Hippocampal lesions impair navigational learning in experienced homing pigeons.

Adult experienced homing pigeons from Maryland were subjected to hippocampal lesion and then transferred to a new loft in Ohio to examine what effect such treatment may have on learning to navigate to a new home loft. When subsequently released from an unfamiliar site, the hippocampal lesioned birds were impaired in taking up a vanishing bearing toward their new Ohio loft. This deficit is interpreted as an impairment in hippocampal-lesioned birds learning a new navigational map. Together with a previous study, the results suggest that an intact hippocampus is necessary if young naive or adult experienced homing pigeons are to learn a navigational map. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Homing in pigeons: the role of the hippocampal formation in the representation of landmarks used for navigation

When given repeated training from a location, homing pigeons acquire the ability to use familiar landmarks to navigate home. Both control and hippocampal-lesioned pigeons succeed in learning to use familiar landmarks for homing. However, the landmark representations that guide navigation are strikingly different. Control and hippocampal-lesioned pigeons were initially given repeated training flights from two locations. On subsequent test days from the two training locations, all pigeons were rendered anosmic to eliminate use of their navigational map and were phase- or clock-shifted to examine the extent to which their learned landmark representations were dependent on the use of the sun as a compass. We show that control pigeons acquire a landmark representation that allows them to directly use landmarks without reference to the sun to guide their flight home, called "pilotage". Hippocampal-lesioned birds only learn to use familiar landmarks at the training location to recall the compass direction home, based on the sun, flown during training, called "site-specific compass orientation." The results demonstrate that for navigation of 20 km or more in a natural field setting, the hippocampal formation is necessary if homing pigeons are to learn a spatial representation based on numerous independent landmark elements that can be used to directly guide their return home.     

The neuroethology of cognitive maps: contributions from research on the hippocampus and homing pigeon navigation

The rich ethological tradition that characterizes the homing behavior of pigeons offers an excellent opportunity to examine the importance of the hippocampal formation for the regulation of spatial cognitive mechanisms. The present review summarizes both anatomical and behavioral data obtained in researches on the pigeon hippocampal formation that have been performed over the last 12 years. Pathway connection studies and investigations on the neurochemical organization of the avian hippocampal formation show that this structure shares many similarities with the mammalian hippocampus and provide the basis for structural as well as functional homology. The initial research on the role of the hippocampal formation in the homing behavior showed that this brain structure is likely to be involved in phenomena of spatial cognition. Therefore, the homing behavior of pigeons has been extensively used as an experimental model to investigate the role of the hippocampal formation in spatial cognition related to a naturally occurring behavior. These studies have revealed that the hippocampal formation plays a fundamental role in the learning of a navigational map based on atmospheric odors, but it doesn't seem to be involved in the operation of such a map. In contrast, both the learning and the operation of a navigational map based on the recognition of familiar landmarks require a functional hippocampal formation. Further investigations indicated that these functions of the hippocampal formation are mediated by its involvement in the use of the sun compass, and suggested that the hippocampal formation plays a fundamental role in a cognitive process in which the sun compass is specifically used to learn about the location of stimuli in space. The studies reviewed in the present paper have provided a considerable amount of experimental data both on the anatomical/neurochemical organization of the avian hippocampal formation and on the role played by this brain structure in spatial cognition. The future development of these researches will need to consider the contribution to hippocampal function of specific transmitter systems that are involved in hippocampal circuitry. In particular, the afferent cholinergic system and some of the peptidergic systems intrinsic to the hippocampal formation deserve particular attention in view of their possible involvement in the acquisition and/or operation of spatial cognitive abilities by homing pigeons.     

Olfaction and the homing ability of pigeons in the southeastern United States

The importance of atmospheric odors for homing pigeon navigation was tested using birds from a loft located in Savannah, GA, in the southeastern United States. When released from a familiar training site, control pigeons and pigeons given intranasal injections of zinc sulfate to produce anosmia both displayed good homeward orientation and homed quickly. When released from three unfamiliar release sites, in contrast, control birds tended to orient southeast, while zinc sulfate-treated birds were more likely to fly northwest. More importantly, while the majority of control pigeons returned to the home loft, few of the zinc sulfate-treated birds returned. The good performance of both groups from the familiar site indicates that zinc sulfate treatment does not impair the general motor ability or motivation of homing pigeons. Therefore, the observed impairment in homing success of the zinc sulfate-treated pigeons from the unfamiliar locations presumably reflects an impaired ability to use atmospheric odors to navigate home. As such, the data support the hypothesis that successful homing pigeon navigation is based on the perception of atmospheric odors and that olfactory navigation is the primary mechanism used by pigeons over a broad range of geographic areas to approximate their relative position with respect to home from unfamiliar locations.     

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. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Effects of ablation of the presumed equivalent of the mammalian prefrontal cortex on pigeon homing.

Pigeons (Columba livia) with bilateral ablation of the posterodorsolateral neostriatum and the overlying corticoid were compared with unoperated control Ss in homing from both familiar and unfamiliar sites. Before the operation all of the pigeons were subjected to 8 training flights from a site destined to be the familiar one. Postoperatively, the groups did not differ in orientation from the familiar site. In their releases from unfamiliar sites, however, the operated birds oriented in the training flight direction, whereas the control Ss were oriented homeward. In all of the releases the homing performance, including both the homing speed and the number of returned birds, was significantly higher in the control group. Thus, the ablated tissue plays a role in homing behavior possibly through mediation of spatial orientation, of olfactory navigation, or of both. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Dissociation of the effects of bilateral lesions of the dorsal hippocampus and parietal cortex on path integration in the rat.

Rodents are able to rely on self-motion (idiothetic) cues and navigate toward a reference place by path integration. The authors tested the effects of dorsal hippocampal and parietal lesions in a homing task to dissociate the respective roles of the hippocampus and the parietal cortex in path integration. Hippocampal rats exhibited a strong deficit in learning the basic task. Parietal rats displayed a performance impairment as a function of the complexity of their outward paths when the food was placed at varying locations. These results suggest that the parietal cortex plays a specific role in path integration and in the processing of idiothetic information, whereas the hippocampus is involved in the calibration of space used by the path integration system. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

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. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Effects of MK-801 on spatial memory in homing and nonhoming pigeon breeds.

Homing pigeon breeds, the product of artificial selection on the basis of navigational and spatial ability, differ from nonhoming breeds in hippocampal size and distribution of N-methyl-{d}-aspartate (NMDA) dependent receptors. The effects of MK-801 (0.1 mg/kg administered intraperitoneally [ip]), a noncompetitive NMDA antagonist, on spatial reference memory (RM) were compared between the 2 breeds in a radial arm maze task. MK-801 disrupted the acquisition of RM in the nonhoming group but not the homing group, which was equivalent to the 2 saline-only control groups. As in previous findings with mammals, working memory was not affected by MK-801. This behavioral dissociation, coupled with differences in NMDA-dependent long-term potentiation between breeds, suggests an exceptional opportunity to investigate the role and function of the dorsomedial telencephalon region in spatial RM, through anatomical, neurochemical, and behavioral comparisons between homing and nonhoming pigeon breeds. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Learning navigational maps through potentiation and modulation of hippocampal place cells

We analyze a model of navigational map formation based on correlation-based, temporally asymmetric potentiation and depression of synapses between hippocampal place cells. We show that synaptic modification during random exploration of an environment shifts the location encoded by place cell activity in such a way that it indicates the direction from any location to a fixed target avoiding walls and other obstacles. Multiple maps to different targets can be simultaneously stored if we introduce target-dependent modulation of place cell activity. Once maps to a number of target locations in a given environment have been stored, novel maps to previously unknown target locations are automatically constructed by interpolation between existing maps.     

Hippocampal lesions and associated learning in the pigeon.

The performance of pigeons with hippocampal lesions was compared with that of unoperated and neostriatal-lesioned control Ss in 3 experiments. In Experiment 1, hippocampal-lesioned birds were retarded in the acquisition and the maintenance levels of autoshaped responding. However, the deficit was attenuated following the addition of a response contingency to the autoshaping schedule. In Experiment 2, the hippocampal-lesioned birds showed impaired performance on a differential reinforcement of low rates of responding schedule. From the high levels of responding in Experiment 2, underresponding was observed in hippocampal-lesioned birds relative to control Ss on return to the autoshaping schedule in Experiment 3. Results are interpreted in terms of impaired classical conditioning in hippocampal-lesioned birds. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The muscarinic acetylcholine antagonist scopolamine impairs short-distance homing pigeon navigation

The present study employed intramuscular (i.m.) injections of the acetylcholine (ACh) receptor antagonist scopolamine hydrobromide (0.10 mg/kg) to investigate the possible involvement of ACh in naturally occurring spatial navigation in homing pigeons (Columba livia). Control pigeons receiving injections of saline or scopolamine methylbromide, an ACh antagonist that does not cross the blood-brain barrier, were oriented in a homeward direction when released from a location 8 km from home. In contrast, pigeons injected with scopolamine hydrobromide (0.10 mg/kg, i.m.) were less well oriented and took more time to return home from the same location. These results suggest that homing pigeon navigation is regulated, in part, by central cholinergic mechanisms.     

Sound localization in pigeon (Columba livia).

The presence of a binaurally activated nucleus (nucleus laminaris) in the hindbrain of birds suggests that they may be capable of binaural sound localization. In this report, after verification that pigeons were capable of either homing or scanning for the source of a sound, 5 Ss were also shown to be (a) capable of localizing a single burst of noise whose duration was too brief for homing or scanning; (b) capable of using either binaural time or intensity disparities for the localization of brief tones; (c) capable of localizing a single tone-pip throughout their frequency range of hearing from 125 Hz to 8 kHz, though having considerable difficulty in their midfrequency range (1–2 kHz); and (d) capable of localizing a single brief burst of narrow band noise even in their midfrequency range. It is concluded that the capacity of pigeons to localize brief sounds and to use binaural disparity cues for doing so is not qualitatively different from that of mammals and, therefore, that the nucleus laminaris or some similar brain-stem nuclei in pigeons are probably analogous in their contribution to sound localization to the superior olivary complex in mammals. (55 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

GluR-A-deficient mice display normal acquisition of a hippocampus-dependent spatial reference memory task but are impaired during spatial reversal.

Acquisition and reversal of a spatial discrimination were assessed in an appetitive, elevated plus-maze task in 4 groups of mice: knockout mice lacking the AMPA receptor subunit GluR-A (GluR1), wild-type controls, mice with cytotoxic hippocampal lesions, and controls that had undergone sham surgery. In agreement with previous studies using tasks such as the water maze, GluR-A-/- mice were unimpaired during acquisition of the spatial discrimination task, whereas performance in the hippocampal group remained at chance levels. In contrast to their performance during acquisition, the GluR-A-/- mice displayed a mild deficit during reversal of the spatial discrimination and were profoundly impaired during discrete trial, rewarded-alternation testing on the elevated T maze. The latter result suggests a short-term. flexible spatial working memory impairment in GluR-A-/- mice, which might also underlie their mild deficit during spatial reversal. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Transfer of a discrimination by pigeons (Columba livia) between pictured locations and the represented environments.

In Exp 1, pigeons (Columba livia) were trained in a successive slide presentation procedure to discriminate between pictures of 2 ends of a room and then trained to find food in the actual room. A congruent-transfer (CT) group learned the spatial discrimination more quickly than an incongruent-transfer (IT) group. In Exp 2's replication we used a simultaneous slide presentation procedure and added a control group. The IT group required significantly more trials than the CT or control groups. In Exp 3, order of the training conditions was reversed. CT and IT conditions had no effect on the speed of acquisition of the discrimination. This indicates that pigeons acquire a representation of spatial locations from pictures, which can then direct behavior, but the direction of transfer observed was unidirectional. This suggests that a discrimination between spatial locations may not be accurately represented in pictorial form. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Goal recognition and hippocampal formation in the homing pigeon (Columba livia).

Stimulus control of food-site recognition and role of the hippocampal formation (HF) were investigated. Control and HF-lesioned pigeons were trained to find food located in a colored bowl, near a landmark beacon, in a constant room location. During later test trials, the sources of information were individually removed and/or disassociated. For all test trial types, HF-lesioned pigeons consistently chose bowls associated with one of the training stimuli. Controls were more sensitive to the changes introduced during the test trials; choosing like HF-lesioned pigeons on some test trials but choosing randomly on others. The data identify a critical role of the avian HF in learning the spatial relationship among environmental stimuli. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Same-different texture discrimination and concept learning by pigeons.

Investigated the acquisition and transfer of a "same-different" conditional discrimination using multidimensional visual texture stimuli in pigeons. Using a choice task, 4 pigeons were reinforced for discriminating different displays, created from aggregated differences in element color or shape, from uniform displays, in which all elements were identical. Discrimination of these 2 display types was readily acquired by the pigeons when they were required to locate and peck the contrasting target region of the different displays. The pigeons showed high levels of discrimination transfer to novel texture stimuli both during acquisition and in 2 subsequent transfer tests. The results suggest that pigeons may be able to learn a generalized same-different concept when promoted by the use of large numbers of multielement stimuli during training. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Role of retroactive interference in the spatial memory of normal rats and rats with hippocampal lesions.

Studied the importance of retroactive interference (RI) in memory for spatial locations by using a 12-arm radial maze and a standard RI paradigm. 26 male albino Sprague-Dawley rats in the RI condition first learned to choose 4 of the 12 arms, followed by training to a 2nd set of 4 arms. In the control condition for interference, Ss learned the 1st set of arms but were not trained to approach the 2nd set. Thereafter, Ss in each interference condition were assigned to groups (hippocampal, cortical control, or unoperated control), the operations were carried out, and then all Ss were tested for retention of the set of arms learned first. Contrary to predictions of the cognitive map theory (J. O'Keefe and L. Nadel, 1978), RI was found in control Ss. The severe memory deficit found in hippocampals was not influenced by the interference variable. In addition to impaired performance early in relearning, Ss with hippocampal lesions continued to make many errors throughout the 10 wks of testing, including choices to unbaited arms and repeated entries into baited arms. However, hippocampals eventually learned not to reenter unbaited arms. Data indicate a deficit in the selection and utilization of sets of responses and are interpreted as implicating the hippocampus in retrieval processes. (42 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Functional dissociation of the prefrontal cortex and the hippocampus in timing behavior.

Using the peak procedure, rats with aspiration lesions to the medial prefrontal cortex (PFC) or the hippocampus were tested for the acquisition of timing behavior and temporal memory. After surgery, rats were trained to discriminate a 40-sec interval and then tested for temporal memory with gap trials. Results indicated that lesions to the medial PFC disrupted the acquisition of timing behavior. Medial PFC animals needed significantly more trials to reach criterion, and their temporal discrimination function was less uniform and steep, indicating a general deficit in timing ability. In hippocampal rats, the ability to estimate the duration of the discriminative stimulus was unaffected by the lesion. It was concluded that the hippocampus is not necessary for the acquisition of timing behavior in this task. Gap trials failed to produce a deficit in the memory for temporal events for either lesion. Thus, it was further concluded that neither the medial PFC nor the hippocampus is necessary for the memory of temporal events. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Backup compass mechanisms in pigeon orientation with the sun in the zenith

The sun is known to guide homing pigeons as a priority cue. The literature indicates that under total overcast conditions pigeons rely on a backup mechanism akin to the magnetic inclination compass for which there is much laboratory evidence in migratory birds. Total overcast conditions are not favorable for orientation research in the State of S?o Paulo, Brazil. The orientation of homing pigeons raised near the tropic of Capricorn was therefore observed around the time of the December solstice, when the sun culminated directly overhead, with a consequent interruption of the sun compass for a short time every day. In these experiments, carried out between 1981 and 1993, local geomagnetic field inclination was -25 degrees to -29 degrees 30', so that a functioning magnetic inclination compass should have been available to the birds. Whereas the birds released with sun to zenith angles between 10 degrees and 30 degrees were well oriented, both in the morning (99 vanishing bearings) and in the afternoon (143 vanishing bearings), those released with the sun less than 5 degrees away from the zenith showed random orientation (105 vanishing bearings), with no evidence of an alternative magnetic compass mechanism.