Intratelencephalic connections of the hippocampus in pigeons (Columba livia)

Abstract

Behavioral experiments using ablation of the hippocampus are increasingly being used to address the hypothesis that the avian hippocampus plays a role in memory, as in mammals. However, the morphological basis of the avian hippocampus has been poorly understood. In the present study, the afferent and efferent connections of the hippocampus in the pigeon telencephalon were defined by injections, at various rostrocaudal sites, of neuronal tracers mainly into the triangular part located between its V-shaped layer of densely packed neurons. The major results obtained in the present study were as follows. 1) A topographical organization of the commissural projections was confirmed. These projections had two courses that projected to the contralateral side, one traveling through the fiber wall of the ventromedial telencephalon, which was the main path from neurons in the caudal hippocampus, and the other running down through the septohippocampal junction, which was the main path from neurons in the middle to rostral hippocampus. Both courses passed through the pallial commissure. 2) The hippocampus projected bilaterally to the septum, parahippocampal area (APH), and dorsolateral cortical area (CDL). These projections were also distributed topographically, with contralateral efferents crossing through the pallial commissure. 3) The hippocampus had ipsilateral reciprocal connections with APH, CDL, and the dorsal hyperstriatum. Septal afferents to the ipsilateral hippocampus were very small. 4) Intrinsic connections were found between the triangular part of the hippocampus and the lateral limb of the V-shaped layer of neurons. 5) The hippocampus projected ipsilaterally to the ventral basal ganglia and the fasciculus diagonalis Brocae. In sum, these connections of the hippocampus may form a neuronal circuit for the processing of spatial memory in pigeons.

A Direct Hippocampo‐Cerebellar Projection in Chicken

“…However, we preferred the Atoji's model because in our previous studies (unpublished data), a group of labeled neurons appeared in the contralateral APHm-APHim following the injection of HRP into the unilateral APHm-APHim in chickens. Similar results were also obtained in pigeons (Casini et al, 1986;Atoji and wild, 2002) and finches (Szekely and Krebs, 1999). In mammals, the commissural projection of the HF originates from the CA4 area of Ammon's horn (Siegel and Landis, 1974;Demeter et al, 1985).…”

“…Based on the neuropeptide distribution and fiber connections, Erichsen et al, (1991) in chicken, Casini et al, (1986) in pigeon, Szekely and Krebs (1996) in finch, and Kahn et al, (2003) in pigeon suggested that the V-shaped layer (perhaps including the triangular area) correspond to the Ammon's horn of mammals, the dorsomedial region (DM) may be a homologue with the dentate gyrus of mammals, and the dorsolateral region (DL) may be likely candidate of the subiculum or enthorhinal cortex of mammals. However, based on fiber connections of the neurons in avian HF and their sensibilities to lesions formed by kainic acid injection into the lateral ventricle, Atoji and Wild (2002, 2004) suggested a subdividing model in contrast to the one described above. According to this model, the V-shaped layer of birds is similar to the dentate gyrus of mammals, and they may be homologous.…”

“…Much evidence suggests that this region is similar to the HF of the mammals in topography (Craigie, 1930;Northcutt, 1967), development (K€ allen, 1962;Redies et al, 2001), cytoarchitecture (Molla et al, 1986;Montagness et al, 1996;T€ omb€ ol et al, 2000a,b), immunohistochemistry Krebs et al, 1991;Szèkely, 1999) fibers connections with other brain structures (Krayniak and Siegel, 1978;Casini et al, 1986;Szèkely and Krebs, 1996;Atoji and wild, 2002Atoji and wild, , 2004Atoji and wild, , 2006Kahn et al, 2003) and functions, especially in spatial and nonspatial memory (Sherry et al, 1992;Colombo and Broadbent, 2000). Hence there is a tight homologous relationship between the HF of the avian and mammals.…”

Associative learning rapidly establishes neuronal representations of upcoming behavioral choices in crows

“…The PFC is intimately connected to the hippocampus, and prefrontal-hippocampal interactions seem to play a major role during association learning (17,31). In contrast, the NCL has no direct connections to the hippocampus or surrounding structures (26,32,33). It is likely that this major anatomical difference could lead to differences in how the cognitive integration areas of birds and mammals process information during associative learning, such as the time point when prospective representations emerge in the trial.…”

Revised nomenclature for avian telencephalon and some related brainstem nuclei

“…Available hodological data on input from the hippocampal complex and output to the hypothalamus (Krayniak and Siegel, 1978b;Atoji et al, 2002), as well as neurochemical data (Reiner et al, 1984b, Reiner, 1994, suggest homology of the lateral septal nucleus of birds with the nucleus of the same name in mammals. A comparable cell group is present in all reptilian orders (Brauth, 1984;Reiner, 1987;Smeets, 1994).…”