Functional asymmetry of left and right avian piriform cortex in homing pigeons' navigation

It has been shown that homing pigeons rely on olfactory cues to navigate over unfamiliar areas and that any kind of olfactory impairment produces a dramatic reduction of navigational performance from unfamiliar sites. The avian piriform cortex is the main projection field of olfactory bulbs and it is supposed to process olfactory information; not surprisingly bilateral lesions to this telencephalic region disrupt homing pigeon navigation. In the present study, we attempted to assess whether the left and right piriform cortex are differentially involved in the use of the olfactory navigational map. Therefore, we released from unfamiliar locations pigeons subjected, when adult, to unilateral ablation of the piriform cortex. After being released, the pigeons lesioned to the right piriform cortex orientated similarly to the intact controls. On the contrary, the left lesioned birds were significantly more scattered than controls, showing a crucial role of the left piriform cortex in processing the olfactory cues needed for determining the direction of displacement. However, both lesioned groups were significantly slower than controls in flying back to the home loft, showing that the integrity of both sides of the piriform cortex is necessary to accomplish the whole homing process.     

Navigation‐induced ZENK expression in the olfactory system of pigeons (Columba livia)

A large body of evidence indicates that pigeons use olfactory cues to navigate over unfamiliar areas with a differential contribution of the left and right hemispheres. In particular, the right nostril/olfactory bulb (OB) and left piriform cortex (Cpi) have been demonstrated to be crucially involved in navigation. In this study we analysed behaviour‐induced activation of the olfactory system, indicated by the expression of the immediate early gene ZENK, under different homing conditions. One experimental group was released from an unfamiliar site, the second group was transported to the unfamiliar site and back to the loft, and the third group was released in front of the loft. To evaluate the differential contribution of the left and/or right olfactory input, the nostrils of the pigeons were either occluded unilaterally or not. Released pigeons revealed the highest ZENK cell density in the OB and Cpi, indicating that the olfactory system is activated during navigation from an unfamiliar site. The groups with no plug showed the highest ZENK cell density, supporting the activation of the olfactory system probably being due to sensory input. Moreover, both Cpis seem to contribute differently to the navigation process. Only occlusion of the right OB resulted in a decreased ZENK cell expression in the Cpi, whereas occlusion of the left nostril had no effect. This is the first study to reveal neuronal activation patterns in the olfactory system during homing. Our data show that lateralized processing of olfactory cues is indeed involved in navigation over unfamiliar areas.     

Hippocampus and homing in pigeons: left and right hemispheric differences in navigational map learning

One-month-old, inexperienced homing pigeons, prior to any opportunity to learn a navigational map, were subjected to either right or left unilateral ablation of the hippocampal formation (HF). These pigeons were then held together with a group of age-matched control birds in an outdoor aviary, where they were kept for about 3 months with the opportunity to learn a navigational map. When subsequently tested for navigational map learning at about 4 months of age posthatching, control and right HF-ablated pigeons were equally good at orienting homeward from distant, unfamiliar locations, indicating successful navigational map learning. By contrast, left HF-ablated pigeons were impaired in orienting homeward, indicating a failure to learn a navigational map. Interestingly, both right and left HF-ablated pigeons displayed impaired homing performance relative to controls. These results suggest that different aspects of homing pigeon navigation may be lateralized to different hemispheres, and in particular, the HF of the different hemispheres. The left HF appears critical for navigational map learning, i.e. determining an approximate direction home from distant, unfamiliar locations. The right HF, and possibly the left HF as well, appear to play an important role in local navigation near the loft, which is likely based on familiar landmarks.     

Evidence for perceptual neglect of environmental features in hippocampal‐lesioned pigeons during homing

The importance of the vertebrate hippocampus in spatial cognition is often related to its broad role in memory. However, in birds, the hippocampus appears to be more specifically involved in spatial processes. The maturing of GPS‐tracking technology has enabled a revolution in navigation research, including the expanded possibility of studying brain mechanisms that guide navigation in the field. By GPS‐tracking homing pigeons released from distant, unfamiliar sites prior to and after hippocampal lesion, we observed, as has been reported previously, impaired navigational performance post‐lesion over the familiar/memorized space near the home loft, where topographic features constitute an important source of navigational information. The GPS‐tracking revealed that many of the lost pigeons, when lesioned, approached the home area, but nevertheless failed to locate their loft. Unexpectedly, when they were hippocampal‐lesioned, the pigeons showed a notable change in their behaviour when navigating over the unfamiliar space distant from home; they actually flew straighter homeward‐directed paths than they did pre‐lesion. The data are consistent with the hypothesis that, following hippocampal lesion, homing pigeons respond less to unfamiliar visual, topographic features encountered during homing, and, as such, offer the first evidence for an unforeseen, perceptual neglect of environmental features following hippocampal damage.     

Bilateral participation of the hippocampus in familiar landmark navigation by homing pigeons

Recent findings indicate a different role of the left and right hippocampal formation (RHF) in homing pigeon navigational map learning. However, it remains uncertain whether the left or the RHF may play a more important role in navigation based on familiar landmarks. In the present study, we attempted to answer this question by experimentally releasing control and left and right hippocampal ablated pigeons from familiar training sites under anosmia, to render their navigational map dysfunctional, and after a phase-shift of the light-dark cycle, to place into conflict a pilotage-like landmark navigational strategy and a site-specific compass orientation landmark navigational strategy. Both left and right hippocampal ablated birds succeeded in learning to navigate by familiar landmarks, and both preferentially relied on sun-compass based, site-specific compass orientation to home. Like bilateral hippocampal lesioned birds, and in contrast to intact controls, neither ablation group adopted a pilotage-like strategy. We conclude that both the left and RHF are necessary if pilotage-like, familiar landmark navigation is to be learned or preferentially used for navigation.     

Interhemispheric transfer of olfactory information in homing pigeon

The role of the anterior commissure in discrimination of and habituation to olfactory stimuli was studied in pigeons by measuring changes in the heart rate. In order to exclude any trigeminal response, we presented odorous stimuli to groups of pigeons with one olfactory nerve cut and either the ipsilateral or the contralateral nostril plugged. When the nostril involved in the experiments was on the same side of the cut olfactory nerve, the pigeons did not show any response, whereas they displayed changes in heart rate when the nostril tested was on the opposite side. In habituation transfer experiments were a control group of pigeons and a group with the anterior commissure cut, both of them subjected to a monolateral habituation training to amylacetate. Later, when the odour was presented to the opposite nostril, both groups maintained the habituation.     

PET shows that odors are processed both ipsilaterally and contralaterally to the stimulated nostril

The olfactory nerve is the only cranial nerve with established ipsilateral primary cerebral anatomical projections. Whether these projections correspond to the functional pathways for monorhinal processing of odor perception is, however, unknown. We therefore studied cerebral blood flow (rCBF) with [15O]butanol-PET in 18 healthy females during monorhinal smelling of single odors (OS) and odorless air (AS). Compared with AS, OS activated right amygdala and piriform cortex (confluent cluster), right orbitofrontal cortex, left insula, right thalamus, and anterior cingulate. A post hoc analysis showed that the first three regions were activated independently of the stimulated side, but that right orbitofrontal rCBF was higher during the right nostril stimulations. Left insula was activated mainly by the right nostril stimuli, and right thalamus by the left nostril stimuli. Odors seem to be processed both ipsi and contralaterally, with a right hemisphere preponderance irrespective of the stimulated nostril.     

Left-hemispheric superiority for visuospatial orientation in homing pigeons

To test for lateralisation of visuospatial orientation during homing, pigeons who had binocularly learned the homeward route from remote release sites were tested monocularly on either their left or their right eye for homing performance. In two experiments with three different release sites, birds using their right eye showed considerably better homing performance. If sun compass information was available, there was no difference in the direction of vanishing. Without this information, a difference between pigeons using their left or right eye emerged. Results show that visuospatial orientation in birds can be lateralised in favour of the left brain hemisphere and lend further support to the view that vision is important for pigeons homing on a familiar route. Cognitive mechanisms which might account for the observed pattern of lateralisation are discussed.     

Asymmetrical olfactory acuity and neuroleptic treatment in schizophrenia

Uni-rhinal olfactory acuity in schizophrenia was investigated in two experiments. The first assessed the presence of a predicted atypical asymmetry of nostril laterality and the second assessed the effect of antipsychotic treatment on the asymmetry. Although olfactory identification impairment has been well documented in schizophrenia, olfactory acuity has been neglected. This may be an oversight as cerebral structures of the mesial temporal lobe important to olfactory perception have often been implicated in the pathophysiology of schizophrenia and it is thus reasonable to postulate a primary impairment of olfactory acuity in schizophrenia. In addition, unmedicated patients with schizophrenia have exhibited asymmetrical laterality favouring the right over the left hemisphere in studies of visual, haptic, and auditory perception, and the few published prospective treatment studies have suggested a reversal of this asymmetry with first generation neuroleptic treatments. In experiment 1 a generalization of the perceptual asymmetry to olfactory acuity was examined by measurement of n-butanol olfactory thresholds with the Connecticut Chemosensory Perception Exam (CCPE) in an unmedicated sample of 17 patients with schizophrenia and 17 age, gender, and handedness matched normal controls. The patient sample showed an asymmetrical impairment of the left nostril that was not apparent in the normal control sample. In experiment 2, the CCPE was administered to a new sample of 10 patients with schizophrenia before and after neuroleptic treatment. The asymmetry observed in experiment 1 was replicated, and the relative advantage of the right nostril shifted to a relative advantage of the left nostril over the course of 8weeks of treatment. Results are discussed in relation to cerebral aspects of schizophrenia and potential implications to cognitive change from treatment.     

Representing the richness of avian spatial cognition: properties of a lateralized homing pigeon hippocampus

Brain organization and its relationship to behavior in any extant species is a reflection of a long evolutionary history of adaptive change. Therefore, it follows that the relationship between the hippocampus and spatial cognition in any species or taxonomic group would be characterized by features adapted to its spatial ecology. Birds are the animal world's supreme navigators, and aspects of their navigational ability are dependent on the integrity of the hippocampal formation. Using the homing pigeon as a model species, we review an accumulating body of data indicating that the avian hippocampus is functionally lateralized. The spatial response properties of left hippocampal neurons, as recorded in freely moving pigeons in a laboratory environment, differ from the response properties of right hippocampal neurons. Left hippocampal lesions generally disrupt navigational behavior under field conditions more than right lesions, while right lesions are more likely to disrupt goal localization behavior under laboratory conditions. We propose that the available data are consistent with a hypothesis of a left hippocampus more involved in navigational processes, and a right hippocampus more involved in representing the locations of events. We also discuss the extent to which the observed hippocampal lateralization should be viewed as an intrinsic property of the hippocampus itself or imposed by the lateralized properties of visual inputs originating in other brain regions. Whatever the nature of the observed hippocampal lateralization, it is likely one adaptive variation in hippocampal organization that supports the extraordinary spatial behavior of birds.     

Congenital olfactory impairment is linked to cortical changes in prefrontal and limbic brain regions

The human sense of smell is closely associated with morphological differences of the fronto-limbic system, specifically the piriform cortex and medial orbitofrontal cortex (mOFC). Still it is unclear whether cortical volume in the core olfactory areas and connected brain regions are shaped differently in individuals who suffer from lifelong olfactory deprivation relative to healthy normosmic individuals. To address this question, we examined if regional variations in gray matter volume were associated with smell ability in seventeen individuals with isolated congenital olfactory impairment (COI) matched with sixteen normosmic controls. All subjects underwent whole-brain magnetic resonance imaging, and voxel-based morphometry was used to estimate regional variations in grey matter volume. The analyses showed that relative to controls, COI subjects had significantly larger grey matter volumes in left middle frontal gyrus and right superior frontal sulcus (SFS). COI subjects with severe olfactory impairment (anosmia) had reduced grey matter volume in the left mOFC and increased volume in right piriform cortex and SFS. Within the COI group olfactory ability, measured with the “Sniffin’ Sticks” test, was positively associated with larger grey matter volume in right posterior cingulate and parahippocampal cortices whereas the opposite relationship was observed in controls. Across COI subjects and controls, better olfactory detection threshold was associated with smaller volume in right piriform cortex, while olfactory identification was negatively associated with right SFS volume. Our findings suggest that lifelong olfactory deprivation trigger changes in the cortical volume of prefrontal and limbic brain regions previously linked to olfactory memory.     

Passive perception of odors and semantic circuits

The sense of smell has been traditionally assumed to be different from other sensory modalities in that odors are encoded perceptually, without a semantic component. Recent findings of improved odor memory upon encoding with verbal cues question this view. Furthermore, familiar odors are easier to remember and discriminate than are unfamiliar ones, and odor familiarity is reported to predict odor naming. To investigate whether familiar odors are processed by different cerebral structures than those that process unfamiliar odors, (15)O H(2)O-positron emission tomography (PET) measurements of cerebral blood flow were carried out in 14 healthy men. The task was passive, birhinal, smelling of familiar odors (FAM), unfamiliar odors (uFAM), and odorless air (AIR). Significant activations (P < 0.05) were calculated using the contrasts FAM-AIR, uFAM-AIR, and FAM-uFAM, and deactivations running these contrasts in the opposite direction. In relation to AIR, both FAM and uFAM activated amygdala, piriform cortex, and parts of anterior cingulate cortex. FAM activated, in addition, left frontal cortex (Brodmann's areas 44,45,47), left parietal cortex incorporating precuneus, and right parahippocampus. Clusters covering parahippocampus and precuneus were observed also in FAM-uFAM. The activation of left frontal cortex and right parahippocampus was positively correlated with familiarity ratings. Smelling of familiar but not unfamiliar odorants seems to engage cerebral circuits mediating memory and language functions, in addition to the engagement of olfactory cortex. Already the most elemental form of odor processing, passive perception thus seems to engage semantic circuits. This is achieved by the ability of odorants to immediately elicit associations and judgments of odor characteristics.     

Unimpaired acquisition of spatial reference memory, but impaired homing performance in hippocampal-ablated pigeons

Hippocampal ablated homing pigeons have been shown to suffer a retrograde spatial reference memory deficit involving a preoperatively acquired homeward orientation response based on local cues around a previously visited release site. Here we report that the postoperative acquisition of such a response is unimpaired. Initially, 25 hippocampal ablated and 11 sham-operated controls were given 5 training releases from each of two sites. In the subsequent experimental releases from the two training sites, the controls and half the hippocampal-ablated pigeons had their navigational maps rendered dysfunctional via an anosmic procedure. Nonetheless, both groups successfully oriented homeward, indicating that the hippocampal-ablated pigeons were unimpaired in the acquisition and implementation of directionally useful information around the training sites to direct a homeward orientation response. The remaining half of the hippocampal-ablated pigeons who were not rendered anosmic, and thus served as controls, also oriented homeward. The data indicate that, for hippocampal-ablated homing pigeons, postoperative acquisition is unimpaired in the same spatial reference memory task where a robust retrograde impairment was observed. However, the hippocampal-ablated pigeons were impaired in the time required to return home, indicating a deficit in homing performance beyond the initial orientation stage.     

Hippocampal participation in navigational map learning in young homing pigeons is dependent on training experience

The homing pigeon navigational map is perhaps one of the most striking examples of a naturally occurring spatial representation of the environment used to guide navigation. In a previous study, it was found that hippocampal lesions thoroughly disrupt the ability of young homing pigeons held in an outdoor aviary to learn a navigational map. However, since that study an accumulation of anecdotal data has hinted that hippocampal-lesioned young pigeons allowed to fly during their first summer could learn a navigational map. In the present study, young control and hippocampal-lesioned homing pigeons were either held in an outdoor aviary or allowed to fly during the time of navigational map learning. At the end of their first summer, the birds were experimentally released to test for navigational map learning. Independent of training experience, control pigeons oriented homeward during the experimental releases demonstrating that they learned a navigational map. Surprisingly, while the aviary-held hippocampal-lesioned pigeons failed to learn a navigational map as reported previously, hippocampal-lesioned birds allowed flight experience learned a navigational map indistinguishable from the two control groups. A subsequent experiment revealed that the navigational map learned by the three groups was based on atmospheric odours. The results demonstrate that hippocampal participation in navigational map learning depends on the type of experience a young bird pigeon has, and presumably, the type of navigational map learned.     

Homing behavior of hippocampus and parahippocampus lesioned pigeons following short-distance releases

The avian hippocampal formation has been proposed to play a critical role in the neural regulation of a navigational system used by homing pigeons to locate their loft once in the familiar area near home. In support of this hypothesis, the homing performance of pigeons with target lesions of either the hippocampus or parahippocampus was found to be impaired compared to controls following releases of about 10 km. Further, radio tracking revealed that the in-flight behavior of the hippocampal lesioned homing pigeons was characterized by numerous direction changes and generally poor orientation with respect to the home loft. The results identify a local navigational impairment on the part of the hippocampal lesioned pigeons in the vicinity of the loft where landmark cues are thought to be important. Additionally, target lesions of the hippocampus or parahippocampus were found to be similarly effective in causing homing deficits.     

Impaired retention of preoperatively acquired spatial reference memory in homing pigeons following hippocampal ablation

Hippocampal-parahippocampal-ablated homing pigeons have been shown to suffer a retrograde loss of information used in the recognition of their home loft. Here we report that the range of retrograde deficits includes spatial reference memory in the form of information gained from repeated training sites that can be used to direct a homeward orientation response. Following 8 training releases from each of two sites, 28 of 42 homing pigeons underwent hippocampal-parahippocampal ablation. In the subsequent test releases from the two sites, untreated controls whose navigational map was rendered temporarily dysfunctional by an anosmic procedure showed no impairment in determining the home direction, indicating the successful retention and utilization of directionally useful information around the release sites. Hippocampal-ablated controls who were not rendered anosmic and thus had access to their navigational map also showed no impairment in determining the home direction, indicating no general impairment in initial orientation as a result of hippocampal ablation. In contrast, hippocampal-ablated pigeons whose navigational map was rendered temporarily dysfunctional failed to successfully orient homeward from the training sites, indicating impairment in the retention and/or implementation of directional information gathered at the release sites during training. The data reveal a spatial reference memory deficit involving pre-ablation acquired directional information in homing pigeons following hippocampal ablation.     

Effects of monocular viewing on orientation in an arena at the release site and homing performance in pigeons

Orientation and homing performance of pigeons with the left or right eye occluded were assessed in an arena at the release site and during the subsequent homing flight. Three release sites near Pisa, Italy, were used. Compared to binocular controls, monocular birds showed a bias in orientation towards the side of the viewing eye. In the arena, this bias was considerable and the mean deviation corresponded to the angle of the optical axis, suggesting a systematic error in visual representation during directional orientation. During flight after leaving the arena the directional bias decreased and the homeward orientation increased. While there was a slight lateralization of overall homing performance in favour of the right eye, there was no lateralization in directional orientation in the arena or at vanishing. Our results show that navigational mechanisms in either brain hemisphere profit from information obtained before take off and while flying over the release site. The existence and degree of lateralization is discussed in comparison to other studies that investigated homing under monocular viewing conditions.     

Hippocampal-dependent familiar area map supports corrective re-orientation following navigational error during pigeon homing: a GPS-tracking study

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.     

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. © 2015 Wiley Periodicals, Inc.     

A lateralized avian hippocampus: preferential role of the left hippocampal formation in homing pigeon sun compass-based spatial learning

The hippocampal formation (HF) plays a crucial role in amniote spatial cognition. There are also indications of functional lateralization in the contribution of the left and right HF in processes that enable birds to navigate space. The experiments described in this study were designed to examine left and right HF differences in a task of sun compass-based spatial learning in homing pigeons (Columba livia). Control, left (HFL) and right (HFR) HF lesioned pigeons were trained in an outdoor arena to locate a food reward using their sun compass in the presence or absence of alternative feature cues. Subsequent to training, the pigeons were subjected to test sessions to determine if they learned to represent the goal location with their sun compass and the relative importance of the sun compass vs. feature cues. Under all test conditions, the control pigeons demonstrated preferential use of the sun compass in locating the goal. By contrast, the HFL pigeons demonstrated no ability to locate the goal by the sun compass but an ability to use the feature cues. The behaviour of the HFR pigeons demonstrated that an intact left HF is sufficient to support sun compass-based learning, but in conflict situations and in contrast to controls, they often relied on feature cues. In conclusion, only the left HF is capable of supporting sun compass-based learning. However, preferential use of the sun compass for learning requires an intact right HF. The data support the hypothesis that the left and right HF make different but complementary contributions toward avian spatial cognition.