Three times as many lamina I neurons project to the periaqueductal gray than to the thalamus: a retrograde tracing study in the cat

doi:10.1016/S0304-3940(98)00723-X

Neuroscience Letters

Volume 255, Issue 2, 2 September 1998, Pages 107-110

https://doi.org/10.1016/S0304-3940(98)00723-X Get rights and content

Abstract

The number and distribution of lamina I neurons projecting to the periaqueductal gray (PAG) were examined by a retrograde tracing study in the cat. WGA-HRP injections in the intermediate and caudal PAG resulted in as much as 1600 labeled lamina I neurons throughout the length of the spinal cord, counted in a 1:4 series of sections. The lamina I-PAG projection was predominantly contralateral and most labeled lamina I neurons were found in the enlargements. Comparing these results with the number of lamina I-thalamic neurons leads to the conclusion that in the cat about three times as many lamina I neurons project to the PAG than to the thalamus. Considering this, one can conclude that the spino-PAG system is a virtually neglected area in pain research.

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Acknowledgements

The authors thank Mr. K. van Linschoten, Mr. M. Platteel and Mrs. E. Meyer for their histotechnical help and Professor Dr. G.N. van Vark for his advice about statistics.

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The next question is how primary sensory information is relayed to Tac1+ neurons. We used rabies-virus-mediated retrograde tracing to label inputs of Tac1+ neurons (Cui et al., 2017), as shown in Figure S5I. Labeled pre-synaptic cells were observed in the spinal trigeminal nucleus (Sp5), the gracile nucleus (Gr), and the cuneate nucleus (Cu) (Figures 3B, S5J, and S5K), areas shown to relay sensory information from the trigeminal ganglia and spinal cord to central brain regions (Abraira and Ginty, 2013; Erzurumlu et al., 2010), consistent with previous reports (Barbaresi and Mensà, 2016; Choi et al., 2020; Keay et al., 1997; Mantyh, 1982; Mouton and Holstege, 1998; Wiberg et al., 1987). These results provide anatomical evidence that l/vlPAG Tac1+ neurons relay somatosensory information from the periphery.
It is well known that affective and pleasant touch promotes individual well-being and facilitates affiliative social communication, although the neural circuit that mediates this process is largely unknown. Here, we show that social-touch-like tactile stimulation (ST) enhances firing of oxytocin neurons in the mouse paraventricular hypothalamus (PVH) and promotes social interactions and positively reinforcing place preference. These results link pleasant somatosensory stimulation to increased social interactions and positive affective valence. We further show that tachykinin 1 (Tac1⁺) neurons in the lateral and ventrolateral periaqueductal gray (l/vlPAG) send monosynaptic excitatory projections to PVH oxytocin neurons. Functionally, activation of PVH-projecting Tac1⁺ neurons increases firing of oxytocin neurons, promotes social interactions, and increases preference for the social touch context, whereas reducing activity of Tac1⁺ neurons abolishes ST-induced oxytocin neuronal firing. Together, these results identify a dipeptidergic pathway from l/vlPAG Tac1⁺ neurons to PVH oxytocin neurons, through which pleasant sensory experience promotes social behavior.
5.11 - Ascending Pathways: Anatomy and Physiology
2020, The Senses: A Comprehensive Reference: Volume 1-7, Second Edition
Nociceptive information traveling from the periphery in primary sensory neurons is transmitted to second-order neurons located at the spinal cord and cranial sensory nuclei. From this first relay, various pathways distribute nociceptive input through higher processing centers, so that pain is ultimately perceived in its multiple dimensions and adequate adaptive responses are generated. Although these ascending pathways are believed to terminate in the cortex with one or several relay stations in their way, the term ‘nociceptive ascending pathways’ is normally used in a restricted sense to designate the neuronal tracts that connect the spinal cord with supraspinal regions, each pathway being named from the brain area at which it terminates. About 20 nociceptive ascending pathways have been uncovered so far, which terminate at multiple sites, from the upper spinal cord up to the thelencephalon.
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Periaqueductal Gray
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Cytoarchitecture of the Spinal Cord
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This chapter describes the cellular architecture of the spinal cord. The gray matter of the spinal cord is morphologically heterogeneous. The cells of the spinal cord gray matter differ considerably in terms of size, shape and density. However, the gray matter does show some intrinsic organization, so that zones of regularity or laminae can be identified. The concept of laminae has been adopted widely for describing cytoarchitectonic boundaries in the spinal cord in many species. These laminae were first described by Rexed (1954) in the cat. Since then, the concept of laminae has been adopted widely for describing cytoarchitectonic boundaries in the spinal cord in many species, though detailed examination and description of these laminae have only been completed in the mouse and human, in addition to Rexed's original work in the cat. In general, the organization of the Rexed's laminae in these mammalian species is similar. Ten laminae are recognized and these are organized in a series of layers from dorsal to ventral, but with lamina 10 (also called area 10) found around the central canal. The chapter discusses the major cytological characteristics of each of the laminae. Many studies have shown that neurons within a lamina often show distinct dendritic architecture, chemoarchitecture and patterns of connections as well as function.
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The perception of pain is a dynamic process that is subject to ongoing modulation by central pro- and anti-nociceptive control systems. Diverse factors that may be genetic, gender specific, environmentally determined, psychological or, indeed, engendered by already existing pain-related neuronal activity influence the level of descending control on spinal nociceptive processing. In particular, pain is exacerbated by anxiety. This review examines the evidence for cholecystokinin (CCK)-evoked activation of descending pro-nociceptive facilitatory pathways from the midbrain periaqueductal grey matter (PAG) in mediating anxiety-induced hyperalgesia as well as in the development and maintenance of hyperalgesia associated with peripheral neuropathy. CCK drives a spinal-PAG-medullo-spinal pro-nociceptive positive feedback loop that potentiates spinal transmission of nociceptive afferent input, whilst at the same time suppressing activity in the opioid-driven anti-nociceptive descending pathway from the PAG. In females, responsiveness of PAG neurones to CCK is further modulated by changes in the levels of circulating ovarian hormones, an effect that could underlie the changes in pain sensitivity and responsiveness to opiates that occur during the menstrual cycle and postpartum period.
Ascending Pathways: Anatomy and Physiology
2008, The Senses: A Comprehensive Reference
Nociceptive information traveling from the periphery in primary sensory neurons is transmitted to second-order neurons located at the spinal cord and cranial sensory nuclei. From this first relay, various pathways distribute nociceptive input through higher processing centers, so that pain is ultimately perceived in its multiple dimensions and adequate adaptive responses are generated. Although these ascending pathways are believed to terminate in the cortex with one or several relay stations in their way, the term ‘nociceptive ascending pathways’ is normally used in a restricted sense to designate the neuronal tracts that connect the spinal cord with supraspinal regions, each pathway being named from the brain area at which it terminates. About 20 nociceptive ascending pathways have been uncovered so far, which terminate at multiple sites, from the upper spinal cord up to the thelencephalon.
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The multitude of ascending nociceptive pathways, together with the subtleness of the anatomical and physiological aspects that separate them as to their origin at the spinal cord, makes difficult to attribute a particular functional meaning to each one. A tentative way of unraveling the role of each pathway in nociceptive processing has been the elucidation of the connections established by the target. There is, however, a fundamental need to further investigate the functional specificity of each pathway and in which way the compound organization of the nociceptive system contributes to the processing of the various pain states.

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Three times as many lamina I neurons project to the periaqueductal gray than to the thalamus: a retrograde tracing study in the cat

Abstract

Section snippets

Acknowledgements

Brain Res.

Neurosci. Lett.

Brain Res.

Neuroscience

The primate spinothalamic pathways. II. The cells of origin of the dorsolateral and ventral spinothalamic pathways

J. Comp. Neurol.

Cells of origin of spinothalamic tract projections to the medial and lateral thalamus in the cat

J. Comp. Neurol.

Spinal afferents to functionally distinct periaqueductal gray columns in the rat: an anterograde and retrograde tracing study

J. Comp. Neurol.

Morphological types of spinomesencephalic neurons in the marginal zone (lamina I) of the rat spinal cord, as shown after retrograde labeling with cholera toxin subunit B

J. Comp. Neurol.