Avian hippocampal role in space and content memory.

The present study examined whether the hippocampal formation of homing pigeons (Columba livia) was necessary for learning the contents of different goal locations in an open-field, laboratory environment. Results showed that, although control animals were able to distinguish between two goal locations that contained food items of different quality, pigeons with bilateral hippocampal lesions were impaired in goal-quality discrimination, even though non-spatial cues could have been used to distinguish between goal locations. Probe trials further revealed that the hippocampal formation-lesioned pigeons were impaired in the use of space to recognize goal locations as well as having a poorer capacity to integrate spatial information with the visual features of food bowls. These results promote a revised view of avian hippocampal memory function, one in which the avian hippocampal formation is critical not only for learning the spatial properties of goal locations but also for learning what happens at goal locations in an animal's environment.

Response properties of avian hippocampal formation cells in an environment with unstable goal locations.

The response properties of 48 right (n=24) and left (n=24) hippocampal formation (HF) cells were examined by recording from freely moving homing pigeons as they foraged in an open-field environment with unstable goal locations. Compared to previous results based on HF recordings from environments with stable goal locations, the spatial signal of the HF neurons recorded in the present study was substantially diminished; there was little indication of PATH cells found in previous HF recordings and nothing resembling place cells routinely recorded in rat hippocampus under similar conditions. However, lateralized response properties were detected. Right HF cells dramatically reduced their firing rates during a foraging session, resulting in very low reliability scores. By contrast, left HF cells maintained firing rates throughout sessions and displayed modestly higher reliability scores compared to right HF neurons. Notable was one striking group of cells (n=13), predominantly found in the right HF, that displayed rate maps characterized by numerous, discrete areas of above baseline firing rates, overall very low firing rates and higher specificity than other cells recorded in this study. Overall, the data emphasize the importance of stable goal locations in shaping the spatial response profile of homing pigeon HF neurons and demonstrate the persistence of lateralized response properties under conditions when space explains little of the temporal variation in firing rate.

The avian hippocampus, homing in pigeons and the memory representation of large-scale space.

The extraordinary navigational ability of homing pigeons provides a unique spatial cognitive system to investigate how the brain is able to represent past experiences as memory. In this paper, we first summarize a large body of lesion data in an attempt to characterize the role of the avian hippocampal formation (HF) in homing. What emerges from this analysis is the critical importance of HF for the learning of map-like, spatial representations of environmental stimuli used for navigation. We then explore some interesting properties of the homing pigeon HF, using for discussion the notion that the homing pigeon HF likely displays some anatomical or physiological specialization(s), compared to the laboratory rat, that account for its participation in homing and the representation of large-scale, environmental space. Discussed are the internal connectivity among HF subdivisions, the occurrence of neurogenesis, the presence of rhythmic theta activity and the electrophysiological profile of HF neurons. Comparing the characteristics of the homing pigeon HF with the hippocampus of the laboratory rat, two opposing perspectives can be supported. On the one hand, one could emphasize the subtle differences in the properties of the homing pigeon HF as possible departure points for exploring how the homing pigeon HF may be adapted for homing and the representation of large-scale space. Alternatively, one could emphasize the similarities with the rat hippocampus and suggest that, if homing pigeons represent space in a way different from rats, then the neural specializations that would account for the difference must lie outside HF. Only future research will determine which of these two perspectives offers a better approximation of the truth.

What does a pigeon (Columba livia) brain look like during homing? selective examination of ZENK expression.

Lesion studies have shown that the avian hippocampus plays a crucial role in homing pigeon (Columba livia) navigation. Using the expression of the immediate early gene protein ZENK in intact pigeons, the authors found regional variation in hippocampal activation as a consequence of homing and, necessarily, the behavior and internal states that accompany it. Specifically, pigeons that homed displayed a significant increase in the number of ZENK-labeled cells in the lateral hippocampal formation compared with pigeons that did not home, whereas no difference was seen in the medial hippocampus. Significant changes in ZENK expression were also found in the medial striatum, which resembles the mammalian ventral striatum. The results identify portions of the hippocampal formation and the medial striatum as sites of plasticity associated with homing.

Hippocampal lesions do not disrupt navigational map retention in homing pigeons under conditions when map acquisition is hippocampal dependent.

In contrast to map-like navigation by familiar landmarks, understanding the relationship between the avian hippocampal formation (HF) and the homing pigeon navigational map has remained a challenge. With the goal of filling an empirical gap, we performed an experiment in which young homing pigeons learned a navigational map while being held in an outdoor aviary, and then half the birds were subjected to HF ablation. The question was whether HF lesion would impair retention of a navigational map learned under conditions known to require participation of HF. The pigeons, which had never flown from the aviary before, together with an additional control group that learned a navigational map with free-flight experience, were then released from two distant release sites. Contrary to expectation, the HF-lesioned birds oriented in a homeward direction in manner indistinguishable from the intact control pigeons raised in the same outdoor aviary. HF lesion did not result in a navigational map retention deficit. Together with previous results, it is now clear that regardless of the learning environment present during acquisition, HF plays no necessary role in the subsequent retention or operation of the homing pigeon navigational map.

Lateralization of spatial learning in the avian hippocampal formation.

The authors investigated lateralization of spatial learning within the avian hippocampal formation (HF). In Experiment 1, homing pigeons (Columba livia) with unilateral lesions of the right or left HF were trained to locate a goal in a square room containing local landmarks and global room cues. All groups learned the task. During probe trials, when landmarks were rotated or removed, intact pigeons and left HF-lesioned pigeons relied exclusively on global room cues to locate the food goal. Pigeons with right HF lesions were the only group to demonstrably use the landmarks. The results suggest that the right HF is preferentially involved in the representation of global environmental space, whereas only the left HF may be sensitive to local landmarks for navigation.

The homing pigeon hippocampus and space: in search of adaptive specialization.

The hippocampus (HF) of birds and mammals is essential for the map-like representation of environmental landmarks used for navigation. However, species with contrasting spatial behaviors and evolutionary histories are likely to display differences, or 'adaptive specializations', in HF organization reflective of those contrasts. In the search for HF specialization in homing pigeons, we are investigating the spatial response properties of isolated HF neurons and possible right-left HF differences in the representation of space. The most notable result from the recording work is that we have yet to find neurons in the homing pigeon HF that display spatial response properties similar to HF 'place cells' of rats. Of interest is the suggestion of neurons that show higher levels of activity when pigeons are near goal locations and neurons that show higher levels of activity when pigeons are in a holding area prior to be being placed in an experimental environment. In contrast to the rat, the homing pigeon HF appears to be functionally lateralized. Results from a current lesion study demonstrate that only the left HF is sensitive to landmarks that are located within the boundaries of an experimental environment, whereas the right HF is indifferent to such landmarks but sensitive to global environmental features (e.g., geometry) of the experimental space. The preliminary electrophysiological and lateralization results offer interesting departure points for better understanding possible HF specialization in homing pigeons. However, the pigeon and rat HF reside in different forebrain environments characterized by a wulst and neocortex, respectively. Differences in the forebrain organization of pigeons and rats, and birds and mammals in general, must be considered in making sense of possible species differences in how HF participates in the representation of space.

Internal connectivity of the homing pigeon (Columba livia) hippocampal formation: an anterograde and retrograde tracer study.

The avian hippocampal formation (HF) is a structure necessary for learning and remembering aspects of environmental space. Therefore, understanding the connections between different HF regions is important for determining how spatial learning processes are organized within the avian brain. The prevailing feed-forward, trisynaptic internal connectivity of the mammalian hippocampus and its importance for cognition have been well described, but the internal connectivity of the avian HF has only recently been investigated. To examine further the connectivity within the avian HF, small amounts of cholera toxin subunit B, primarily a retrograde tracer (n = 15), or biotinylated dextran amine, primarily an anterograde tracer (n = 10), were injected into localized regions of the HF. Examination of the immunohistochemically labeled tissue showed projections from extrinsic sensory processing areas into dorsolateral HF and the dorsal portion of the dorsomedial HF (DMd). DMd in turn projected into the medial (VM) and lateral (VL) ventral cell layers. A projection from VM into VL was found, and together these areas and DM provided input into the contralateral ventral cell layers. Ipsilaterally, a ventral portion of dorsomedial HF (DMv) received input from VL and VM. From DMv, projections exited HF laterally. The highlighted projections formed a discernible feed-forward processing network through the avian HF that resembled the trisynaptic circuit of the mammalian HF.