Homing Pigeon Hippocampal Formation Research Articles

Neuronal circuits within the homing pigeon hippocampal formation.

The current study aimed to reveal in detail patterns of intrahippocampal connectivity in homing pigeons (Columba livia). In light of recent physiological evidence suggesting differences between dorsomedial and ventrolateral hippocampal regions and a hitherto unknown laminar organization along the transverse axis, we also aimed to gain a higher-resolution understanding of the proposed pathway segregation. Both in vivo and high-resolution in vitro tracing techniques were employed and revealed a complex connectivity pattern along the subdivisions of the avian hippocampus. We uncovered connectivity pathways along the transverse axis that started in the dorsolateral hippocampus and continued to the dorsomedial subdivision, from where information was relayed to the triangular region either directly or indirectly via the V-shaped layers. The often-reciprocal connectivity along these subdivisions displayed an intriguing topographical arrangement such that two parallel pathways could be discerned along the ventrolateral (deep) and dorsomedial (superficial) aspects of the avian hippocampus. The segregation along the transverse axis was further supported by expression patterns of the glial fibrillary acidic protein and calbindin. Moreover, we found strong expression of Ca2+ /calmodulin-dependent kinase IIα and doublecortin in the lateral but not medial V-shape layer, indicating a difference between the two V-shaped layers. Overall, our findings provide an unprecedented, detailed description of avian intrahippocampal pathway connectivity, and confirm the recently proposed segregation of the avian hippocampus along the transverse axis. We also provide further support for the hypothesized homology of the lateral V-shape layer and the dorsomedial hippocampus with the dentate gyrus and Ammon's horn of mammals, respectively.

Avian forebrain processing of magnetic intensity and inclination: hippocampus, anterior forebrain Wulst and an unexpected double-dissociation

It is often neglected that the ability of birds to extract navigational information from the earth’s magnetic field can be shaped by learning and memory, which would necessarily recruit brain regions of the telencephalon that support cognitive processes. In the current study, we exploited a validated, conditioning experimental paradigm to explore the possible role of the homing pigeon hippocampal formation (HF) and anterior forebrain Wulst in the detection of variation in both magnetic field intensity and inclination. Whereas HF lesions resulted in a complete loss of intensity discrimination while sparing inclination discrimination, Wulst lesions had the opposite effect, resulting in a complete loss of inclination discrimination while sparing intensity discrimination. It is not surprising that Wulst lesions should disrupt inclination discrimination because in migratory songbirds, regions of the Wulst are known to support the geomagnetic compass, which relies on inclination. More challenging is explaining why HF should be sensitive to variation in magnetic intensity. We suggest that the observed HF sensitivity to intensity may reflect incorporation of geomagnetic irregularities (anomalies) as pigeons learn a map-like representation of familiar landmarks and landscape features. The parallel processing of magnetic intensity and inclination in the homing pigeon forebrain sets the foundation for future studies designed to better understand how cognitive processing can influence geomagnetically guided navigational behavior in birds.

Network structure of functional hippocampal lateralization in birds.

Functional hemispheric asymmetry is a common feature of vertebrate brain organization, yet little is known about how hemispheric dominance is implemented at the neural level. One notable example of hemispheric dominance in birds is the leading role of the left hippocampal formation in controlling navigational processes that support homing in pigeons. Relying on resting state fMRI analyses (where Functional connectivity (FC) can be determined by placing a reference 'seed' for connectivity in one hemisphere), we show that following seeding in either an anterior or posterior region of the hippocampal formation of homing pigeons and starlings, the emergent FC maps are consistently larger following seeding of the left hippocampus. Left seedings are also more likely to result in FC maps that extend to the contralateral hippocampus and outside the boundaries of the hippocampus. The data support the hypothesis that broader FC is one neural-organizational property that confers, with respect to navigation, functional dominance to the left hippocampus of birds.

Hippocampal lesions in homing pigeons do not impair feature-quality or feature-quantity discrimination

The role of the avian hippocampal formation (HF) in spatial cognition is well demonstrated. However, it remains uncertain if the avian hippocampus, like its mammalian counterpart, has a role in the integration of elements that could compose a memory independent of space. The two experiments in the current study examined whether the HF of homing pigeons (Columba livia) was required to encode into memory a discriminative representation of food quality (Experiment 1) and quantity (Experiment 2) with different food bowl-features. Pigeons were exposed to an array of different colored bowls, two of which contained food rewards differing in preferred quality or quantity. To render space irrelevant for memory encoding, the location of the food-rewarded bowls was altered between each trial, while the features of the rewarded bowls remained constant. Both groups learned the feature-based quality and quantity discrimination tasks and no difference in performance between control pigeons and those with bilateral lesions of the hippocampus were found. The findings do not support the hypothesis that the avian HF is recruited when only non-spatial elements are integrated into a unified memory. From the current study, and the literature as a whole, it appears that the avian HF, unlike the mammalian hippocampus, may play no necessary role in memory processes where space is irrelevant.

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.

Neuronal Implementation of Hippocampal-Mediated Spatial Behavior: A Comparative Evolutionary Perspective

The hippocampal formation (HF) of mammals and birds plays a strikingly similar role in the representation of space. This evolutionarily conserved property, however, belies the contrasting spatial ecology of animals such as rats and homing pigeons, differing spatial ecologies that should have promoted the evolution of group-specific adaptations to the HF representation of space. However, the spatial response properties of pigeon and rat HF neurons reveal surprising similarity in the contribution of position, direction, and trajectory toward explaining spatial variation in firing rate. By contrast, the asymmetrical distribution of neuronal response properties in the left and right HF of homing pigeons, but not rats, indicates a difference in network organization. The authors propose that hippocampal evolution may be characterized by inertia with respect to changes in the basic spatial elements that determine the response properties of neurons but considerable plasticity in how the neuronal response elements are organized into functional networks.

The effects of a changing ambient magnetic field on single-unit activity in the homing pigeon hippocampus

The central representation of geomagnetic information in the avian brain continues to challenge researchers. Although the homing pigeon hippocampal formation primarily participates in the map-like representation of landmarks, some suggestive data indicate that it may also participate in spatial behavior guided by geomagnetic information. Forty-four isolated neurons were recorded from the hippocampal formation of homing pigeons trained to shuttle between two goal locations under changing (direction and intensity, and direction only) magnetic field conditions. Of the 37 slow-firing cells sampled (<14 spikes/s), none displayed a change in firing rate at the time of magnetic field transitions or during different ambient magnetic field conditions. By contrast, three of seven fast firing cells (>17 spikes/s) clearly displayed a phasic increase in firing during at least one of the magnetic field transitions used. The results are consistent with the hypothesis that a subset of hippocampal formation neurons receives information regarding changes in the earth's magnetic field that may be used to guide behavior.

Lateralized functional components of spatial cognition in the avian hippocampal formation: Evidence from single‐unit recordings in freely moving homing pigeons

Previous research has revealed that the functional components of spatial cognition are lateralized in the forebrain of birds, including the hippocampal formation (HF). To investigate how HF cells in the left and right avian brain may differentially participate in representations of space, we recorded single-units from the HF of homing pigeons as they ran a plus maze for food. The rate maps of left HF cells often displayed elongated regions of increased activity in the center of the maze and along the maze corridors, whereas right HF cells tended to display patches at the ends of maze arms at/near goal locations. Left HF cells displayed a higher degree of spatial-specificity compared with right HF cells, including higher patch-specificity, higher reliability, and a higher incidence of location-correlated activity. Analysis of speed-correlated and trajectory-dependent activity also revealed significant HF-lateralized differences. Right HF cells tended to display significant negative correlations between spike rate and speed, although speed-dependent rate maps indicate that this relationship did not explain their space-specific activity. Left HF cells displayed a significantly higher incidence of trajectory-dependent space-specific activity than was observed in the right HF, suggesting that left HF cells may participate in navigating among goal locations. Differences in the correlates of left and right pigeon HF cells are consistent with unilateral HF-lesion data suggesting that the functional components of spatial cognition are lateralized in the avian brain, and furthermore, provide a basis for hypotheses regarding how the left and right HF support different aspects of spatial cognition.

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.

Spatial-specificity of single-units in the hippocampal formation of freely moving homing pigeons.

The importance of space-specific single-unit activity for hippocampal formation (HF)-mediated learning and memory in rodents has been extensively studied, yet little is known about how the unit findings in rodents generalize to other vertebrate species. We report a first assessment of the space-specific single-unit activity recorded from the HF of homing pigeons as they moved through a plus maze for food reward. Rate maps of pigeon HF single-unit activity typically revealed multiple regions (2-5 per cell) of increased activity (on average, 2.5 times higher than other regions of the maze) that in 27% of slow-firing cells was reliably space-specific over time. The qualitative appearance of rate maps and the degree of spatial-specificity observed for most all pigeon HF cells suggests more modest space-specific activity than typically reported for rat hippocampal cells. The nature of space-specific activity in the pigeon HF includes (1) often transiently reliable regions of increased activity for many cells, (2) multiple patches of activity that were sometimes observed in analogous maze areas, and (3) cells displaying substantial decreases in firing rate between baseline and maze-run conditions that could not be explained by a simple relationship between firing rate and a pigeon's speed. These observations suggest that pigeon HF cells may be coding for an unspecified behavioral/motivational/environmental factors in addition to a pigeon's momentary location. The data further suggest that the spatial ecology and evolutionary history of different species may be a critical feature shaping how HF neurons capture properties of space.

Intrahippocampal connections in the pigeon (Columba livia) as revealed by stimulation evoked field potentials.

The hippocampal formation (HF) of mammals and birds is crucial for spatial learning and memory. However, although the underlying synaptic organization and connectivity of the mammalian HF are well characterized, comparatively little is known about the avian HF. Localized regions of the homing pigeon HF were stimulated at 400-600 microA while evoked field potentials (EFPs) were recorded from adjacent and more distant HF areas relative to the stimulation site. The shortest discernible EFP latency was 12.2 msec. The emerging connectivity profile (using the location of peak EFP amplitude after stimulation and making no determination of the number of intervening synapses) was characterized by projections from the dorsolateral (DL) HF to the dorsomedial (DM) HF (15-msec latency) at the same anterior/posterior (A/P) level, DM to ventrolateral (VL) and ventromedial (VM; 15 msec) HF across A/P levels, VM to VL (12 msec) and contralateral VM (15 msec) at the same A/P level, and VL to ventral DL (DLv; 15 msec) across A/P levels posterior to the stimulation site. Using these data as a first approximation, connectivity through the avian HF appears to be characterized by a discernible feed-forward network starting with a projection from DL to DM, DM to VL, VM, and contralateral VM, VM to VL, and VL to posterior ventral DLv. Although still speculative, the results suggest that the internal connectivity of the avian HF is similar to that of the mammalian HF, despite the large evolutionary divergence between the two taxa.

The homing pigeon hippocampus and the development of landmark navigation

The role of the homing pigeon hippocampal formation was examined in the development of loft fidelity and landmark navigation. During the course of five summers, different groups of young pigeons (hippocampal-lesioned, control-lesioned, and unoperated controls) were given free flight experience followed by short distance training and experimental releases. In Experiment 1, a census of which loft each pigeon entered revealed that hippocampal lesioned pigeons displayed less loft fidelity than controls. In Experiment 2 and 3, the percent of young birds lost during their first summer of training and their first experimental release was examined. Despite displaying similarly good homeward-oriented vanishing bearings, significantly more hippocampal lesioned pigeons were lost compared to control groups. The results support the hypothesis that the homing pigeon hippocampal formation participates in the learning/operation of a spatial representation of local landmarks near the loft that can be used for loft recognition and navigation.