Neural Substrates of Homing Pigeon Spatial Navigation: Results From Electrophysiology Studies

Abstract

Over many centuries, the homing pigeon has been selectively bred for returning home from a distant location. As a result of this strong selective pressure, homing pigeons have developed an excellent spatial navigation system. This system passes through the hippocampal formation (HF), which shares many striking similarities to the mammalian hippocampus; there are a host of shared neuropeptides, interconnections, and its role in the storage and manipulation of spatial maps. There are some notable differences as well: there are unique connectivity patterns and spatial encoding strategies. This review summarizes the comparisons between the avian and mammalian hippocampal systems, and the responses of single neurons in several general categories: (1) location and place cells responding in specific areas, (2) path and goal cells responding between goal locations, (3) context-dependent cells that respond before or during a task, and (4) pattern, grid, and boundary cells that increase firing at stable intervals. Head-direction cells, responding to a specific compass direction, are found in mammals and other birds but not to date in pigeons. By studying an animal that evolved under significant adaptive pressure to quickly develop a complex and efficient spatial memory system, we may better understand the comparative neurology of neurospatial systems, and plot new and potentially fruitful avenues of comparative research in the future.

Keywords: action potentials; adaptive evolution; birds; hippocampus; space perception; spatial memory.

FIGURE 1

Anatomical differences between mammalian (A) and homing pigeon (B) brain anatomy. (A) The mammalian hippocampus (shaded) is located under a significant amount of neocortex (approximately 3 mm). The simplified flow of information through this structure is as follows: from entorhinal cortex (EC) to Ammon’s Horn CA3 to Ammon’s Horn CA1 to dentate gyrus (DG) and then back to EC. (B) The pigeon hippocampal formation (shaded) is a dorsomedial structure that overlies the lateral ventricle on the surface of the brain. The subdivisions in the avian HF include the following areas: dorsal and ventral dorsolateral (DLd and DLv respectively), dorsomedial (DM), ventrolateral and ventromedial dense cell layers (VL and VM, respectively), and the triangular subdivision (Tr). The area parahippocampal (APH) is not considered to be part of the avian HF but has substantial connections to it. The location of the overlying central sinus blood vessel is indicated by the shaded area. Photomicrographs of cresyl violet stained tissue were taken by the author. Pigeon subdivisions are based on Atoji and Wild (2006).

FIGURE 2

Headstage design used in the majority of the studies involving the Bingman lab. A custom Drive screws were tapped into a Delrin block and connected to bundles of tetrode microelectrodes such that every full turn of the drive screw drove the tetrode bundles 320-μm further into the brain. The wires were soldered into a 16-pot connector connected to the headstage via threaded rod that also had a ground connection that was secured to the brain via a separate wire. Once assembled, the headstage was secured to the skull using stainless steel screws that were covered with dental cement (gray shading), which also protected the small area of exposed brain. In two studies (Hough and Bingman, 2004, 2008), the drive was implanted at a 30-degree angle as pictured, to maximize coverage of the medial HF (dotted lines indicate representative tetrode trajectories) without damaging the central sinus on the surface of the brain (gray stippled oval in Figure 1B). The drive was mounted inside an inverted 35-mm film canister lid, so that the delicate tetrode connections would be protected by the rest of the canister (black outline) during and between experimental trials. Further details can be found in Siegel et al. (2002) and Hough and Bingman (2004).

FIGURE 3

Representative response profiles seen in the homing pigeon hippocampal formation. (A) Path cells have a characteristic high firing rate when the animal is traversing between goal locations (red boxes) but less response at goal locations (blue boxes). (B) Location cells have their highest firing rates when in a localized area near food bowls. The pattern pictured corresponded to a place-like cell. (C) Arena-off cells are presumably context-dependent and fire while in the holding area (in this arena, in the NW corner) but have reduced firing while exploring the arena. (D) Pattern cells have multiple regions of high firing in multiple areas of an open arena that appear to be clustered around the arena edges. (A–C) Adapted from raw data included in Hough and Bingman (2004); (D) adapted from Figure 6A in Kahn et al. (2008) with permission from Elsevier.

FIGURE 4

Evidence of a pigeon place cell summarized in Figure 3B, broken into 2-min epochs. The cell consistently and reliably fired while in the entrance to the SW arm of the radial maze (black squares), even though the animal was visiting all four of the baited arms. The holding area portion of the experiment is not included in this figure (in the N area of the map). In two of the epochs, the bird did not move very much (16–18 and 18–20 min), and the cell only fired as it went from the SE to the SW arms.