Compartmentation of the cerebellar cortex of hummingbirds (Aves: Trochilidae) revealed by the expression of zebrin II and phospholipase C beta 4.

The parasagittal organization of the mammalian cerebellar cortex into zones has been well characterized by immunohistochemical, hodological and physiological studies in recent years. The pattern of these parasagittal bands across the cerebellum is highly conserved across mammals, but whether a similar conservation of immunohistochemically defined parasagittal bands occurs within birds has remained uncertain. Here, we examine the compartmentation of the cerebellar cortex of a group of birds with unique cerebellar morphology-hummingbirds (Trochilidae). Immunohistochemical techniques were used to characterize the expression of zebrin II (aldolase C) and phospholipase C beta 4 (PLC beta 4) in the cerebellar cortex of two hummingbird species. A series of zebrin II immunopositive/immunonegative parasagittal stripes was apparent across most folia representing three major transverse zones: an anterior zone with a central stripe flanked by three lateral stripes on either side; a central zone of high/low immunopositive stripes; and a posterior zone with a central stripe flanked by four to six lateral stripes on either side. In addition, both folia I and X were uniformly immunopositive. The pattern of PLC beta 4 immunoreactivity was largely complementary-PLC beta 4 positive stripes were zebrin II negative and vice versa. The similarity of zebrin II expression between the hummingbirds and the pigeon indicates that the neurochemical compartmentation of the cerebellar cortex in birds is highly conserved, but species differences in the number and width of stripes do occur.

Expression of calcium-binding proteins in pathways from the nucleus of the basal optic root to the cerebellum in pigeons.

Calcium-binding protein expression has proven useful in delineating neural pathways. For example, in birds, calbindin is strongly expressed in the tectofugal pathway, whereas parvalbumin (PV) is strongly expressed in the thalamofugal pathway. Whether neurons within other visual regions also differentially express calcium-binding proteins, however, has not been extensively studied. The nucleus of the basal optic root (nBOR) is a retinal-recipient nucleus that is critical for the generation of the optokinetic response. The nBOR projects to the cerebellum both directly and indirectly via the inferior olive (IO). The cerebellar and IO projections originate from different neurons within the nBOR, but whether they can also be differentiated based on calcium-binding protein expression is unknown. In this study, we combined retrograde neuronal tracing from the cerebellum and IO with fluorescent immunohistochemistry for PV and calretinin (CR) in the nBOR of pigeons. We found that about half (52.3%) of the cerebellar-projecting neurons were CR+ve, and about one-third (33.6%) were PV+ve. Most (90%) of these PV+ve cells were also labeled for CR. In contrast, very few of the IO-projecting neurons expressed CR or PV (

Neural specialization for hovering in hummingbirds: hypertrophy of the pretectal nucleus Lentiformis mesencephali.

Hummingbirds possess an array of morphological and physiological specializations that allow them hover such that they maintain a stable position in space for extended periods. Among birds, this sustained hovering is unique to hummingbirds, but possible neural specializations underlying this behavior have not been investigated. The optokinetic response (OKR) is one of several behaviors that facilitates stabilization. In birds, the OKR is generated by the nucleus of the basal optic root (nBOR) and pretectal nucleus lentiformis mesencephali (LM). Because stabilization during hovering is dependent on the OKR, we predicted that nBOR and LM would be significantly enlarged in hummingbirds. We examined the relative size of nBOR, LM, and other visual nuclei of 37 species of birds from 13 orders, including nine hummingbird species. Also included were three species that hover for short periods of time (transient hoverers; a kingfisher, a kestrel, and a nectarivorous songbird). Our results demonstrate that, relative to brain volume, LM is significantly hypertrophied in hummingbirds compared with other birds. In the transient hoverers, there is a moderate enlargement of the LM, but not to the extent found in the hummingbirds. The same degree of hypertrophy is not, however, present in nBOR or the other visual nuclei measured: nucleus geniculatus lateralis, pars ventralis, and optic tectum. This selective hypertrophy of LM and not other visual nuclei suggests that the direction-selective optokinetic neurons in LM are critical for sustained hovering flight because of their prominent role in the OKR and gaze stabilization.

Purkinje cell compartmentation as revealed by zebrin II expression in the cerebellar cortex of pigeons (Columba livia).

Purkinje cells in the cerebellum express the antigen zebrin II (aldolase C) in many vertebrates. In mammals, zebrin is expressed in a parasagittal fashion, with alternating immunopositive and immunonegative stripes. Whether a similar pattern is expressed in birds is unknown. Here we present the first investigation into zebrin II expression in a bird: the adult pigeon (Columba livia). Western blotting of pigeon cerebellar homogenates reveals a single polypeptide with an apparent molecular weight of 36 kDa that is indistinguishable from zebrin II in the mouse. Zebrin II expression in the pigeon cerebellum is prominent in Purkinje cells, including their dendrites, somata, axons, and axon terminals. Parasagittal stripes were apparent with bands of Purkinje cells that strongly expressed zebrin II (+ve) alternating with bands that expressed zebrin II weakly or not at all (-ve). The stripes were most prominent in folium IXcd, where there were seven +ve/-ve stripes, bilaterally. In folia VI-IXab, several thin stripes were observed spanning the mediolateral extent of the folia, including three pairs of +ve/-ve stripes that extended across the lateral surface of the cerebellum. In folium VI the zebrin II expression in Purkinje cells was stronger overall, resulting in less apparent stripes. In folia II-V, four distinct +ve/-ve stripes were apparent. Finally, in folia I (lingula) and X (nodulus) all Purkinje cells strongly expressed zebrin II. These data are compared with studies of zebrin II expression in other species, as well as physiological and neuroanatomical studies that address the parasagittal organization of the pigeon cerebellum.

Comparative morphology of the avian cerebellum: II. Size of folia.

Despite the highly conserved circuitry of the cerebellum, its overall shape varies significantly among and within vertebrate classes. In birds, one of the most prominent differences among orders is the relative size of the cerebellar folia. The enlargement/reduction of individual folia is thought to relate to specific behavioral differences among taxa, but this has not been adequately tested. Here, we survey variation in cerebellar folia size among 96 species of birds and test for phylogenetic effects and correlations with behavior using a combination of conventional and phylogeny-based statistics. Overall, we found that phylogenetic history accounts for a significant amount of variation in the relative size of individual folia. Order membership, in particular, accounted for more than half of the interspecific variation in folia size. There are also complex relationships among folia such that the expansion of one folium is often accompanied by a reduction in other folia. With respect to behavioral correlates: (1) we did not find any significant correlations between folia size and reliance on trigeminal input; (2) there was some evidence supporting a correlation between strong hindlimbs and an expansion of the anterior lobe; and (3) there were significant reductions in folia I-III and expansions in folia VI and VII in species classified as strong fliers. This expansion likely reflects increased visual processing requirements in species with rapid and/or agile flight. It therefore appears that folium size is a product of both phylogenetic history and behavior in birds.

Two optic flow pathways from the pretectal nucleus lentiformis mesencephali to the cerebellum in pigeons (Columba livia).

Neurons in the pretectal nucleus lentiformis mesencephali (LM) are involved in the analysis of optic flow. LM provides mossy fiber inputs to folia VI-VIII of the posterior cerebellum and IXcd of the vestibulocerebellum. Previous research has shown that the vestibulocerebellum is involved in visual-vestibular integration supporting gaze stabilization. The function of folia VI-VIII in pigeons is not well understood; however, these folia receive input from a tectopontine system, which is likely involved with analyzing local motion as opposed to optic flow. We sought to determine whether the mossy fiber input from LM to IXcd differs from that to VI-VIII. Fluorescent retrograde tracers were injected into these folia, and the pattern of labeling in LM was observed. Large multipolar neurons were labeled throughout the rostrocaudal extent of LM. There was a clear mediolateral difference: 74.3% of LM neurons projecting to IXcd were located in the lateral subnucleus of LM (LMl), whereas 73.8% of LM neurons projecting to VI-VIII were found in medial LM (LMm). This suggests that the subnuclei of LM have differing roles. In particular, the LMl-IXcd pathway is involved in generating the optokinetic response. We suggest that the pathway from LMm to VI-VIII is integrating optic flow and local motion to support various oculomotor and visuomotor behaviors, including obstacle avoidance during locomotion.

Projections of the nucleus lentiformis mesencephali in pigeons (Columba livia): a comparison of the morphology and distribution of neurons with different efferent projections.

The avian nucleus lentiformis mesencephali (LM) is a visual structure involved in the optokinetic response. The LM consists of several morphologically distinct cell types. In the present study we sought to determine if different cell types had differential projections. Using retrograde tracers, we examined the morphology and distribution of LM neurons projecting to the vestibulocerebellum (VbC), inferior olive (IO), dorsal thalamus, nucleus of the basal optic root (nBOR), and midline mesencephalon. From injections into the latter two structures, small LM cells were labeled. More were localized to the lateral LM as opposed to medial LM. From injections into the dorsal thalamus, small neurons were found throughout LM. From injections into the VbC, large multipolar cells were found throughout LM. From injections into IO, a strip of medium-sized fusiform neurons along the border of the medial and lateral subnuclei was labeled. To investigate if neurons project to multiple targets we used fluorescent retrograde tracers. After injections into IO and VbC, double-labeled neurons were not observed in LM. Likewise, after injections into nBOR and IO, double-labeled neurons were not observed. Finally, we processed sections through LM for glutamic acid decarboxylase (GAD). Small neurons, mostly in the lateral LM, were labeled, suggesting that projections from LM to nBOR and midline mesencephalon are GABAergic. We conclude that two efferents of LM, VbC and IO, receive input from morphologically distinct neurons: large multipolar and medium-sized fusiform neurons, respectively. The dorsal thalamus, nBOR, and midline mesencephalon receive input from small neurons, some of which are likely GABAergic.

Echolocation, vocal learning, auditory localization and the relative size of the avian auditory midbrain nucleus (MLd).

The avian nucleus mesencephalicus lateralis, pars dorsalis (MLd) is an auditory midbrain nucleus that plays a significant role in a variety of acoustically mediated behaviours. We tested whether MLd is hypertrophied in species with auditory specializations: owls, the vocal learners and echolocaters. Using both conventional and phylogenetically corrected statistics, we find that the echolocating species have a marginally enlarged MLd, but it does not differ significantly from auditory generalists, such as pigeons, raptors and chickens. Similarly, all of the vocal learners tend to have relatively small MLds. Finally, MLd is significantly larger in owls compared to all other birds regardless of how the size of MLd is scaled. This enlargement is far more marked in asymmetrically eared owls than symmetrically eared owls. Variation in MLd size therefore appears to be correlated with some auditory specializations, but not others. Whether an auditory specialist possesses a hypertrophied MLd appears to be depend upon their hearing range and sensitivity as well as the ability to resolve small azimuthal and elevational angles when determining the location of a sound. As a result, the only group to possess a significantly large MLd consistently across our analyses is the owls. Unlike other birds surveyed, owls have a battery of peripheral and other central auditory system specializations that correlate well with their hearing abilities. The lack of differences among the generalists, vocal learners and echolocaters therefore reflects an overall similarity in hearing abilities, despite the specific life history requirements of each specialization and species. This correlation between the size of a neural structure and the sensitivity of a perceptual domain parallels a similar pattern in mammals.

The effects of environmental exposure to DDT on the brain of a songbird: changes in structures associated with mating and song.

Dichlorodiphenyltrichloroethane (DDT) is a persistent organochlorine compound found worldwide that causes significant anatomical, physiological and behavioural abnormalities in humans and wildlife. However, little is known about whether environmental exposure to DDT affects the brain. Here, we show that environmental exposure to DDT alters the brains of American Robins (Turdus migratorius) in several ways. Increasing levels of DDT resulted in: (i) smaller brain and relative forebrain volumes; (ii) a reduction in the size of two song nuclei, nucleus robustus arcopallialis (RA) and HVC; and (iii) a drastic reduction in neuronal size and overall volume of nucleus intercollicularis (ICo), a structure that is critical for normal sexual behaviour. These changes likely result from stress, direct neurotoxicity and androgen receptor antagonism by the primary metabolite of DDT, p,p'-DDE and this is corroborated by analyses of brain region volumes and p,p'-DDE levels. Our results therefore demonstrate that environmental exposure to DDT is correlated with significant changes in the brain and specifically those structures related to mating and song. Given the magnitude of these changes in the brain and the fact that environmental DDT exposure was restricted to early development, we conclude that both humans and wildlife that live in DDT contaminated environments may be at risk of neurological damage.

A dissociation of motion and spatial-pattern vision in the avian telencephalon: implications for the evolution of "visual streams".

The ectostriatum is a large visual structure in the avian telencephalon. Part of the tectofugal pathway, the ectostriatum receives a large ascending thalamic input from the nucleus rotundus, the homolog of the mammalian pulvinar complex. We investigated the effects of bilateral lesions of the ectostriatum in pigeons on visual motion and spatial-pattern perception tasks. To test motion perception, we measured performance on a task requiring detection of coherently moving random dots embedded in dynamic noise. To test spatial-pattern perception, we measured performance on the detection of a square wave grating embedded in static noise. A double dissociation was revealed. Pigeons with lesions to the caudal ectostriatum showed a performance deficit on the motion task but not the grating task. In contrast, pigeons with lesions to the rostral ectostriatum showed a performance deficit on the grating task but not the motion task. Thus, in the avian telencephalon, there is a separation of visual motion and spatial-pattern perception as there is in the mammalian telencephalon. However, this separation of function is in the targets of the tectofugal pathway in pigeons rather than in the thalamofugal pathway as described in mammals. The implications of these findings with respect to the evolution of the visual system are discussed. Specifically, we suggest that the principle of parallel visual streams originated in the tectofugal pathway rather than the thalamofugal pathway.

Inferior olivary neurons innervate multiple zones of the flocculus in pigeons (Columba livia).

Complex spike activity of floccular Purkinje cells responds to patterns of rotational optic flow about the vertical axis (rVA neurons) or a horizontal axis 45 degrees to the midline (rH45 neurons). The pigeon flocculus is organized into four parasagittal zones: two rVA zones (zones 0 and 2) interdigitated with two rH45 zones (zones 1 and 3). Climbing fiber input to the rVA and rH45 zones arises in the caudal and rostral regions of the medial column of the inferior olive (mcIO), respectively. To determine whether the two rVA zones and the two rH45 zones receive input from different areas of the caudal and rostral mcIO and whether individual neurons project to both zones of the same rotational preference, different colors of fluorescent retrograde tracer were injected into the two rVA or two rH45 zones. For the rVA injections, retrogradely labeled cells from the two zones were intermingled in the caudal mcIO, but the distribution of cells labeled from zone 0 was slightly caudal to that from zone 2. On average, 18% of neurons were double labeled. For the rH45 injections, cells retrogradely labeled from the two zones were intermingled in the rostral mcIO, but the distribution of cells labeled from zone 1 was slightly rostral to that from zone 3. On average, 22% of neurons were double labeled. In sum, each of the two rVA zones and the two rH45 zones receives input from slightly different regions of the mcIO, and about 20% of the neurons project to both zones.

Zonal organization of the vestibulocerebellum in pigeons (Columba livia): I. Climbing fiber input to the flocculus.

Previous studies in pigeons have shown that the neurons in the medial column of the inferior olive respond best to patterns of optic flow resulting from self-rotation. With respect to the axis of rotation, there are two functional groups: rVA neurons prefer rotation about the vertical axis, whereas rH45 neurons respond best to rotation about an horizontal axis oriented at 45 degrees ipsilateral azimuth. The rVA and rH45 neurons are located in the caudal and rostral margins of the medial column, respectively. These olivary neurons project as climbing fibers to the contralateral flocculus. In this study, injections of anterograde tracers into the medial column were used to investigate the zonal organization of the climbing fiber input to the flocculus of pigeons. Iontophoretic injections of either cholera toxin subunit-B or biotinylated dextrin amine were made into the medial column of the inferior olive at locations responsive to rVA or rH45 rotational optic flow. Anterogradely labeled climbing fibers in the flocculus showed a clear zonal organization. There were four parasagittal bands spanning both folia IXcd and X consisting of two rVA zones interdigitated with two rH45 zones. These findings are compared with the zonal organization of the flocculus in mammalian species.

Zonal organization of the vestibulocerebellum in pigeons (Columba livia): III. Projections of the translation zones of the ventral uvula and nodulus.

Previous electrophysiological studies in pigeons have shown that the complex spike activity of Purkinje cells in the medial vestibulocerebellum (nodulus and ventral uvula) is modulated by patterns of optic flow that result from self-translation along a particular axis in three-dimensional space. There are four response types based on the axis of preferred translational optic flow. By using a three axis system, where +X, +Y, and +Z represent rightward, upward, and forward self-motion, respectively, the four cell types are t(+Y), t(-Y), t(-X-Z), and t(-X+Z), with the assumption of recording from the left side of the head. These response types are organized into parasagittal zones. In this study, we injected the anterograde tracer biotinylated dextran amine into physiologically identified zones. The t(-X-Z) zone projected dorsally within the vestibulocerebellar process (pcv) on the border with the medial cerebellar nucleus (CbM), and labeling was found in the CbM itself. The t(-X+Z) zone also projected to the pcv and CbM, but to areas ventral to the projection sites of the t(-X-Z) zone. The t(-Y) zone also projected to the pcv, but more ventrally on the border with the superior vestibular nucleus (VeS). Some labeling was also found in the dorsal VeS and the dorsolateral margin of the caudal descending vestibular nucleus, and a small amount of labeling was found laterally in the caudal margin of the medial vestibular nucleus. The data set was insufficient to draw conclusions about the projection of the t(+Y) zone. These results are contrasted with the projections of the flocculus, compared with the primary vestibular projection, and implications for collimotor function are discussed.

Zonal organization of the vestibulocerebellum in pigeons (Columba livia): II. Projections of the rotation zones of the flocculus.

Previous neurophysiologic research in birds and mammals has shown that there are two types of Purkinje cells in the flocculus. The first type shows maximal modulation in response to rotational optokinetic stimulation about the vertical axis (rVA neurons). The second type shows maximal modulation in response to rotational optokinetic stimulation about a horizontal axis oriented 45 degrees to contralateral azimuth (rH45c neurons). In pigeons, the rVA and rH45c are organized into four alternating parasagittal zones. In this study we investigated the projections of Purkinje cells in the rVA and rH45c zones by using the anterograde tracers biotinylated dextran amine and cholera toxin subunit B. After iontophoretic injections of tracers into the rH45c zones, heavy anterograde labeling was found in the infracerebellar nucleus and the medial margin of the superior vestibular nucleus. Some labeling was also consistently observed in the lateral cerebellar nucleus and the dorsolateral vestibular nucleus. After injections into the rVA zones, heavy anterograde labeling was found in the medial and descending vestibular nuclei, the nucleus prepositus hypoglossi, and the central region of the superior vestibular nucleus. Less labeling was seen in the tangential nucleus, the dorsolateral vestibular nucleus, and the lateral vestibular nucleus, pars ventralis. These results are compared and contrasted with findings in mammalian species.

The optic tectum of birds: mapping our way to understanding visual processing.

Over the past few decades there has been a massive amount of research on the geniculo-striate visual system in primates. However, studies of the avian visual system have provided a rich source of data contributing to our understanding of visual processing. In this paper we review the connectivity and function of the optic tectum (homolog of the superior colliculus) in birds. We highlight the retinotopic projections that the optic tectum has with the isthmal nuclei, and the functional topographic projections that the optic tectum has with the nucleus rotundus and entopallium (homologs of the pulvinar and extrastriate cortex, respectively) where retinotopy has been sacrificed. This work has been critical in our understanding of basic visual processes including attention, parallel processing, and the binding problem.

Differential projections from the vestibular nuclei to the flocculus and uvula-nodulus in pigeons (Columba livia).

The pigeon vestibulocerebellum is divided into two regions based on the responses of Purkinje cells to optic flow stimuli: the uvula-nodulus responds best to self-translation, and the flocculus responds best to self-rotation. We used retrograde tracing to determine whether the flocculus and uvula-nodulus receive differential mossy fiber input from the vestibular and cerebellar nuclei. From retrograde injections into the both the flocculus and uvula-nodulus, numerous cells were found in the superior vestibular nucleus (VeS), the cerebellovestibular process (pcv), the descending vestibular nucleus (VeD), and the medial vestibular nucleus (VeM). Less labeling was found in the prepositus hypoglossi, the cerebellar nuclei, the dorsolateral vestibular nucleus, and the lateral vestibular nucleus, pars ventralis. In the VeS, the differential input to the flocculus and uvula-nodulus was distinct: cells were localized to the medial and lateral regions, respectively. The same pattern was observed in the VeD, although there was considerable overlap. In the VeM, the majority of cells labeled from the flocculus were in rostral margins on the ipsilateral side, whereas labeling from uvula-nodulus injections was distributed bilaterally throughout the VeM. Finally, from injections in the flocculus but not the uvula-nodulus, moderate labeling was observed in a paramedian area, adjacent to the medial longitudinal fasciculus. In summary, there were clear differences with respect to the projections from the vestibular nuclei to functionally distinct parts of the vestibulocerebellum. Generally speaking, the mossy fibers to the flocculus and uvula-nodulus arise from regions of the vestibular nuclei that receive input from the semicircular canals and otolith organs, respectively.

Relative Wulst volume is correlated with orbit orientation and binocular visual field in birds.

In mammals, species with more frontally oriented orbits have broader binocular visual fields and relatively larger visual regions in the brain. Here, we test whether a similar pattern of correlated evolution is present in birds. Using both conventional statistics and modern comparative methods, we tested whether the relative size of the Wulst and optic tectum (TeO) were significantly correlated with orbit orientation, binocular visual field width and eye size in birds using a large, multi-species data set. In addition, we tested whether relative Wulst and TeO volumes were correlated with axial length of the eye. The relative size of the Wulst was significantly correlated with orbit orientation and the width of the binocular field such that species with more frontal orbits and broader binocular fields have relatively large Wulst volumes. Relative TeO volume, however, was not significant correlated with either variable. In addition, both relative Wulst and TeO volume were weakly correlated with relative axial length of the eye, but these were not corroborated by independent contrasts. Overall, our results indicate that relative Wulst volume reflects orbit orientation and possibly binocular visual field, but not eye size.

Projections of the nucleus of the basal optic root in pigeons (Columba livia): a comparison of the morphology and distribution of neurons with different efferent projections.

The avian nucleus of the basal optic root (nBOR) is a visual structure involved in the optokinetic response. nBOR consists of several morphologically distinct cell types, and in the present study, we sought to determine if these different cell types had differential projections. Using retrograde tracers, we examined the morphology and distribution of nBOR neurons projecting to the vestibulocerebellum (VbC), inferior olive (IO), dorsal thalamus, the pretectal nucleus lentiformis mesencephali (LM), the contralateral nBOR, the oculomotor complex (OMC) and a group of structures along the midline of the mesencephalon. The retrogradely labeled neurons fell into two broad categories: large neurons, most of which were multipolar rather than fusiform and small neurons, which were either fusiform or multipolar. From injections into the IO, LM, contralateral nBOR, and structures along the midline-mesencephalon small nBOR neurons were labeled. Although there were no differences with respect to the size of the labeled neurons from these injections, there were some differences with the respect to the distribution of labeled neurons and the proportion of multipolar vs. fusiform neurons. From injections into the VbC, the large multipolar cells were labeled throughout nBOR. The only other cases in which these large neurons were labeled were contralateral OMC injections. To investigate if single neurons project to multiple targets we used paired injections of red and green fluorescent retrograde tracers into different targets. Double-labeled neurons were never observed indicating that nBOR neurons do not project to multiple targets. We conclude that individual nBOR neurons have unique projections, which may have differential roles in processing optic flow and controlling the optokinetic response.

The evolution of stereopsis and the Wulst in caprimulgiform birds: A comparative analysis.

Owls possess stereopsis (i.e., the ability to perceive depth from retinal disparity cues), but its distribution amongst other birds has remained largely unexplored. Here, we present data on species variation in brain and telencephalon size and features of the Wulst, the neuroanatomical substrate that subserves stereopsis, in a putative sister-group to owls, the order Caprimulgiformes. The caprimulgiforms we examined included nightjars (Caprimulgidae), owlet-nightjars (Aegothelidae), potoos (Nyctibiidae), frogmouths (Podargidae) and the Oilbird (Steatornithidae). The owlet-nightjars and frogmouths shared almost identical relative brain, telencephalic and Wulst volumes as well as overall brain morphology and Wulst morphology with owls. Specifically, the owls, frogmouths and owlet-nightjars possess relatively large brains and telencephalic and Wulst volumes, had a characteristic brain shape and displayed prominent laminae in the Wulst. In contrast, potoos and nightjars both had relatively small brains and telencephala, and Wulst volumes that are typical for similarly sized birds from other orders. The Oilbird had a large brain, telencephalon and Wulst, although these measures were not quite as large as those of the owls. This gradation of owl-like versus nightjar-like brains within caprimulgiforms has significant implications for understanding the evolution of stereopsis and the Wulst both within the order and birds in general.