Perineuronal satellite neuroglia in the telencephalon of New Caledonian crows and other Passeriformes: evidence of satellite glial cells in the central nervous system of healthy birds?

Abstract

Glia have been implicated in a variety of functions in the central nervous system, including the control of the neuronal extracellular space, synaptic plasticity and transmission, development and adult neurogenesis. Perineuronal glia forming groups around neurons are associated with both normal and pathological nervous tissue. Recent studies have linked reduction in the number of perineuronal oligodendrocytes in the prefrontal cortex with human schizophrenia and other psychiatric disorders. Therefore, perineuronal glia may play a decisive role in homeostasis and normal activity of the human nervous system.Here we report on the discovery of novel cell clusters in the telencephala of five healthy Passeriforme, one Psittaciform and one Charadriiforme bird species, which we refer to as Perineuronal Glial Clusters (PGCs). The aim of this study is to describe the structure and distribution of the PGCs in a number of avian species.PGCs were identified with the use of standard histological procedures. Heterochromatin masses visible inside the nuclei of these satellite glia suggest that they may correspond to oligodendrocytes. PGCs were found in the brains of nine New Caledonian crows, two Japanese jungle crows, two Australian magpies, two Indian mynah, three zebra finches (all Passeriformes), one Southern lapwing (Charadriiformes) and one monk parakeet (Psittaciformes). Microscopic survey of the brain tissue suggests that the largest PGCs are located in the hyperpallium densocellulare and mesopallium. No clusters were found in brain sections from one Gruiform (purple swamphen), one Strigiform (barn owl), one Trochiliform (green-backed firecrown), one Falconiform (chimango caracara), one Columbiform (pigeon) and one Galliform (chick).Our observations suggest that PGCs in Aves are brain region- and taxon-specific and that the presence of perineuronal glia in healthy human brains and the similar PGCs in avian gray matter is the result of convergent evolution. The discovery of PGCs in the zebra finch is of great importance because this species has the potential to become a robust animal model in which to study the function of neuron-glia interactions in healthy and diseased adult brains.

Neuronal satellitosis is a common finding in the avian brain

“…Similarly to the HA, the hyperpallium intercalatum (HI) also frequently showed neuronal satellitosis (n = 46/49; 93.9%), but compared to HA, grade 1 (n = 29; 63%) and grade 2 (n = 17; 37%) were less and more frequent, respectively. Compared to HA neuronal satellitosis, hyperpallium densocellulare (HD) neuronal satellitosis was observed in more birds (n = 48/49; 97.9%) ranging from grade 1 (n = 23/48; 48%) to grade 3 (n = 14/48; 29%) as reported previously (Medina et al, 2013) (Table 2). The hyperpallium (formerly known as the Wulst), and in particular the HD, is generally considered the avian equivalent of the cortex of mammals, playing a major role in the somatosensory system and in the action and control of movement (Reiner et al, 2005;Medina, 2007;Stacho et al, 2020).…”

“…Currently, the term NS seems to be accepted in both physiologic and pathologic conditions (Garman, 2011;Wohlsein et al, 2013). In animals, NS has been reported in different species, from mammals (Wohlsein et al, 2013) to birds (Medina et al, 2013). For birds, neuronal satellitosis has been reported as a feature of avian neuroinvasive viral diseases, such as avian influenza, West Nile fever and Usutu (Austin et al, 2004;Bröjer et al, 2012;Rijks et al, 2016;Benzarti et al, 2020).…”

“…For birds, neuronal satellitosis has been reported as a feature of avian neuroinvasive viral diseases, such as avian influenza, West Nile fever and Usutu (Austin et al, 2004;Bröjer et al, 2012;Rijks et al, 2016;Benzarti et al, 2020). Only a single study reports this finding in Passeriformes as a brain-area-associated normal pattern, characterized by high numbers of glial cells surrounding a neuronal soma, namely "perineuronal glial clusters" (PGCs) (Medina et al, 2013). Unfortunately, more studies on the association between satellitosis as a normal feature and specific brain regions in different avian orders are lacking.…”

Clustered organization and region‐specific identities of estrogen‐producing neurons in the forebrain of Zebra Finches (Taeniopygia guttata)

“…In songbirds, cell clusters in the brain have been previously described in a handful of studies (Fortune & Margoliash, 1992;Fortune & Margoliash, 1995;Gahr & Garcia-Segura, 1996;Kirn, Fishman, Sasportas, Alvarez-Buylla, & Nottebohm, 1999;Medina, Hunt, Gray, Wild, & Kubke, 2013). In zebra finches, cell clusters have been reported in the nidopallium, mesopallium, and hyperpallium (Fortune & Margoliash, 1992;Fortune & Margoliash, 1995;Medina et al, 2013). Medina et al (2013), suggested that the clusters in the mesopallium are composed of one neuron and multiple glial cells, based on Nissl stain.…”

“…In zebra finches, cell clusters have been reported in the nidopallium, mesopallium, and hyperpallium (Fortune & Margoliash, ; Fortune & Margoliash, ; Medina et al, ). Medina et al (), suggested that the clusters in the mesopallium are composed of one neuron and multiple glial cells, based on Nissl stain. Our use of NeuN staining here indicates that the majority of the clusters are composed of neurons in all regions we examined, including the NCM and CMM (i.e., in both nidopallium and mesopallium).…”