleus of the lateral olfactory tract: A hub linking the water homeostasis‐associated supraoptic nucleus‐arginine vasopressin circuit and neocortical regions to promote social behavior under osmotic challenge

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