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Neuroanatomical and Functional Relationship Between Parvocellular and Magnocellular Oxytocin and Vasopressin Neurons

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Book cover Neuroanatomy of Neuroendocrine Systems

Part of the book series: Masterclass in Neuroendocrinology ((MANEURO,volume 12))

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Abstract

Hypothalamic neuroendocrine cells that synthesize oxytocin (OT) and vasopressin (AVP) can be categorized into two major cell types, namely magnocellular and parvocellular neurons. In addition to the previously known differences in morphology, connectivity, and electrophysiological properties, recent studies highlight fundamentally different functions and genetic compositions of these cells. Parvocellular OT neurons have recently been implicated in pain perception and processing, regulation of OT release during fear, and promotion of social behavior in female rats following gentle touch. Despite the vast knowledge of parvocellular OT neurons, surprisingly little is known about parvocellular AVP cells. The activity of AVP receptor-expressing presympathetic cells in the paraventricular nucleus of the hypothalamus is regulated by somato-dendritically released AVP from nearby magnocellular AVP cells. However, the contribution of actual parvocellular AVP neurons to this phenomenon remains questionable. Here we summarize the current body of knowledge about the neuroanatomy and functional relationship of the magnocellular and parvocellular OT and AVP systems. In addition, we discuss several controversial topics including the post-synaptic location of OT receptors, various modes of OT release, and misconceptions/fallacies that might have led to oversimplified models of the OT system.

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Abbreviations

AC:

Auditory cortex

AN:

Accessory nuclei

AON:

Anterior olfactory nucleus

Arc:

Arcuate hypothalamic nucleus

AVP:

Arginine-vasopressin

BLA:

Basolateral amygdala

BNST:

Bed nucleus of stria terminalis

BS:

Brainstem

CB:

Cerebellum

CeA:

Central amygdala

CRH:

Corticotropin-releasing hormone

HC:

Hippocampus

HDB:

Horizontal limb of diagonal band nucleus

iCj:

Island of Calleja

LC:

Locus coeruleus

LS:

Lateral septum

magnAVP neuron:

magnocellular vasopressin neuron

magnOT neuron:

magnocellular oxytocin neuron

MC:

Motor cortex

MeA:

Medial amygdala

NAcc:

Nucleus accumbens

OB:

Olfactory bulb

OT:

oxytocin

parvAVP neuron:

parvocellular vasopressin neuron

parvOT neuron:

parvocellular oxytocin neuron

PC:

Piriform cortex

PFC:

Prefrontal cortex

PLC:

Prelimbic cortex

PV:

Paraventricular thalamus

PVN:

Paraventricular nucleus of the hypothalamus

RGC:

Retina ganglion cells

RMg:

Raphe magnus nucleus

RVLM:

Rostral ventrolateral medulla

SC:

Spinal cord

SCN:

Suprachiasmatic nucleus

SON:

Supraoptic nucleus

SSC:

Somatosensory cortex

Tu:

Olfactory tubercele

vDB:

Ventral diagonal band of Broca

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Acknowledgments and Funding

This work was supported by DFG Postdoc Fellowship AL 2466/1-1 to FA; National Institute of Heart and Lung Grant NIH R01HL090948 and National Institute of Neurological Disorders and Stroke Grant NIH R01NS094640 to JES; (DFG) grants: GR 3619/8-1, GR 3619/13-1, GR 3619/15-1, GR 3619/16-1, and DFG Consortium SFB 1158/2 to VG.

Key References

Althammer F. and Grinevich V., 2017 Diversity of oxytocin neurons: beyond magno- and parvocellular cell types? J Neuroendocrinol. doi: https://doi.org/10.1111/jne.12549. Comprehensive review about common and distinct features of magno- and parvocellular OT cells that lists the most commonly used methods for cell type discrimination.

Chini, B., Verhage, M., and Grinevich, V. (2017). The Action Radius of Oxytocin Release in the Mammalian CNS: From Single Vesicles to Behavior. Trends Pharmacol Sci 38, 982–991. This paper illustrates how OT acts on nearby and distant targets and discusses receptor affinity and the role of the OT concentration gradient.

Eliava, M., Melchior, M., Knobloch-Bollmann, H.S., Wahis, J., da Silva Gouveia, M., Tang, Y., Ciobanu, A.C., Triana del Rio, R., Roth, L.C., Althammer, F., et al. (2016). A New Population of Parvocellular Oxytocin Neurons Controlling Magnocellular Neuron Activity and Inflammatory Pain Processing. Neuron 89, 1291–1304. This is the first paper to show a clear, functionally relevant connection from parvocellular PVN OT neurons to magnocellular OT neurons in the SON.

Grinevich, V., and Neumann, I. (2020). Brain oxytocin: How puzzle stones from animal studies translate into psychiatry. Molecular Psychiatry. Review of the translational aspects of OT-related behavioral studies in rodents.

Grinevich, V., and Stoop, R. (2018). Interplay between Oxytocin and Sensory Systems in the Orchestration of Socio-Emotional Behaviors. Neuron 99, 887–904. Comprehensive review of the role of OT in the development and regulation of sensory modalities.

Hasan, M.T., Althammer, F., Silva da Gouveia, M., Goyon, S., Eliava, M., Lefevre, A., Kerspern, D., Schimmer, J., Raftogianni, A., Wahis, J., et al. (2019). A Fear Memory Engram and Its Plasticity in the Hypothalamic Oxytocin System. Neuron 103, 133–146 e138. This paper demonstrates that parvocellular OT neurons tightly control the fear response and release of OT from magnocellular OT neurons.

Knobloch, H.S., Charlet, A., Hoffmann, L.C., Eliava, M., Khrulev, S., Cetin, A.H., Osten, P., Schwarz, M.K., Seeburg, P.H., Stoop, R., et al. (2012). Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 73, 553–566. This seminal paper showed that OT neurons project to more than 50+ forebrain regions.

Ludwig, M., and Leng, G. (2006). Dendritic peptide release and peptide-dependent behaviours. Nat Rev. Neurosci 7, 126–136. Brilliant review about the role and mechanisms of somato-dendritically released peptides in the brain.

Luther, J.A., and Tasker, J.G. (2000). Voltage-gated currents distinguish parvocellular from magnocellular neurones in the rat hypothalamic paraventricular nucleus. J Physiol 523 Pt 1, 193–209. Seminal work on the different electrophysiological features of magnocellular and parvocellular neurons in the PVN.

Son, S.J., Filosa, J.A., Potapenko, E.S., Biancardi, V.C., Zheng, H., Patel, K.P., Tobin, V.A., Ludwig, M., and Stern, J.E. (2013). Dendritic peptide release mediates interpopulation crosstalk between neurosecretory and preautonomic networks. Neuron 78, 1036–1049. This paper highlights the role of somato-dendritically released AVP in the regulation of preautonomic networks in the PVN.

Stern, J.E., and Armstrong, W.E. (1995). Electrophysiological differences between oxytocin and vasopressin neurones recorded from female rats in vitro. J Physiol 488 (Pt 3), 701–708. Classical paper addressing the different electrophysiological properties of AVP and OT neurons.

Tang, Y., Benusiglio, D., Lefevre, A., Hilfiger, L., Althammer, F., Bludau, A., Hagiwara, D., Baudon, A., Schimmer, J., Kirchner, M.K., et al. (2020). Social touch promotes inter-female communication via oxytocin parvocellular neurons. Nat Neurosci 23, 1125–1137. First paper to show that OT neurons are activated during social interactions using in vivo recordings of identified OT neurons.

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Authors and Affiliations

  1. Center for Neuroinflammation and Cardiometabolic Diseases, Georgia State University, Atlanta, GA, USA

    Ferdinand Althammer, Javier E. Stern & Valery Grinevich

  2. Department of Neuropeptide Research in Psychiatry, Central Institute of Mental Health, University of Heidelberg, J5, Mannheim, Germany

    Valery Grinevich

Authors
  1. Ferdinand Althammer
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  2. Javier E. Stern
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  3. Valery Grinevich
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Correspondence to Ferdinand Althammer , Javier E. Stern or Valery Grinevich .

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  1. Department of Neuropeptide Research in Psychiatry, Central Institute of Mental Health, University of Heidelberg, Mannheim, Baden-Württemberg, Germany

    Valery Grinevich

  2. Department of Physiology & Neurobiology, Eötvös Loránd University, Budapest, Hungary

    Árpád Dobolyi

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Althammer, F., Stern, J.E., Grinevich, V. (2021). Neuroanatomical and Functional Relationship Between Parvocellular and Magnocellular Oxytocin and Vasopressin Neurons. In: Grinevich, V., Dobolyi, Á. (eds) Neuroanatomy of Neuroendocrine Systems. Masterclass in Neuroendocrinology, vol 12. Springer, Cham. https://doi.org/10.1007/978-3-030-86630-3_6

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