Olfactory lateralization in homing pigeons: initial orientation of birds receiving a unilateral olfactory input

It has been shown that homing pigeons (Columba livia) rely on olfactory cues to navigate from unfamiliar locations. In fact, the integrity of the olfactory system, from the olfactory mucosa to the piriform cortex, is required for pigeons to navigate over unfamiliar areas. Recently it has been shown that there is a functional asymmetry in the piriform cortex, with the left piriform cortex more involved in the use of the olfactory navigational map than the right piriform cortex. To investigate further the lateralization of the olfactory system in relation to navigational processes in carrier pigeons, we compared their homing performance after either their left or the right nostril was plugged. Contrary to our expectations, we observed an impairment in the initial orientation of the pigeons with their right nostril plugged. However, both groups released with one nostril plugged tended to be poorer than control pigeons in their homing performance. The observed asymmetry in favour of the right nostril might be due to projections from the olfactory bulbs to the contralateral globus pallidum, a structure involved in motor responses.     

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.     

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.     

Homing behavior of pigeons after telencephalic ablations

In a first experiment, dorsomedial forebrain ablated birds showed similar homeward orientation when compared to untreated controls independent of whether the birds were released from a previous training site or a site they had never been before. However, although all control birds returned to the home loft, only 2 of 28 birds with lesions homed successfully. In a subsequent experiment, both sham operated control birds and birds with lesions of the visual Wulst homed successfully when released only 800 m from and in full view of their respective home lofts. Pigeons with dorsomedial forebrain lesions, however, failed to return to their respective home lofts. The results show that the avian dorsomedial forebrain plays a critical role in that step of the homing process by which a pigeon returns to its home loft once in its vicinity, and that the failure to reassociate with the home loft is a likely result of deficient recognition of the home loft and/or its surrounding area. In an additional experiment, pigeons with Wulst lesions were shown to orient as controls and to successfully return to the home loft when released from two distant sites. This experiment demonstrated that the avian Wulst plays no necessary role in the homing behavior of pigeons.     

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.     

The nature of unilateral neglect in the olfactory sensory system

This study investigated two major theories of unilateral neglect utilizing the ipsilaterally innervated olfactory sense. The sensory theory states that unilateral neglect is due to a diminished or attenuated sensory input. The representational theory states that unilateral neglect is due to a disordered internal representation, which is not dependent on sensory input. Results of the study revealed that right hemisphere lesion patients with left unilateral neglect failed to respond to their left contralateral nostril on olfactory double simultaneous stimulation, consistent with the representational theory because the left nostril has no direct sensory input to the right hemisphere.     

Chemosensory Event-Related Potentials in Patients with Temporal Lobe Epilepsy

Summary: We investigated chemosensory functions in patients with temporal lobe epilepsy (TLE) to discover whether olfactory and trigeminal stimuli applied either ipsilaterally or contralaterally to the epileptic focus are processed differently. Twenty-two patients were investigated, 12 of whom had epilepsy with a focus located in left temporal lobe (LTL). The remaining 10 patients had a right temporal lobe (RTL) focus. Input from the trigeminal system was examined by use of CO₂; input from the olfactory system was evaluated with vanillin and hydrogen sulfide as stimuli. Chemosensory function was assessed by evaluation of chemosensory event-related potentials (CSERP) and the patients' verbal reports in an odor identification test. In both groups of patients, prolonged CSERP latencies were noted after stimulation of the left nostril with CO₂ as compared with stimulation of the right nostril. In contrast, a different pattern emerged for olfactory stimuli. After right-sided olfactory stimulation, latencies were prolonged in patients with right-sided epileptical foci. Similarly, when the left nostril was stimulated in patients with a left-sided focus, CSERP latencies were prolonged. Thus, neocortical processing of olfactory, but not trigeminally mediated information evidently is affected by functional lesions of the temporal lobe. After olfactory stimulation in patients with a right-sided focus, the distribution of amplitudes was different from normal. Moreover, analyses showed nonoverlapping 95% confidence intervals (CI) for latency N1 when vanillin was applied to the right nostril. These results indicate that RTL may play a different role in processing of olfactory information as compared with LTL.     

Navigational experience affects hippocampus size in homing pigeons

Homing (racing) pigeons (Columba livia f.d.) are well-known for their homing abilities, which are thought to be based on a genetic predisposition, multimodal learning and spatial cognition. On average, the hippocampus, a forebrain structure that processes spatial information, is larger in homing pigeons compared to other non-homing pigeon breeds or their wild ancestor, the rock dove. Here we show that this characteristic hippocampus volume is dependent on flying and navigational experience. Twenty homing pigeons originating from the same breeding stock were raised in the same loft under identical constraints. After fledging, 10 of them were allowed to fly around the loft, gain navigational experience and participate successfully in races. The other 10 stayed permanently in the loft and thus did not share the navigational skill experienced by the first group. After reaching sexual maturity, individuals of both groups were sacrificed and morphometric analyses were carried out to measure the volumes of total brain, telencephalon, hippocampus and 12 other brain structures. Individuals with experience in flying and navigation had an 11.2% larger hippocampus relative to the telencephalon compared to non-experienced individuals (p = 0.028). This effect is not seen in any of the other measured brain subdivisions. Given that plasticity in hippocampal volume has a genetic component, our results confirm that there is also an experience component, and that has certain implications for navigational ability. Evidently, experience is a precondition to full hippocampal development.     

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.     

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.     

Dorsomedial forebrain ablations and home loft association behavior in homing pigeons

In a series of experiments which involved only short distance experimental releases (800 m or less and within view of the home loft), it was demonstrated that dorsomedial forebrain ablated pigeons generally failed to reassociate with their home loft if the postablation experimental release took place soon postablation or if during the time between ablation and experimental release they were kept away from their home loft. In contrast, if dorsomedial forebrain ablated pigeons were allowed to recover at their home loft prior to experimental release, they succeeded in associating with their home loft in a manner similar to controls. However, only postablation exposure to a pigeon's own loft was sufficient to permit continued home loft association. Pigeons from one loft failed to associate with a foreign postablation recovery loft when released within sight of it. The results show that dorsomedial forebrain ablations result in pigeons which no longer succeed in associating with their home loft; recovery from failed home loft association behavior is possible with postablation exposure to the home loft, and a pigeon's previous association with a loft was a precondition if postablation association was to be affected. The results suggest that dorsomedial forebrain ablated pigeons retain something like a 'home loft trace' which they can use to mediate retrieval and reformation of the recognition properties needed for proper home loft association.     

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.     

Unilateral displacement in the olfactory sense: a manifestation of the unilateral neglect syndrome

Unilateral neglect is a syndrome primarily occurring with right hemisphere--particularly right parietal lobe--brain damage and involving the failure to respond to stimuli presented to the left side of the body and space. Unilateral displacement (a less severe manifestation of the neglect syndrome) involves the accurate identification of a stimulus, but the displacement or mislocalization of that stimulus to the opposite side of the body and space. This study investigated two major theories of unilateral neglect utilizing the primarily ipsilaterally innervated olfactory sense. The sensory theory states that unilateral neglect is due to a diminished sensory input, whereas the representational theory states that it is due to a disordered internal representation which is not dependent on sensory input. Results revealed that right hemisphere lesion patients with left unilateral neglect exhibited a significantly greater number of displacements in their left nostril on olfactory double simultaneous stimulation, consistent with the representational theory.     

Role of sensory activity on chemospecific populations of interneurons in the adult olfactory bulb

The olfactory bulb (OB) retains a remarkable capacity to renew its interneuronal populations throughout the lifespan of animals. Neuronal precursors giving rise to the bulbar interneurons are generated in the subventricular zone and have to migrate long distances before reaching the OB. In the adult OB these neuronal precursors differentiate into distinct neuronal types, including GABAergic cells located in the granule cell layer and a diverse set of neurons in the glomerular layer comprising GABAergic and dopaminergic interneurons, as well as other neuronal subtypes expressing calretinin and calbindin. While the role of sensory activity in the integration and/or survival of newly generated cells in the olfactory system is well established, very little is known about how odorant‐induced activity affects fate specification of newborn cells as well as survival and fate maintenance of preexisting neuronal populations generated in adulthood. The present study demonstrates that sensory deprivation diminishes not only the number of newborn cells in the OB, but also reduces the density of granule and periglomerular cells generated before nostril occlusion. It also shows that sensory activity has an important influence on the development and expression of dopaminergic, but not GABAergic, calretinin or calbindin phenotypes. Our data reveal that odorant‐induced activity is important for the survival of both newborn and preexisting OB interneurons generated at adulthood and suggests that these chemospecific populations are differentially affected by sensory deprivation. J. Comp. Neurol. 518:1847–1861, 2010. © 2009 Wiley‐Liss, Inc.     

Investigation of unirhinal olfactory identification in antipsychotic-free patients experiencing a first-episode schizophrenia

Although olfactory deficits have been reported in patients with schizophrenia, few studies have examined whether these deficits are lateralized or investigated their possible clinical correlates. In this study, we administered the University of Pennsylvania Smell Identification Test (UPSIT) unirhinally (one nostril at a time) to 15 patients experiencing a first-episode of schizophrenia and 17 healthy comparison subjects. Clinical and olfactory assessments were conducted on the same day in patients while they were antipsychotic drug-free. Patients performed more poorly compared to healthy volunteers in their ability to identify odors across both nostrils, but there were no group differences in right and left nostril impairment. Among patients, greater deficits in grooming and hygiene correlated significantly and more strongly with poorer ability in identifying odors presented to the left compared to the right nostril. Our findings suggest that deficits in grooming and hygiene, including poor body odor, observed in patients experiencing a first-episode of schizophrenia are associated with an impairment in left nostril, and possibly left hemisphere, olfactory processing.     

Changes in olfactory bulb volume following lateralized olfactory training

Repeated exposure to odors modifies olfactory function. Consequently, “olfactory training” plays a significant role in hyposmia treatment. In addition, numerous studies show that the olfactory bulb (OB) volume changes in disorders associated with olfactory dysfunction. Aim of this study was to investigate whether and how olfactory bulb volume changes in relation to lateralized olfactory training in healthy people. Over a period of 4 months, 97 healthy participants (63 females and 34 males, mean age: 23.74 ± 4.16 years, age range: 19–43 years) performed olfactory training by exposing the same nostril twice a day to 4 odors (lemon, rose, eucalyptus and cloves) while closing the other nostril. Before and after olfactory training, magnetic resonance imaging (MRI) scans were performed to measure OB volume. Furthermore, participants underwent lateralized odor threshold and odor identification testing using the “Sniffin‘ Sticks” test battery.OB volume increased significantly after olfactory training (11.3 % and 13.1 % respectively) for both trained and untrained nostril. No significant effects of sex, duration and frequency of training or age of the subjects were seen. Interestingly, PEA odor thresholds worsened after training, while olfactory identification remained unchanged.These data show for the first time in humans that olfactory training may involve top-down process, which ultimately lead to a bilateral increase in olfactory bulb volume.     

Efferent and afferent connections of the olfactory bulb and prepiriform cortex in the pigeon (Columba livia)

Although olfaction in birds is known to be involved in a variety of behaviors, there is comparatively little detailed information on the olfactory brain. In the pigeon brain, the olfactory bulb (OB) is known to project to the prepiriform cortex (CPP), piriform cortex (CPi), and dorsolateral corticoid area (CDL), which together are called the olfactory pallium, but centrifugal pathways to the OB have not been fully explored. Fiber connections of CPi and CDL have been reported, but those of other olfactory pallial nuclei remain unknown. The present study examines the fiber connections of OB and CPP in pigeons to provide a more detailed picture of their connections using tract‐tracing methods. When anterograde and retrograde tracers were injected in OB, projections to a more extensive olfactory pallium were revealed, including the anterior olfactory nucleus, CPP, densocellular part of the hyperpallium, tenia tecta, hippocampal continuation, CPi, and CDL. OB projected commissural fibers to the contralateral OB but did not receive afferents from the contralateral olfactory pallium. When tracers were injected in CPP, reciprocal ipsilateral connections with OB and nuclei of the olfactory pallium were observed, and CPP projected to the caudolateral nidopallium and the limbic system, including the hippocampal formation, septum, lateral hypothalamic nucleus, and lateral mammillary nucleus. These results show that the connections of OB have a wider distribution throughout the olfactory pallium than previously thought and that CPP provides a centrifugal projection to the OB and acts as a relay station to the limbic system. J. Comp. Neurol. 522:1728–1752, 2014. © 2013 Wiley Periodicals, Inc.     

The effects of lesions to the caudolateral neostriatum on sun compass based spatial learning in homing pigeons

To better define the role of the avian caudolateral neostriatum (NCL) in spatial behavior, we used homing pigeons to explore the effects of NCL lesions on a sun compass based spatial learning task. Although NCL lesioned birds learned the task, they required more sessions to reach criterion than controls. NCL lesioned pigeons were also able to acquire a color discrimination task that was procedurally similar to the sun compass spatial learning task, but they made more errors than controls. Both the deficits observed in sun compass based spatial learning and color discrimination were correlated with the volume of lesion damage to dorsal rather than ventral portions of NCL. Overall, these findings suggest that the role of NCL in homing pigeon navigation from distant unfamiliar locations is not related to a bird's ability to learn stimulus-direction associations using a sun compass. However NCL does appear involved in a pigeon's ability to perform at least some behaviors common to both the color discrimination and the sun compass based spatial learning tasks.     

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

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