Distribution of neurotransmitter receptors and zinc in the pigeon (Columba livia) hippocampal formation: A basis for further comparison with the mammalian hippocampus

Abstract

The avian hippocampal formation (HF) and mammalian hippocampus share a similar functional role in spatial cognition, but the underlying neuronal mechanisms allowing the functional similarity are incompletely understood. To understand better the organization of the avian HF and its transmitter receptors, we analyzed binding site densities for glutamatergic AMPA, NMDA, and kainate receptors; GABAA receptors; muscarinic M1 , M2 and nicotinic (nACh) acetylcholine receptors; noradrenergic α1 and α2 receptors; serotonergic 5-HT1A receptors; dopaminergic D1/5 receptors by using quantitative in vitro receptor autoradiography. Additionally, we performed a modified Timm staining procedure to label zinc. The regionally different receptor densities mapped well onto seven HF subdivisions previously described. Several differences in receptor expression highlighted distinct HF subdivisions. Notable examples include 1) high GABAA and α1 receptor expression, which rendered distinctive ventral subdivisions; 2) high α2 receptor expression, which rendered distinctive a dorsomedial subdivision; 3) distinct kainate, α2 , and muscarinic receptor densities that rendered distinctive the two dorsolateral subdivisions; and 4) a dorsomedial region characterized by high kainate receptor density. We further observed similarities in receptor binding densities between subdivisions of the avian and mammalian HF. Despite the similarities, we propose that 300 hundred million years of independent evolution has led to a mosaic of similarities and differences in the organization of the avian HF and mammalian hippocampus and that thinking about the avian HF in terms of the strict organization of the mammalian hippocampus is likely insufficient to understand the HF of birds.

Contribution of Genoarchitecture to Understanding Hippocampal Evolution and Development

“…One important issue regarding the comparison of the HF between birds, reptiles, and mammals is the recurrent assumption that the cytoarchitecture of this region in birds is different to that in reptiles and mammals because it shows a nonlaminar organization [for example, discussed by Herold et al, 2014]. In contrast to this view, developmental studies have shown that this structure is also formed according to a layered cytoarchitectonic pattern [Redies et al, 2001].…”

“…The latter field was previously suggested to be a caudolateral extension of the APH (and was accordingly called APHcl) based on its cytoarchitecture and cadherin expression profile [Redies et al, 2001]. In adult pigeons, all of these areas, including the hippocampus and all APH, show moderate to strong zinc expression with differences between different layers, resembling hippocampal projections in mammals [Herold et al, 2014; note that zinc ions are also present in many corticocortical and other palliopallial glutamatergic projections, but they show a remarkably high concentration in the hippocampal mossy fiber system; Paoletti et al, 2009]. As in mammals, the density of zinc-positive terminals in the avian hippocampal complex correlates well with that of NMDA glutamate synapses [Herold et al, 2014].…”

“…In contrast to this view, developmental studies have shown that this structure is also formed according to a layered cytoarchitectonic pattern [Redies et al, 2001]. As in other amniotes, the layers of the avian HF are orthogonal to radial glial fibers (i.e., parallel to the surface) [Abellán et al, 2014] and, although less visible, are also present in adult animals [Suarez et al, 2006], where such layers are respected by patterns of connections [Atoji and Wild, 2004], zinc terminals and glutamate receptor subunit distributions [Herold et al, 2014], which are confined to particular layers of specific radial divisions (for example, the ventral and dorsal subdivisions of the avian dorsolateral APH would correspond to deep versus superficial layers of that field).…”

“…In adult pigeons, all of these areas, including the hippocampus and all APH, show moderate to strong zinc expression with differences between different layers, resembling hippocampal projections in mammals [Herold et al, 2014; note that zinc ions are also present in many corticocortical and other palliopallial glutamatergic projections, but they show a remarkably high concentration in the hippocampal mossy fiber system; Paoletti et al, 2009]. As in mammals, the density of zinc-positive terminals in the avian hippocampal complex correlates well with that of NMDA glutamate synapses [Herold et al, 2014]. Moreover, all of these areas, including APHcl/CDL, show extensive connections between them resembling the axonal networks found between subdivisions of the mammalian hippocampal complex Wild, 2004, 2005;Atoji et al, 2016].…”

“…Birds, particularly flying birds, have remarkable navigation abilities and the interest on their HF has justified numerous studies on its anatomical and neurochemical organization, connections and function [Benowitz and Karten, 1976;Bingman et al, 1984Bingman et al, , 2003Casini et al, 1986;Erichsen et al, 1991;Montagnese et al, 1996;Székely and Krebs, 1996;Colombo and Broadvent, 2000;Atoji et al, 2002;Atoji and Wild, 2004;Suárez et al, 2006;Mayer et al, 2013;Herold et al, 2014]. Some of these studies have led to various proposals of subdivisions [reviewed by Suárez et al, 2006] and to the finding of serial projections between several hippocampal and APH [Atoji and Wild, 2004].…”