The afferent-efferent connections of the pigeon dorsomedial forebrain, which is composed of the "hippocampus" (Hp) and "parahippocampus" (APH), presumed homologues of the mammalian hippocampal complex, were studied. Afferent projections were identified by wheat germ agglutinin-conjugated horseradish peroxidase (WGA-HRP) and efferent projections were identified by 3H-proline and WGA-HRP. In addition to identified intrinsic connections within Hp and APH, both Hp and APH were found to be in receipt of ipsilateral forebrain afferents from each other, the hyperstriatum accessorium, nucleus of the diagonal band, nucleus taeniae, and area corticoidea dorsolateralis. Only Hp received input from the contralateral Hp while only APH received input from the ipsilateral hyperstriatum dorsale and archistriatum, pars ventralis. Both Hp and APH received ipsilateral diencephalic afferents from the nucleus mamillaris lateralis, stratum cellulare internum, nucleus lateralis hypothalami, and nucleus paramedianus internus thalami. Only APH received bilateral input from the nucleus superficialis parvicellularis (this nucleus may send a small projection to Hp) and nucleus dorsolateralis anterior thalami, pars medialis, and an ipsilateral projection from the nucleus subrotundus. Brainstem afferents to Hp and APH included ipsilateral projections from the area ventralis (Tsai) nucleus reticularis pontis oralis, nucleus raphes, nucleus subceruleus dorsalis, and nucleus centralis superior of Bechterew, and bilateral projections from the nucleus linearis caudalis and locus ceruleus, of which the nucleus subceruleus dorsalis, nucleus centralis superior of Bechterew, and locus ceruleus projected to APH only. Forebrain efferents from both Hp and APH were found to project ipsilaterally to the septum, the area of the fasciculus diagonalis Brocae, nucleus taeniae, and area corticoidea dorsolateralis. Only Hp appeared to send efferents to the contralateral septum and Hp, while only APH sent efferents to the hyperstriatum dorsale and the archistriatum. A hypothalamic projection from Hp and APH was found to partially terminate near the nucleus mamillaris lateralis. At the level of pathway connections, the results demonstrate a striking similarity between the avian dorsomedial forebrain and the dorsomedial cortex of reptiles and the mammalian hippocampus.

Many species of birds, including pigeons, possess demonstrable cognitive capacities, and some are capable of cognitive feats matching those of apes. Since mammalian cortex is laminar while the avian telencephalon is nucleated, it is natural to ask whether the brains of these two cognitively capable taxa, despite their apparent anatomical dissimilarities, might exhibit common principles of organization on some level. Complementing recent investigations of macro-scale brain connectivity in mammals, including humans and macaques, we here present the first large-scale “wiring diagram” for the forebrain of a bird. Using graph theory, we show that the pigeon telencephalon is organized along similar lines to that of a mammal. Both are modular, small-world networks with a connective core of hub nodes that includes prefrontal-like and hippocampal structures. These hub nodes are, topologically speaking, the most central regions of the pigeon's brain, as well as being the most richly connected, implying a crucial role in information flow. Overall, our analysis suggests that indeed, despite the absence of cortical layers and close to 300 million years of separate evolution, the connectivity of the avian brain conforms to the same organizational principles as the mammalian brain.

The distribution of six neuropeptides [substance P (SP), leucine (leu5-) enkephalin (LENK), vasoactive intestinal polypeptide (VIP), cholecystokinin (CCK), neuropeptide Y (NPY), and somatostatin (SS)] in the dorsomedial telencephalon (hippocampal region) of the pigeon was studied by immunohistochemistry. All six peptides were found in fibers passing through the septo-hippocampal junction and along the medial wall of the hippocampal region. NPY-, SS-, and VIP-like staining of fibers was seen in the hippocampal commissure. NPY and SS had similar distributions within the hippocampal region, both being most conspicuous in cell bodies, terminals, and fibers of the medial hippocampal region. VIP-positive cells were found in an area dorsal to the SS/NPY cell region. CCK-like immunoreactivity was found in terminal baskets surrounding large cells of a v-shaped structure in the ventromedial hippocampal region. SP- and LENK-like immunoreactivity was found in neuropils in a lateral-dorsal region, the two substances showing similar distributions. This region is thought to lie lateral to the limit of the hippocampal region. Parallels with the distribution of immunoreactivity in the mammalian hippocampus are used to suggest possible equivalent subdivisions of the avian and mammalian hippocampal regions.

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.

Immunoreactivity to four neurotransmitters/transmitter-related enzymes was found in the dorsomedial telencephalon (hippocampal region) of the pigeon. Putative afferent fibers containing choline acetyltransferase-like, serotonin-like, and tyrosine hydroxylase-like immunoreactivity were seen in a fiber tract passing through the septo-hippocampal junction and along the medial wall of the hippocampal region. The most intensive labeling of neuropil and terminals of all four substances was found in the dorsomedial area of the hippocampal region. Glutamic acid decarboxylase-like immunoreactivity was seen in sparsely scattered cells throughout the region. These results are discussed in relation to hypotheses about the boundaries and subdivisions of the hippocampal region of the pigeon.