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Keywords:

  • cognitive map;
  • GPS;
  • hippocampus;
  • homing pigeon;
  • landmark navigation

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

It is hypothesized that a central role of the vertebrate hippocampal formation (HF) in behavior is the learning and operation of a map-like representation of familiar landmarks and landscape features. One critical property of a map is that it should enable an individual to re-orient towards a goal location following a navigational error. To test this prediction on a spatial scale consistent with their naturally occurring behavior, control and HF-lesioned homing pigeons were trained from two locations and then subsequently released, while carrying portable GPS-tracking devices, following a phase-shift treatment. Analyses revealed that the HF-lesioned pigeons were less successful than control pigeons in re-orienting homewards following the phase-shift-induced error in their initial orientation. Furthermore, the observation that HF-lesioned pigeons were found to routinely ignore a land–sea landscape boundary when returning home from one of the release sites suggests that coarse landscape features may be an underappreciated source of navigational information for homing pigeons. The data demonstrate that, on a scale of tens of kilometers, homing pigeons are able to learn a hippocampal-dependent, map-like representation of familiar landmarks/landscape features that can support corrective re-orientation following a navigational error.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The ability of homing pigeons to navigate to their loft from distant, unfamiliar sites has been a cornerstone of ethological research for more than 50 years (Wallraff, 1991, 2004; Papi, 2001; Wiltschko & Wiltschko, 2003). The emphasis of the ethological research has been on the sensory nature of the so-called navigational map and compass mechanisms that guide homing from distant, unfamiliar locations. For example, it has been demonstrated that the navigational map can be based on sufficiently stable, spatial variation in the distribution of atmospheric odors (Papi et al., 1972; Wallraff, 2005a; Gagliardo et al., 2008). A navigational map enables a pigeon to determine the direction of displacement relative to home from unfamiliar as well as familiar locations. However, over familiar terrain, navigation can be guided by a memory representation of familiar landmarks/landscape features in addition to the navigational map (Wallraff & Neumann, 1989; Braithwaite & Guilford, 1991; Wallraff et al., 1993; Gagliardo et al., 2001; Biro et al., 2004, 2007). Recently, there has been growing interest in the landmark-based navigational mechanisms that homing pigeons can employ over previously experienced, familiar areas closer to the loft, with an emphasis on visual landmarks/landscape features (Bingman & Able, 2002; Biro et al., 2002; Wallraff, 2005b; Gagliardo et al., 2007).

Our knowledge of familiar landmark navigation has grown substantially with the development and use of portable GPS trackers, which have permitted the reconstruction of homing pigeon flight paths with remarkable precision, and the correlation of variations in flight tracks with visual features in the environment (Biro et al., 2004; Lipp et al., 2004; Lau et al., 2006). The conclusion that emerges from these studies [but see Wiltschko et al. (2007)] is that visual landmarks are routinely used by pigeons to guide their homing flights over familiar areas. Notably, lesions to the hippocampal formation (HF) of homing pigeons interferes precisely with that portion of the homing flight expected to be guided by familiar visual landmarks [see Bingman & Cheng (2005); Bingman et al. (2005) for reviews], for example as pigeons approach the home loft (Gagliardo et al., 2007). HF lesions typically do not affect the navigational map and compass mechanisms used to home from more distant, unfamiliar areas (Bingman et al., 1984). More specifically, the pigeon HF is necessary when familiar landmarks are used in a map-like fashion to directly guide the flight paths of pigeons, but not when landmarks are used to recall a compass direction home (Gagliardo et al., 1999). However, with the exception of a modest telemetry study (Bingman & Mench, 1990), the previous work examining the relationship between HF and landmark navigation in homing pigeons has relied on the traditional experimental procedures of recording vanishing bearings and homing times. Therefore, little is known about how the familiar-area flight paths of homing pigeons with and without an HF may differ, and what those differences may reveal about the properties of an HF-dependent, familiar landmark map, which would enable an individual to re-orient homewards following a navigational error.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

General procedure

Fifty pigeons, 2–3 years of age and hatched at the Arnino field station, Pisa, Italy, were used in the study. The pigeons were bred as free flyers and were kept according to Italian law on animal welfare. The experiments took place with one group of pigeons in 2006 and another in 2007. Pigeons from both years participated in Experiment 1; only the 2007 pigeons participated in Experiment 2. The pigeons were divided into two experimental groups: intact control pigeons (= 25, 11 of which were used in 2006), and pigeons subjected to bilateral ablation of the HF (= 25, 11 of which were used in 2006). Prior to experimental training, and at least 1 month after surgery for the HF-lesioned pigeons (see below), birds were equipped with a PVC dummy weight, similar in dimension and weight to the GPS data logger that they would be carrying, in order to accustom them to flying with a load. The dummy was attached to a pigeon’s back by means of a Velcro strip glued on the feathers, which had been trimmed. The pigeons were then subjected to a series of training releases from two sites located at opposite directions and at different distances with respect to the home loft (Livorno, home 341°, 11.9 km; La Costanza, home 190°, 17.2 km).

Surgery

The HF-lesioned pigeons were first anesthetized with an intramuscular injection of 20% chloral hydrate (2 mL/kg body weight). The lesion target coordinates were stereotaxically identified according to the pigeon brain atlas of Karten & Hodos (1967). Bilateral aspiration lesions were targeted to the hippocampus and parahippocampus. The procedures used were identical to those described in Bingman et al. (1984) and Gagliardo et al. (1999). The project was approved by the Scientific Ethics Committee of the University of Pisa (CASA), and was in accordance with the NIH Guide for the Care and Use of Animals.

GPS data logger

We used miniature GPS data loggers (http://www.technosmart.eu) for recording the positional data of flying birds with an accuracy of about 4 m (Steiner et al., 2000; Lipp et al., 2004). For the current study, the GPS data loggers stored one position fix every 5–10 s. However, occasionally, some devices were, for a short period, unable to receive a satellite signal. During such gaps, straight flight paths were assumed between interrupted fixation points. The position fixes stored by a GPS data logger include latitude, longitude, and time of recording. The devices also provide information about altitude, but with insufficient precision to allow a reliable analysis. The tracks for each pigeon for each recorded release were visualized with mapinfo software (One Global View, Troy, NY, USA).

Training releases

Control and HF-lesioned pigeons were released seven times from each of the two training sites of Livorno and La Costanza. The birds were given group training (all pigeons released together), except for the last training release from each site, when they were released singly. During the training releases, six control and seven HF-lesioned pigeons were lost.

Experiment 1

After the pigeons had completed the training releases, each bird (19 control and 18 HF-lesioned pigeons pooled from 2006 to 2007) was equipped with a GPS data logger and subjected to two experimental releases with recorded flight paths from each training site; one just prior to being phase-shifted (essentially another training release) and one after being phase-shifted. For the phase shift, the birds were shifted 6 h fast for at least 6 days. Phase-shifting birds 6 h fast reliably leads to a counter-clockwise shift in orientation as compared with non-shifted birds when the sun compass is used for orientation. Therefore, the aim of phase-shifting was to purposely induce an initial orientation error during the test release. The error would emerge as a consequence of the demonstrated preference of pigeons to initially rely on their navigational map and coupled sun compass to determine a homeward bearing before engaging in the hypothesized corrective re-orientation behavior based on their familiarity with local landmarks [see Holland (2003) for a more complete review examining the relationship between navigational map and compass mechanisms and navigation by familiar landmarks]. Just prior to release, the dummy on the back of each pigeon was replaced with a GPS data logger. Each pigeon was released singly, with at least 30 min between releases. All the experimental releases took place in sunny conditions, with no or light wind.

Experiment 2

For the 2007 pigeons only, after having completed the two experimental releases of Experiment 1, seven control and seven HF-lesioned pigeons continued to be housed in the phase-shift room/condition and subsequently subjected, while under continual phase shift, to three more training releases (with dummy weight) and a third test release with GPS data loggers in series from each release site. During the entire period of extended training under phase shift and the third test release from each site, which lasted for approximately 3 weeks, each bird was released singly, and, once homed, was quickly re-housed in the phase-shift room to maintain a ‘permanent’ phase shift. If a pigeon returned home during its subjective night, it was kept in the phase-shift room for at least 3 days before being released again. The training and third test release from Livorno were completed before the series from La Costanza.

Quantitative analyses and statistical procedures

For each track recorded, we determined the directional bearing relative to the release site at the first point when a pigeon was every kilometer away from the release site. More points were taken from La Costanza (= 17), because it is further away from home than Livorno (= 11). Note that, depending on the flight track of a pigeon, later points taken, for example 9 km from Livorno or 15 km from La Costanza, could be close to home if a pigeon was well oriented homewards, or a considerable distance from home if they oriented poorly. For the tracks recorded under the phase shift of Experiments 1 and 2, we calculated the expected deflection away from home, on the basis of sun-compass use, by taking into account sun azimuth at the time when a bird crossed each distance boundary for the first time. For each pigeon, the angular difference between its actual bearing and expected, deflected bearing was determined at each point and expressed as a percentage of expected deflection (again, on the basis of sun-compass use). Analyses were carried out using both (i) the direction home and (ii) the mean direction for each experimental group using the non-phase-shifted GPS data from the first release of Experiment 1 at each kilometer from the release site. (Note that we chose to use the group mean bearing at each distance rather each individual’s direction, because we were unable to reconstruct the non-shifted tracks of several pigeons in both groups.) As an illustrative example, at 4 km from the Livorno release site, the directional bearing of a pigeon would be expected to have a deflection of 100° relative to the home direction based on the phase-shift treatment and sun-compass use. However, assume that a tracked pigeon’s recorded bearing at 4 km was only 10° counter-clockwise from the homeward direction. The 10° deflection in the expected phase-shift direction would result in a percentage deflection score of 10% (note that a 10° deflection opposite/clockwise to the expected phase-shift direction would have resulted in a score of −10%; however, in the analysis, the absolute value was considered). Scores close to 0% would therefore indicate a directional bearing oriented towards the direction home or similar to the group flight bearing taken during the non-phase-shifted release, and, more importantly, indicate corrective re-orientation. Scores close to 100% would indicate little or no corrective re-orientation. In order to statistically compare the deviation (expressed as percentage of the expected deflection) of the two experimental groups, we used linear mixed models (Pinheiro et al., 2008), with treatment as the fixed factor, and subjects and distance from the release site as random factors. The AR(1) correlation structure was used to take into account the autocorrelation of the data. When the model was used to analyse the deviation from home displayed by the two experimental groups released in the non-shifted condition, a logarithmic transformation was applied to the data.

Histology and lesion reconstruction

To assess the extent of the lesion damage, 11 of the 13 HF-lesioned pigeons that yielded data were killed for histology (the remaining two birds were lost during the course of the study). The birds were deeply anesthetized with an overdose of a 20% solution of chloral hydrate, and perfused intracardially with 10% formalin. Once extracted, the brains were cut coronally, in 50 μm sections, with a freezing sliding microtome. The sections were stained with cresyl violet, and, with the aid of a macroprojector, the lesions were reconstructed on standard coronal sections derived from the atlas of Karten & Hodos (1967). The range of lesion damage for each group was visualized as a summary figure.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Experiment 1: homing prior to phase shift

Table 1 shows the median deflection values of the control and HF-lesioned pigeons that were successfully recorded when the pigeons were released prior to phase shift (therefore, no percentage expected deflection based on a phase-shift treatment was calculated) from Livorno (control, = 12; HF-lesioned, = 11) and La Costanza (control, = 9; HF-lesioned, = 8) (see also Figs 2, 3, 5, 6, 8 and 9 for representative, actual flight paths). In general, the median angular deflection scores were small for the individuals of both groups, indicating that the birds were well oriented homewards. On examination of the angular deflection scores of the two groups as the homing flight progressed from both Livorno and La Costanza (Fig. 1), no significant differences were found between the flight paths of the HF-lesioned and control pigeons (Livorno, F1,21 = 0.017, = 0.89; La Costanza, F1,15 = 0.71, = 0.41). As would be expected, the magnitude of the angular deflection with respect to home diminished as the pigeons approached the home loft (Livorno, F1,228 = 106.23, < 0.0001; La Costanza, F1,270 = 101.17, < 0.0001), but no interaction between the treatment and the distance from the release site was found (Livorno, F1,228 = 3.34; = 0.06; La Costanza, F1,270 = 0.03; = 0.85). Both groups tended to be attracted by the coast during their homing flight from Livorno, and this resulted in a small counter-clockwise deflection with respect to the home direction when they were released from Livorno. An initially more pronounced clockwise deviation was observed when the pigeons were released from La Costanza. In conclusion, by the end of training, both control and HF-lesioned pigeons learned to take almost straight flight paths to the home loft from both training sites. The critical question was whether the learned spatial representations would enable corrective re-orientation following navigational error.

Table 1.   Releases from Livorno and La Costanza without phase-shift
Releases from LivornoReleases from La Costanza
ControlsHF-lesionedControlsHF-lesioned
No.Deflection (%)No.Deflection (%)No.Deflection (%)No.Deflection (%)
  1. For each subject (controls and HF-lesioned), the median percentage angular deflection from the home direction is given, based on its GPS-recorded track from Livorno and La Costanza sampled at every kilometer from the release site. Scores close to 0% indicate better-oriented homeward tracks. The first and the last quartile deflection values for each recorded track are given in parentheses. HF, hippocampal formation.

4151 (0, 5)4101 (0, 2)3580 (−6, 12)3770 (−1, 5)
397−1 (−5, 0)A15−2 (−12, 3)3781 (−4, 7)7660 (−2, 1)
2144 (0, 9)357−1 (−6, 4)4155 (2, 8)4108 (4, 15)
574−4 (−21, 0)563−5 (−6, −2)5058 (4, 16)6926 (2, 8)
358−5 (−3, 12)667−5 (−21, −2)3878 (3, 15)1106 (1, 11)
521−6 (−11, −1)493−6 (−13, −3)66615 (2, 26)8668 (3, 15)
505−7 (−9, −3)359−5 (−8, −1)62314 (4, 25)35711 (4, 16)
417−8 (−12, −3)766−4 (−9, 0)21415 (9, 46)359−32 (−38, −19)
378−3 (−7, −2)866−7 (−8, −4)52116 (5, 35)
623−6 (−25, −3)377−8 (−14, −7)
666−18 (−27, −10)11014 (11, 19)
578−17 (−23, −8)
image

Figure 2.  Experiment 1: GPS flight-path reconstructions of four control (C) (top) and four hippocampal formation (HF)-lesioned (bottom) pigeons from Livorno. From left to right for each group, the first track is from the pigeon that was best homeward oriented, the second is from the pigeon at the first quartile, the third is from the pigeon at the median quartile, and the fourth is from the pigeon at the third quartile (see Table 2). Thin black lines represent the flight paths taken prior to the phase-shift manipulation. Thick black lines represent the flight paths taken following the phase-shift treatment. The triangle represents the Livorno release site, and the circle the home loft. The identity of each pigeon is also included, and 1 km scale bars are shown.

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image

Figure 3.  Experiment 1: GPS flight-path reconstruction of hippocampal formation (HF)-lesioned pigeon HF667, released from Livorno, which performed an extraordinary flight out to sea before returning home. See Fig. 2 for further explanation of the figure.

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image

Figure 5.  Experiment 1: GPS flight-path reconstructions of four control and four hippocampal formation (HF)-lesioned pigeons from La Costanza. The triangle represents the La Costanza release site, and the circle the home loft. See Fig. 2 for further explanation of the figure.

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image

Figure 6.  Experiment 2: GPS flight-path reconstructions of two control (C) (top) and two hippocampal formation (HF)-lesioned (bottom) pigeons, released from Livorno after extended training while under continual phase shift. The pigeons selected as representative cases were the second (left) and fourth (right) best homeward-oriented pigeons from each group (see Table 4). Thin black lines represent the flight paths taken prior to the phase-shift manipulation. Thick black lines represent the flight paths taken following the phase-shift treatment of Experiment 1. Thick gray lines represent the flight paths taken following extended training under continual phase shift (the focus of Experiment 2). See Fig. 2 for further explanation of the figure.

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image

Figure 8.  Experiment 2: GPS flight-path reconstructions of two control (C) (top) and two hippocampal formation (HF)-lesioned (bottom) pigeons, released from La Costanza after extended training while under continual phase shift. The pigeons selected as representative cases were the second (left) and fourth (right) best homeward-oriented pigeons from each group (see Table 5). Thin black lines represent the flight paths taken prior to the phase-shift manipulation. Thick black lines represent the flight paths taken following the phase-shift treatment of Experiment 1. Thick gray lines represent the flight paths taken following extended training under continual phase shift (the focus of Experiment 2). The triangle represents the La Costanza release site. See Fig. 2 for further explanation of the figure.

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image

Figure 9.  Experiment 2: GPS flight-path reconstructions of hippocampal formation (HF)-lesioned pigeons HF110 and HF563, released from La Costanza. The tracks are examples of HF-lesioned pigeons that overflew the latitude of the home loft during the flight home when released following extended training under continual phase shift. The triangle represents the La Costanza release site. See Fig. 8 for further explanation of the figure.

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image

Figure 1.  Mean deviation from the home direction taken every kilometer from the release site when pigeons were released from Livorno (A) and La Costanza (B) under non-phase-shifted conditions. Standard errors are reported. HF, hippocampal formation; C, control.

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Experiment 1: re-orienting homewards

Livorno

From Livorno, we obtained 12 analysable tracks following phase shift for both the control and HF-lesioned groups. Visual inspection of the flight tracks of the pigeons reveals a striking difference in the ability of the control and HF-lesioned pigeons to re-orient their flights towards home (representative flight tracks are shown in Figs 2, 3 and 6). This difference is also evident in the quantitative data of Table 2 and Fig. 4A.

Table 2.   Experiment 1: release from Livorno
ControlsHF-lesioned
No.Deflection from home direction expected with phase shift (%)Deflection from previous control flight (%)No.Deflection from home direction expected with phase shift (%)Deflection from previous control flight (%)
  1. For each subject (C, control; HF, hippocampal formation-lesioned), two median percentage deflections are given, based on its GPS-recorded track from Livorno. During the return home, a directional bearing was determined on the first occasion when the pigeon reached each successive kilometer distance from the release site. For each pigeon, a median bearing was then calculated from this sequence of readings (= 11 from Liverno) and used to compute, firstly, a percentage deflection (relative to the expected direction based on the phase-shift treatment) away from the home direction and, secondly, a percentage deflection relative to the group median bearing recorded at the same distances during a previous, non-phase-shifted control flight. Scores close to 0% indicate flight tracks oriented towards home, scores close to 100% indicate flight tracks that were consistently deflected in the direction expected with the phase-shift treatment and sun-compass use, and scores of more than 100% indicate flight tracks with greater deflections than those expected with the phase-shift and sun-compass use. The first and the last quartile deflection values for each recorded track are given in parentheses. HF, hippocampal formation.

5744 (2, 23)0 (−1, 17)4933 (1, 118)0 (0, 108)
6235 (4, 86)3 (1, 80)A1576 (35, 128)73 (32, 122)
41711 (5, 66)7 (3, 61)35980 (79, 83)76 (75, 81)
66616 (9, 98)11 (5, 89)41085 (41, 82)80 (39, 85)
57820 (10, 35)17 (5, 22)66798 (87, 103)94 (84, 100)
37821 (11, 49)16 (8, 42)866108 (9, 111)105 (9, 108)
35820 (6, 33)16 (3, 26)377109 (105, 113)105 (103, 107)
41567 (56, 102)58 (49, 98)357115 (11, 136)112 (9, 31)
521101 (14, 104)95 (11, 98)110120 (9, 134)117 (6, 128)
214101 (80, 112)96 (81, 114)563118 (110, 129)117 (57, 124)
505108 (106, 110)103 (101, 107)580121 (118, 124)117 (116, 124)
397123 (115, 125)119 (107, 120)766151 (58, 151)145 (54, 148)
image

Figure 4.  Experiment 1: first phase-shift release, from Livorno (A) and from La Costanza (B). Mean percentage angular deflection scores taken every kilometer from the release site calculated using the home direction as reference. Standard errors are reported. HF, hippocampal formation; C, control.

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Generally, after flying a relatively short distance, the control birds were able to correct for the initial orientation errors created by the false sun-compass information to orient homewards; this capacity was clearly diminished in the HF-lesioned pigeons. Table 2 shows the individual, median deflection values for each pigeon expressed as a percentage of the expected deflection due to the phase shift (false sun-compass information) and direction based on their group behaviour when not phase-shifted. The HF-lesioned pigeons displayed larger flight-path deflections (median percentage deflection values closer to 100) relative to the home direction than the intact control pigeons (median percentage deflection values closer to 0). Quantitatively, the control birds’ deflection values were distributed bimodally (Table 2). Seven control birds quickly corrected their flight paths homewards and displayed median deflections of 20% or less. Four control birds persisted in flying in the expected (incorrect) phase-shift direction and displayed median deflections of 90% or more. They displayed a marked deviation consistent with the use of the sun compass, and flew south for several kilometers before correcting their routes towards home. By contrast, 11 of 12 HF-lesioned pigeons displayed median deflections of 70% or more, and generally persisted in failing to re-orient homewards for a substantially longer distance than many of the even poorer-correcting control pigeons. One noteworthy qualitative difference between the control and HF-lesioned pigeons is that only HF-lesioned pigeons were ever found to fly over the sea (Figs 2 and 6; see the particularly interesting track of pigeon HF667 in Fig. 3). Control pigeons typically followed the coast either after correcting their flight path homewards (north) or when deviating south.

The statistical analysis of the groups’ angular deflection with respect to home during the progression of the homing flight (Fig. 4A; note that only the data with respect to the home direction are presented, because the data with respect to group mean direction when non-shifted are very similar) revealed a significant difference between the control and HF-lesioned pigeons (F1,22 = 9.20, < 0.006, and F1,22 = 9.59, = 0.005, taking the non-shifted mean direction and the home direction as reference, respectively), further demonstrating the poor corrective behavior of the HF-lesioned birds. The magnitude of the deflection diminished in both groups as the birds approached the home loft (F1,238 = 109.76, < 0.0001, and F1,238 = 35.80, < 0.0004, taking the non-shifted mean direction and the home direction as reference, respectively), but no significant interaction between treatment and distance from the release site was found (F1,238 = 3.62, = 0.057, and F1,238 = 0.37, = 0.54).

La Costanza

From La Costanza, we obtained 11 analysable tracks following phase shift for both the control and HF-lesioned groups (Table 3 and Figs 5, 8 and 9). As compared with Livorno, visual inspection of the flight tracks from La Costanza reveals a similar pattern of between-group differences, which were perhaps less striking because of the lack of extended flights over the sea. This impression is supported by the quantitative data summarized in Table 3 (individual performance) and Fig. 4B (group performance).

Table 3.   Experiment 1: release from La Costanza
ControlsHF-lesioned
No.Deflection from home direction expected with phase shift (%)Deflection from previous control flight (%)No.Deflection from home direction expected with phase shift (%)Deflection from previous control flight (%)
  1. Explanation as in Table 2, with the exception that medians were calculated on the basis of directional bearings taken at every kilometer away from the release site (= 17 from La Costanza), and negative scores indicate deflections in the direction opposite to that expected with phase-shift treatment and sun-compass use.

574−3 (−5, −2)4 (2, 8)66712 (3, 13)11 (7, 14)
539−6 (−14, 3)5 (5, 8)A1527 (17, 37)29 (16, 48)
3789 (3, 15)14 (12, 20)69235 (19, 40)41 (32, 48)
60820 (8, 24)24 (19, 34)41039 (38, 45)39 (38, 50)
21422 (8, 26)27 (19, 34)35740 (33, 44)42 (34, 45)
41728 (20, 33)39 (24, 41)76647 (46, 51)48 (45, 56)
41536 (32, 37)41 (40, 44)86648 (29, 53)51 (50, 56)
35836 (34, 38)41 (38, 49)37775 (72, 79)75 (73, 81)
50544 (36, 68)49 (40, 81)35977 (77, 78)81 (78, 82)
38746 (43, 50)52 (43, 65)11082 (75, 84)86 (74, 88)
521−60 (−76, 4)−46 (−68, 4)563−99 (−101, −99)−95 (−99, −84)

Six control pigeons displayed deflections of 30% or less of the expected deflection based on the phase-shift treatment, using as reference both the homeward direction and direction based on their group behavior when not phase-shifted. Notable also is that whereas the control pigeons’ deflection values were bimodally distributed from Livorno, the variation in the magnitude of deflection from La Costanza appeared continuous (Table 3). By contrast, only two HF-lesioned pigeons displayed a deflection of 30% or less (Table 3). The statistical analysis applied to the group performance data of Fig. 4B, in contrast to Livorno (Fig. 4A), did not reveal a significant difference between the control and HF-lesioned pigeons from La Costanza (F1,20 = 1.93, = 0.18, and F1,20 = 2.14, = 0.15, taking the non-shifted mean direction and the home direction as reference, respectively). We attribute the lack of a statistical effect from La Costanza to the control pigeons, which appeared to correct for the induced navigational error later in the homing flight as compared with Livorno [contrast the early portion of the flight home between the two groups from Livorno (Fig. 4A) and La Costanza (Fig. 4B)]. Also, from La Costanza the percentage deflection scores diminished as the pigeons approached the home loft (F1,338 = 25.36, < 0.0001, and F1,338 = 58.63, < 0.0001, taking the non-shifted mean direction and the home direction as reference, respectively), but no significant interaction between treatment and distance from release site was revealed (F1,338 = 2.80, = 0.09, and F1,338 = 1.44, = 0.2).

Experiment 2: learning under phase shift

Livorno

Experiment 2 involved giving some pigeons from the 2007 group additional training from the release sites, while living under continual phase shift, to determine whether continued training would enable them, particularly the HF-lesioned pigeons, to learn to better compensate for the orientation error induced by the phase-shift treatment. From Livorno, six control and seven HF-lesioned pigeons produced tracks that were suitable for quantitative analysis (individual performance in Table 4 and group performance in Fig. 7). Examination of the flight tracks (representative tracks can be found in Fig. 6) reveals that virtually all of the pigeons, regardless of group, tended to be better at re-orienting their flight homewards than their first flight in the phase-shifted condition (Table 4). The ability of both experimental groups to re-orient after training in continual phase shift is also evident in Fig. 7A (compare with Fig. 4A), which shows the group mean percentage deflection at every kilometer from the release site. In fact, the statistical analysis of the group data (Fig. 7A) did not reveal a significant difference between the control and HF-lesioned pigeons (F1,11 = 0.48, = 0.5, and F1,11 = 1.34, = 0.27, taking the non-shifted mean direction and the home direction as reference, respectively). The magnitude of the deflection decreased as the pigeons approached home (F1,128 = 14.18, < 0.001, and F1,128 = 35.12, < 0.0001), but no significant interaction between treatment and distance from release site was revealed (F1,128 = 0.64, = 0.42, and F1,128 = 0.59, = 0.4).

Table 4.   Experiment 2: release from Livorno
ControlsHF-lesioned
No.Deflection from home direction expected with phase shift (%) Deflection from previous control flight (%)No.Deflection from home direction expected with phase shift (%)Deflection from previous control flight (%)
  1. Explanation as in Tables 2 and 3.

2142 (2, 3)0 (0, 1)3572 (2, 4)0 (−3, 1)
521−3 (−9, 0)−7 (−16, −2)4106 (5, 6)3 (0, 3)
4153 (2, 14)1 (−1, 6)56311 (8, 14)12 (6, 13)
3786 (4, 23)3 (2, 17)76618 (7, 30)13 (6, 19)
5056 (5, 10)3 (0, 5)35917 (10, 31)15 (6, 22)
3587 (2, 13)3 (0, 5)86620 (14, 23)10 (7, 20)
11020 (12, 28)15 (10, 22)
image

Figure 7.  Experiment 2 from Livorno (A) and La Costanza (B). Mean percentage angular deflection scores taken every kilometer from the release site calculated using the home direction as reference. Standard errors are reported. HF, hippocampal formation; C, control.

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La Costanza

From La Costanza, six tracks from each experimental group were suitable for quantitative analysis (representative tracks can be found in Figs 8 and 9). Overall, pigeons from both groups tended to show better re-orientation homewards after the additional training under continual phase shift, but the HF-lesioned pigeons continued to be poorer at it (see Table 5, which summarizes the individual, median percentage deflection values). Most salient in this context is that all six control pigeons approached the home loft from the north; by contrast, three of six HF-lesioned pigeons approached the home loft from the south after having overflown the latitudinal coordinate of the loft (see Fig. 9 for examples). The pattern observed at the level of individual performance (Table 5) can also be observed at the group level (Fig. 7B). In contrast to Livorno (Fig. 7A), the statistical analysis of the La Costanza group data (Fig. 7B) revealed a significant difference between the control and HF-lesioned pigeons; the HF-lesioned pigeons maintained a greater deflection from the home direction than the intact birds even after training under continual clock-shift conditions (F1,10 = 6.67, = 0.027, and F1,10 = 9.04, = 0.013, taking the non-shifted mean direction and the home direction as reference, respectively). Again, the magnitude of the deflection diminished as the pigeons approached the home loft (F1,190 = 130.79, < 0.0001, and F1,190 = 53.65, < 0.0001), but now a significant interaction between treatment and distance from release site was found (F1,190 = 5.21, = 0.023, and F1,190 = 8.11, < 0.005). We interpret the significant interaction effect as being a consequence of the relatively poorer corrective behavior of the HF-lesioned pigeons early in the homing flight (Fig. 7B).

Table 5.   Experiment 2: release from La Costanza
ControlsHF-lesioned
No.Deflection from home direction expected with phase shift (%)Deflection from previous control flight (%)No.Deflection from home direction expected with phase shift (%)Deflection from previous control flight (%)
  1. Explanation as in Tables 2 and 3.

5213 (0, 7)12 (9, 14)7667 (−1, 26)10 (−2, 32)
3586 (4, 14)18 (9, 25)35714 (11, 27)20 (10, 36)
5056 (4, 9)16 (4, 22)41015 (8, 19)17 (8, 24)
3789 (5, 11)16 (6, 28)56318 (15, 19)21 (14, 26)
41511 (9, 21)18 (10, 37)86638 (25, 42)40 (24, 48)
21422 (19, 28)30 (14, 46)11050 (45, 53)56 (50, 57)
Lesion reconstruction

Figure 10 summarizes the brain damage sustained by the 11 sampled HF-lesioned pigeons. The substantial damage to both the hippocampus and parahippocampus subdivisions of the HF was somewhat variable across the 11 subjects. However, no pattern was observed between the extent of HF damage and percentage deflection scores or quality of the flight tracks. For all pigeons, sparing was primarily limited to the most anterior portions of the hippocampus and parahippocampus. In some birds, the lesions extended modestly into either the hyperpallium apicale (formerly hyperstriatum accessorium) or nidopallium (formerly neostriatum).

image

Figure 10.  Summary lesion reconstruction of the 11 sampled hippocampal formation-lesioned pigeons. Black areas identify regions of brain damage common to at least nine of the 11 pigeons; gray areas identify regions of brain damage common to at least four of the 11 pigeons. Numbers on the right indicate anterior–posterior coordinates of the sections (Karten & Hodos, 1967). Abbreviations [from Reiner et al. (2004)]: APH, parahippocampus; CDL, corticoid; E, entopallium; Hp, hyperpallium apicale; HD, hyperpallium densocellulare; M, mesopallium; N, nidopallium; V, ventricle.

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Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The prevailing view of the role of the HF in homing pigeon navigation is that it is important for the learning and operation of a map-like or relational representation of familiar, visual landmarks (Bingman et al., 2005), very much in the spirit of the cognitive map of O’Keefe & Nadel (1978). Prior to the current study, the most compelling evidence in support of our description of HF function in homing was the lost ability of HF-lesioned pigeons to orient their vanishing bearings towards home from a familiar training site following phase shift and anosmic treatment, an ability readily displayed by intact control pigeons (Gagliardo et al., 1999). However, the signature feature of a map-like representation is that it would enable an organism to compute a corrective route to a goal location that would allow it to re-orient towards the goal when displaced from a familiar path. The present study is the first to document an impoverished ability of HF-lesioned pigeons to carry out corrective re-orientation following navigational error. Using a phase-shift manipulation to purposely lead pigeons with an intact navigational map and sun compass to fly in a direction away from home, we tested how readily the pigeons’ familiarity with the landmarks and landscape features in the vicinity of the training sites would enable them to correct for the induced error and re-orient homewards. The use of GPS-tracking technology allowed us to record the flight paths that the pigeons had taken home, and the analyses carried out demonstrated, as predicted, that the control pigeons engaged in corrective, re-orientation behavior more rapidly and efficiently in space than the HF-lesioned pigeons. Arguably, the ability to re-orient following an induced error provides the best evidence for the map-like quality of the familiar landmark navigation used by the intact pigeons, and diminished capacity for map-like corrective behavior following HF lesion.

It should be emphasized that the superior corrective re-orientation behavior of the control pigeons in the present study is fundamentally different from the demonstration that, as compared with HF-lesioned pigeons, control pigeons are more likely to use landmarks to directly guide the flight home, with only modest influence of their sun compass (Gagliardo et al., 1999). Gagliardo et al. (1999) revealed different representational strategies when homing pigeons were constrained to use familiar landmarks to navigate home. In fact, in that study, both intact and HF-lesioned pigeons were anosmic, and therefore forced to rely on familiar landmarks/landscape features to guide their flight home; and they did so in different ways. By contrast, the simultaneous capacity to use both their olfactory navigational map and visual, familiar landmarks for navigation, as in the present study, results in pigeons initially relying on a ‘map and compass strategy’ to return home (Gagliardo et al., 2005). Therefore, in the present study, both phase-shifted control and HF-lesioned pigeons were initially predisposed to rely on their map and compass (erroneous) to compute a homeward bearing.

An interesting feature of the flight paths of some HF-lesioned pigeons was the fact that, despite initially large deviations away from home, they were often able to subsequently take up a homeward bearing while still a considerable distance from the home loft (Figs 2 and 5). We can only speculate on how they were able to correct their flight homewards, but it should be noted that pigeons can rely on a range of navigational mechanisms to return home (Wallraff, 2005a), many of which are not hippocampus-dependent (Bingman et al., 2005). Candidate explanations include correcting for disrupted calibration between their olfactory navigational map and sun compass, or rejection of the sun compass in favor of magnetic compass use.

No sensory manipulation was carried out in the present study, and therefore we cannot be certain that the proposed landmark navigation, as we believe, was based on visual information. However, there is a growing body of evidence demonstrating the importance of vision for navigation over familiar areas and in the vicinity of the home loft (Braithwaite & Guilford, 1991; Biro et al., 2002, 2004; Lipp et al., 2004; Gagliardo et al., 2007) [but see Wiltschko et al. (2007)], and we consider visual landmarks and landscape features to be the primary source of information used by the pigeons to correct for their deflected initial flight trajectories.

These general conclusions notwithstanding, there was notable variability in the performance of the control pigeons both within and between release sites. Using route recorders (less precise ‘route recorders’ were used before the development of the GPS recorders used in the present study), Bonadonna et al. (2000) previously documented that the degree to which homing pigeons rely on familiar landmarks to correct for errors in initial orientation varies among individuals and across release sites. In the current study, the behavior of the control pigeons from Livorno differed from their behavior from La Costanza; for those from Livorno (Table 2), but not for those from La Costanza (Table 3), the deflection scores were bi-modal. What is notable about this difference is that the phase shift biased the pigeons towards the sea from Livorno but inland from La Costanza. The behavior of pigeons from Livorno, therefore, can be explained in part by the control pigeons recognizing that the sea was a salient landscape boundary and that the loft was on the ‘land side’ (the home loft is only a few kilometers away from the coast). The majority of the control birds that reached the coast subsequently re-oriented northwards towards home, but some initially flew south along the coast. Such a salient landscape boundary was not present from La Costanza, which would explain the absence of a bi-modal distribution.

Our interpretation of the control pigeon behavior leads to two noteworthy speculations. First, in discussing navigation from familiar areas, point source landmarks (a specific mountain, distinctive building, power plant, etc.) are often considered to be important sources of navigational information. However, the proposed importance of the sea as a landscape boundary suggests that rather than point source landmarks, coarse landscape features and the ease with which different landscape features may be segmented from other landscape features may be more important [see also Wallraff (2005a)]. Consistent with this idea are recent modeling and GPS route recorder data from Lau et al. (2006) showing that the flight paths of pigeons can be influenced by landscape features such as variations in the distribution of colors associated with landscape boundaries. Second, it was extraordinary to observe that seven of the 12 HF-lesioned pigeons (no control pigeons) spent a considerable amount of time flying over the sea on their way home from Livorno. If our assumption that the coastline is a segmental-landscape boundary used as an important source of navigational information is correct, then the behavior of the HF-lesioned pigeons suggests that they are specifically diminished in their capacity to use such landscape features for navigation.

The finding that sensitivity to landscape boundaries may be important for HF-dependent representations of space in homing pigeons is reminiscent of rat hippocampus involvement in navigation. For example, hippocampal place cells in rats are sensitive to the geometric relationships among boundary walls of a laboratory enclosure (O’Keefe & Burgess, 1996; Lever et al., 2002). Furthermore, hippocampus lesions in rats can influence how geometry can be used to locate a goal (Tommasi & Save, 2005). It is noteworthy that HF lesions in pigeons also diminish the importance of geometric information for locating a goal in a laboratory environment (Vargas et al., 2004; Bingman et al., 2006). Assuming that landscape boundaries in nature serve as geometric features similar to wall boundaries in a laboratory setting, then a common property of the rat and pigeon hippocampus-dependent spatial representations would be their use of ‘boundaries’ to define space.

The HF-lesioned birds, after subsequent training while living under continual phase shift, improved their ability to orient homewards, although their performance never reached the level of the control pigeons. It should be emphasized that HF lesions do not eliminate the capacity of homing pigeons to return home; they still possess an operational navigational map and compass mechanism, and are able to use landmarks as cues to recall a previously learned sun-compass direction home [see Bingman et al. (2005) for a review]. Therefore, we do not interpret the improved performance of the HF-lesioned pigeons as an indication that they learned the kind of flexible map-like representation of familiar landmarks and landscape features possessed by pigeons with an intact HF. The relatively impoverished quality of what the HF-lesioned pigeons learned with continued training is attested to by the observation that, from La Costanza, three of the six lesioned pigeons overflew the latitude of the home loft (none of six control birds did). But what did the HF-lesioned pigeons learn? In our view, the most parsimonious explanation is that continued training under phase shift enabled the HF-lesioned pigeons to acquire a home-oriented, navigational route associated with local features of unspecified sensory modality in a manner similar to that described by Foà & Albonetti (1980). In this context, it is noteworthy that, with the additional training, the HF pigeons learned to home better from Livorno than from La Costanza (compare Fig. 7A and B), perhaps because they learned to not cross the landscape boundary of land and sea. However, an alternative explanation is that the improved navigation by the HF pigeons resulted simply from a re-calibrated sun compass, perhaps based on a reference supplied by their magnetic compass (Wiltschko et al., 1976, 1984), a possibility that is nonetheless contradicted by the findings of Foà & Albonetti (1980).

In summary, corrective re-orientation following navigational error is perhaps the most salient adaptive quality of a map-like representation of space. It is this capacity that makes the maps of migratory birds so spectacular (Thorup et al., 2007). The data presented in the current study offer compelling support for the hypothesis that the capacity for corrective re-orientation in homing pigeons is dependent on an intact hippocampus. It therefore follows that, in the context of navigation, the role of the hippocampus is bound to the idea of relational representations of space and the enduring notion of a ‘cognitive map’ (O’Keefe & Nadel, 1978).

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We wish to thank Fabio Chini and Andrea Guidi for their help in training the pigeons, Daniele Santerini for preparation of the figures, and Dimitri Giunchi for help with the statistics. This work was partially supported by NSF (USA) grant IBN-0075891 to V. P. Bingman and by the Association Ornis Italica.

Abbreviation
HF

hippocampal formation

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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