Tectofugal Visual Pathway Research Articles

Early Development of the Thalamo-Pallial Stage of the Tectofugal Visual Pathway in the Chicken (Gallus gallus).

The tectofugal pathway is a highly conserved visual pathway in all amniotes. In birds and mammals, retinorecipient neurons located in the midbrain roof (optic tectum/superior colliculus) are the source of ascending projections to thalamic relays (nucleus rotundus/caudal pulvinar), which in turn project to specific pallial regions (visual dorsal ventricular ridge [vDVR]/temporal cortex) organized according to a columnar recurrent arrangement of interlaminar circuits. Whether or to which extent these striking hodological correspondences arise from comparable developmental processes is at present an open question, mainly due to the scarcity of data about the ontogeny of the avian tectofugal system. Most of the previous developmental studies of this system in birds have focused on the establishment of the retino-tecto-thalamic connectivity, overlooking the development of the thalamo-pallial-intrapallial circuit. In this work, we studied the latter in chicken embryos by means of immunohistochemical assays and precise ex vivo crystalline injections of biocytin and DiI. We found that the layered organization of the vDVR as well as the system of homotopic reciprocal connections between vDVR layers were present as early as E8. A highly organized thalamo-vDVR projection was also present at this stage. Our immunohistochemical assays suggest that both systems of projections emerge simultaneously even earlier. Combined with previous findings, these results reveal that, in striking contrast with mammals, the peripheral and central stages of the avian tectofugal pathway develop along different timelines, with a tecto-thalamo-intrapallial organization arising before and possibly independently of the retino-isthmo-tectal circuit.

Tangentially migrating cells differentiate into stratum griseum central neurons to form tectofugal visual pathway in the developing chick optic tectum.

The optic tectum is the main visual processor of nonmammalian vertebrates and relays visual information from the eye to the telencephalon via the tectofugal pathway. In the development of the avian optic tectum, while the multipolar neurons are arranged by tangential migration, the behavior of individual cells in tangential migration, neural differentiation, and cell fate remain unclear. Here, we pursued the transition of tangentially migrating cells and their involvement in visual circuit formation during chick development. After tangential movement along the axons, the migrating cells relocated to the upper layers and turned back upon differentiation toward the multipolar neurons. The multipolar neurons are destined to differentiate into the stratum griseum central (SGC) neurons with the large dendritic field, which form the tectorotundal projection. Trans-synaptic virus labeling demonstrated that the tangentially migrating cells eventually participate in the tectofugal visual pathway. These results indicate that tangential migration is a crucial process in the formation of the tectofugal visual pathway during the development of the optic tectum.

Central prolactin receptor distribution and pSTAT5 activation patterns in breeding and non-breeding zebra finches (Taeniopygia guttata)

The hormone prolactin has many diverse functions across taxa such as osmoregulation, metabolism, and reproductive behavior. In ring doves, central prolactin action is important for parental care and feeding behavior. However, there is a considerable lack of information on the distribution of the prolactin receptor (PRLR) in the avian CNS to test the hypothesis that prolactin mediates these and other functions in other birds. In order to advance this research, we collected brains from breeding and non-breeding zebra finches to map the PRLR distribution using immunohistochemistry. We found PRLRs are distributed widely across the brain, both in hypothalamic sites known to regulate parental care and feeding, but also in many non-hypothalamic sites, including the tectofugal visual pathway, song system regions, reward associated areas, and pallium. This raises the possibility that prolactin has other functions throughout the brain that are not necessarily related to feeding or parental care. In addition, we also stained brains for pSTAT5, a transcription factor which is expressed when the PRLR is activated and is used as a marker for PRLR activity. We found several notable differences in pSTAT5 activity due to the breeding state of the animal, in both directions, further supporting the hypothesis that prolactin has many diverse functions in the brain both within and outside times of breeding. Together, this study represents the first essential step to inform the design of causative studies which manipulate PRLR-expressing cells to test their role in a wide variety of behaviors and other physiological functions.

Searching for Face-Category Representation in the Avian Visual Forebrain.

Visual information is processed hierarchically along a ventral (‘what’) pathway that terminates with categorical representation of biologically relevant visual percepts (such as faces) in the mammalian extrastriate visual cortex. How birds solve face and object representation without a neocortex is a long-standing problem in evolutionary neuroscience, though multiple lines of evidence suggest that these abilities arise from circuitry fundamentally similar to the extrastriate visual cortex. The aim of the present experiment was to determine whether birds also exhibit a categorical representation of the avian face-region in four visual forebrain structures of the tectofugal visual pathway: entopallium (ENTO), mesopallium ventrolaterale (MVL), nidopallium frontolaterale (NFL), and area temporo-parieto-occipitalis (TPO). We performed electrophysiological recordings from the right and left hemispheres of 13 pigeons while they performed a Go/No-Go task that required them to discriminate between two sets of stimuli that included images of pigeon faces. No neurons fired selectively to only faces in either ENTO, NFL, MVL, or TPO. Birds’ predisposition to attend to the local-features of stimuli may influence the perception of faces as a global combination of features, and explain our observed absence of face-selective neurons. The implementation of naturalistic viewing paradigms in conjunction with electrophysiological and fMRI techniques has the potential to promote and uncover the global processing of visual objects to determine whether birds exhibit category-selective patches in the tectofugal visual forebrain.

The nucleus pretectalis principalis: A pretectal structure hidden in the mammalian thalamus.

A defining feature of the amniote tecto-fugal visual pathway is a massive bilateral projection to the thalamus originating from a distinct neuronal population, tectal ganglion cells (TGCs), of the optic tectum/superior colliculus (TeO/SC). In sauropsids, the thalamic target of the tecto-fugal pathway is the nucleus rotundus thalami (Rt). TGCs axons collateralize en route to Rt to target the nucleus pretectalis principalis (PT), which in turn gives rise to bilateral projection to the TeO. In rodents, the thalamic target of these TGCs afferents is the caudal division of the pulvinar complex (PulC). No pretectal structures in receipt of TGC collaterals have been described in this group. However, Baldwin et al. (Journal of Comparative Neurology, 2011;519(6):1071-1094) reported in the squirrel a feedback projection from the PulC to the SC. Pulvino-tectal (Pul-T) cells lie at the caudal pole of the PulC, intermingled with the axonal terminals of TGCs. Here, by performing a combination of neuronal tracing, immunohistochemistry, immunofluorescence, and in situ hybridization, we characterized the pattern of projections, neurochemical profile, and genoarchitecture of Pul-T cells in the diurnal Chilean rodent Octodon degus. We found that Pul-T neurons exhibit pretectal, but not thalamic, genoarchitectonical markers, as well as hodological and neurochemical properties that match specifically those of the avian nucleus PT. Thus, we propose that Pul-T cells constitute a pretectal cell population hidden within the dorsal thalamus of mammals. Our results solve the oddity entailed by the apparent existence of a noncanonic descending sensory thalamic projection and further stress the conservative character of the tectofugal pathway.

How do migrating birds find their way?

Bird is one of the most abundant and widespread groups in the world. With many specialized structures, such as plumage, air sacs, and hollow bones, most bird species have got flight ability to adapt various niches. Therefore, bird can migrate between wintering and breeding ground, which is usually a long distance, and it’s called migration. Bird navigation is important in migration and is a complex process, which attracts many scientists to dig in how bird finds its way. Since 1873, Charles Darwin has ever mentioned that bird might take the method of dead reckoning on a long-distance migration like human, but at that time no one made further progress. Until 1950s, Kramer firstly found that Common Starling ( Sturnus vulgaris ) can respond to solar azimuth via mirror test. From then on, many experiments revealed that at least four navigation mechanisms are used in bird migration via more than nine external factors. They are: (i) celestial navigation, celestial clues (e.g. solar azimuth, star position, and polarized light) are used during migration period. (ii) Olfactory navigation, odor distributing in the air forms odorous gradient map or mosaic map which can be detected, or can activate directly certain mechanism to navigate. (iii) Auditory navigation, infrasound (0.05 Hz) produced by mountains and rivers generate sonic gradient map. And (iv) magnetic navigation, geomagnetic field can be detected via magnetic materials or chemical magnetoreception to find correct directions. Although many scientists approve that magnetic navigation may be the main mechanism to orientate and navigate, bird has never taken just one mechanism to migrate. Indeed, many species also use the other three mechanisms to calibrate direction, for example, Savannah Sparrow ( Passerculus sandwichensis ) can use polarized light to calibrate the magnetic compass at both sunrise and sunset. Different external clues correspond to different sense organs, so various brain areas should deal with information from different navigation mechanisms. The hippocampus participates in spatial perception and manages anything about celestial navigation via the tectofugal visual pathway and the thalamofugal visual pathway. The piriform cortex (CPi) is the main area to receive stimulation from olfactory bulb and determines how to migrate after receiving olfactory clues. Nervous systems of magnetic navigation include two parts which are trigeminus system and Cluster N. Despite the controversy whether there are some magnetic materials on bird, many experimental evidences have proved that magnetic materials detecting geomagnetic field involve to Trigeminus system. Cluster N, however, is an active area when bird migrates at night and it has an important role in transferring information from chemical magnetoreception to the hippocampus. As illustrated above, navigation mechanisms can get full information from many clues, and then, different brain areas trade off those and co-operate each other to make an elaborate map. Bird navigation involves the receptors to environment and the response of nervous system, so many issues are still maintained. The exact mechanism will be revealed with the new techniques and model animal applied.

Calcium-binding proteins and cytochrome oxidase activity in the turtle optic tectum with special reference to the tectofugal visual pathway

Using immunohistochemistry and a tracer technique we investigated the distribution in the optic tectum of turtles (Emys orbicularis and Testudo horsfieldi) of the calcium-binding proteins (CaBPr) parvalbumin (PV), calbindin (CB) and calretinin (CR) before and after labeling of the nucleus rotundus (Rot) with horseradish peroxidase. The optic tectum activity of the cytochrome oxidase (CO) was studied in parallel. In the principal link of the tectofugal visual pathway (central gray layer, SGC) in both chelonian species, the sparse PV-ir as well as CB- and CR-ir neurons were found significantly varying both in number and the intensity of immunoreactivity of their bodies and dendrites. In contrast, the superficial (SGFS) and deeper periventricular (SGP) tectal layers comprised numerous cells immunoreactive to all three CaBPr in different proportions. Only few retrogradely labeled tectorotundal SGC neurons expressed PV, CB or CR. The very large PV-ir neurons in SGC and SAC were not retrogradely labeled; morphologically they matched the efferent neurons with descending projections. SGC neurons of two chelonian species differed in the level of CO activity. Intense immunoreactivity to all three CaBPr and high CO activity were detected in both species in SGFS neuropil with some differences in sublaminar distribution patterns. The peculiarities of the CaBPr and CO activity distribution patterns in different segments of SGC neurons are discussed as related to the laminar organization of the turtle tectum and its retinal innervation. It is suggested that in the projection tectorotundal SGC neurons the CaBPr are concentrated mainly in their distal dendrites that contact retinal afferents in the superficial retinorecipient tectal layer.

Anatomical Specializations for Nocturnality in a Critically Endangered Parrot, the Kakapo (Strigops habroptilus)

The shift from a diurnal to nocturnal lifestyle in vertebrates is generally associated with either enhanced visual sensitivity or a decreased reliance on vision. Within birds, most studies have focused on differences in the visual system across all birds with respect to nocturnality-diurnality. The critically endangered Kakapo (Strigops habroptilus), a parrot endemic to New Zealand, is an example of a species that has evolved a nocturnal lifestyle in an otherwise diurnal lineage, but nothing is known about its' visual system. Here, we provide a detailed morphological analysis of the orbits, brain, eye, and retina of the Kakapo and comparisons with other birds. Morphometric analyses revealed that the Kakapo's orbits are significantly more convergent than other parrots, suggesting an increased binocular overlap in the visual field. The Kakapo exhibits an eye shape that is consistent with other nocturnal birds, including owls and nightjars, but is also within the range of the diurnal parrots. With respect to the brain, the Kakapo has a significantly smaller optic nerve and tectofugal visual pathway. Specifically, the optic tectum, nucleus rotundus and entopallium were significantly reduced in relative size compared to other parrots. There was no apparent reduction to the thalamofugal visual pathway. Finally, the retinal morphology of the Kakapo is similar to that of both diurnal and nocturnal birds, suggesting a retina that is specialised for a crepuscular niche. Overall, this suggests that the Kakapo has enhanced light sensitivity, poor visual acuity and a larger binocular field than other parrots. We conclude that the Kakapo possesses a visual system unlike that of either strictly nocturnal or diurnal birds and therefore does not adhere to the traditional view of the evolution of nocturnality in birds.

Calcium-binding proteins label functional streams of the visual system in a songbird

The vertebrate nervous system has been shown to contain high concentrations of intracellular calcium-binding proteins, each of them with a restricted expression pattern in specific brain regions and specific neuronal subpopulations. Using immunohistochemical staining techniques, we analyzed the expression pattern of calbindin, calretinin and parvalbumin in visual brain areas of a songbird species, the zebra finch ( Taeniopyga guttata). Here we show that the analyzed proteins are expressed in a complementary fashion within different brain substructures generally corresponding to functional subpathways of the avian visual system. In detail, calbindin is expressed in the brain structures that belong to the thalamofugal pathway, whereas parvalbumin-positive neurons are found in the brain structures that are part of the tectofugal visual pathway. Originally, the expression of calcium-binding proteins has been associated with specific morphological or neurochemical criteria of neurons. Our results suggest that their expression pattern also indicates a functional segregation of brain substructures linked to vision in the zebra finch brain. As the selective labeling of functional streams has also been shown for the visual system in mammalian species, function-selective expression of calcium-binding proteins might be a general feature of vertebrates.

Reduction of GABAergic neurons within the tectofugal visual system of white zebra finches

The central visual system of white zebra finches is physiologically and anatomically different from normally coloured (wild type) animals. The main difference to normal birds is an enhanced response to ipsilateral stimulation in all areas of the tectofugal visual pathway. Previous experiments indicated that besides an enhancement of recrossing fibers, it might be a lack of inhibition which causes this effect. We show here that such an explanation can only be true for a part of the entopallium, the telencephalic station of this projection. Only within the so-called perientopallium, the number of GABAergic neurons is strongly reduced, while there is no significant difference between white and wild type birds in the other visual areas. It is speculated that these neurons in normal birds inhibit ipsilateral input conveyed by the second visual projection in birds, the thalamofugal pathway.

Organization of the ectostriatum based on afferent connections in the zebra finch ( Taeniopygia guttata)

In birds with laterally-located eyes, such as zebra finches and pigeons, the tectofugal visual pathway is the most prominent route from the retina to the telencephalon. However, little is known about exactly how the visual information is processed in this pathway, especially at the core region of the ectostriatum (Ec) in the telencephalon. In order to reveal a detailed organization of Ec, we decided to systematically analyze the afferent connections of Ec by injecting small amounts of sensitive tracers (biotinylated dextran amine and cholera toxin subunit B) selectively into different regions of Ec and the thalamic center of the tectofugal pathway (the nucleus rotundus, Rt). The present study revealed a clearer picture of the organization of Ec subdivisions than previously known. The present results showed that the anterior portion of Rt sent a heavy projection to the ventral region of the anterior Ec, whereas the more caudal subdivisions of Rt sent projections to more caudal and dorsal portions in Ec. The results suggest that Ec subdivisions appear to be arranged along an axis ‘rotated’ in the anterior direction, almost parallel to other major telencephalic laminae. These results may clarify the physiological and chemical heterogeneity of Ec found in the previous studies. The present findings also provide an insight into the possible organization of a visual processing center in a non-mammal.

Integration of information from both eyes by single neurons of nucleus rotundus, ectostriatum and lateral neostriatum in the zebra finch ( Taeniopygia guttata castanotis Gould)

Although the optic nerve in birds crosses completely, visual information from the ipsilateral eye also reaches the ectostriatum, the telencephalic statibon of the tectofugal pathway, by recrossing fibers. These recrossing projections connect the contralateral tectum opticum with the ipsilateral nucleus rotundus, which in turn projects to the ectostriatum. The ectostriatum itself projects to the overlying lateral neostriatum, an area which serves an important role in sexual imprinting. This study shows that contralateral and ipsilateral information converges on single neurons within the nucleus rotundus, the ectostriatal region and the lateral neostriatum. In the three brain areas almost all isolated neurons exhibited responses to contralateral as well as bilateral visual stimuli. The number of neurons responding to ipsilateral stimuli increases from nucleus rotundus to the lateral neostriatum. We did not find any neurons driven exclusively by ipsilateral stimuli. The strength of ipsilateral responses is rather weak within the nucleus rotundus and ectostriatum, but shows a sharp increase in the lateral neostriatum. For most neurons of nucleus rotundus and ectostriatum, an additional ipsilateral stimulus did not significantly affect the response to a contralateral one. In contrast, a strong excitatory effect can be found in the neostriatum. The results are in agreement with previous evoked-potential studies and give new insights on the integration of ipsilateral and contralateral stimuli in zebra finch tectofugal visual pathway.

'Natural' and artificial monocular deprivation effects on thalamic soma sizes in pigeons.

The dominance for visual pattern analysis of the left hemisphere in normal pigeons and the concomitant morphological asymmetries in the optic tectum can be attributed to a 'natural' prehatch monocular deprivation of the left eye resulting from an asymmetrical embryonic position within the egg. Using control animals and pigeons which were monocularly deprived for 10 days after hatching, the present study could show that the cellular soma sizes of the nucleus rotundus within the tectofugal visual pathway are modified by light experience depending on the timepoint and direction of lateralized stimulation. Although rotundal cell size is thus ontogenetically modified in an activity-dependent manner, a detailed comparison makes it likely that the mechanisms which govern developmental plasticity of visual pathways differ between birds and mammals.

Single cell responses from the optic tectum of the zebra finch ( Taeniopygia guttata castanotis Gould)

Responses of neurons of the optic tectum, the prominent, highly laminated mesencephalic station of the tectofugal visual pathway in birds, to computer-generated and other visual stimuli were examined in zebra finches. Our study shows that the contralateral retina projects to the tectum in topographic order. The representation of the visual field is tilted against the horizon by 22°. The representation of the contralateral hemifield extends to the ipsilateral side by 15°. Most neurons have receptive fields with excitatory centres of different shapes and inhibitory surround. A new type of neuronal receptive field is described which has an excitatory centre and a surround which is movement sensitive and preferably excited by very small spots. The first type of neurons is mostly located in upper tectal layers, the latter only in deeper layers. Excitatory centre sizes increase with depth, and there is a tendency of smaller receptive fields in the foveal region. The representation of the frontal visual field does not show specializations which could be expected if it were used for fixation of grain during pecking. Our results are in accordance with previous behavioural experiments.

Color reversal-learning deficits after tectofugal pathway lesions in the pigeon telencephalon

Pigeons were post-operatively trained to discriminate two colors presented simultaneously. After reaching criterion on this task, they were required to perform a series of reversals of the color discrimination in which the positive and negative consequences of the stimuli were interchanged. Lesions of ectostriatum (the telencephalic target of the avian tectofugal visual pathway) impaired the ability of pigeons to learn a color-reversal task. An examination of the pattern of sparing and loss of performance on this task after lesions of various components of the ascending visual pathways suggests that deficits in color-reversal learning observed after lesions of the visual Wulst are not due to the Wulst's connections with the thalamofugal pathway. Instead, the data suggest that the visual Wulst maintains a role in color-reversal learning through its connections with the tectofugal pathway.

Hyperstriatum ventrale in pigeons: effects of lesions on color-discrimination and color-reversal learning.

Previous lesion studies of color-reversal learning in pigeons show that an impairment results when (1) the tectofugal visual pathway is damaged at either the thalamic level (nucleus rotundus) or the telencephalic level (ectostriatum), or (2) the thalamofugal visual pathway is damaged at the telencephalic level (the visual Wulst). An impairment does not result, however, when the thalamic source of thalamofugal input (n. opticus principalis thalami or OPT) to the visual Wulst is damaged. These results suggest that the visual Wulst plays a role in color-reversal learning as a consequence of visual information routed from the tectofugal pathway via other visual areas in the telencephalon. One such area is the hyperstriatum ventrale (HV). In the present study, after ablation of the medial and lateral regions of HV, pigeons were trained postoperatively to discriminate between two colors presented simultaneously. After reaching criterion, the pigeons were required to perform a series of discrimination reversals in which the positive and negative stimuli were interchanged. Lesions of medial HV resulted in impaired performance of a color-discrimination task (i.e. original learning), but did not affect discrimination reversal. An impairment in color-reversal learning resulted from combined damage to lateral HV and the fronto-thalamic tract (FT), which carries ascending visual input from OPT to the visual Wulst. No deficits were observed when either lateral HV or FT were damaged alone. These findings suggest that both the thalamofugal and tectofugal pathways provide the visual Wulst with visual input relevant to color-reversal learning.

Visual Lateralization in Birds: From Neurotrophins to Cognition?

Birds which are tested monocularly in visual discrimination tasks generally show higher performance levels with the right eye seeing. Due to the virtual complete decussation of the optic nerves, a right eye superiority is probably related to a left hemisphere dominance. If visual processes between the hemispheres differ, each half-brain might be differently prone to be deceived by visual illusions. Indeed pigeons tested with the herringbone illusions are deceived to a stronger extent with the right eye. These functional asymmetries are accompanied by anatomical left-right differences in the ascending thalamo- and tectofugal visual pathways in chicks and pigeons, respectively. The neuroanatomical and behavioral assymmetries result from an asymmetrical posture before hatching in which the embryo keeps his head turned to the right, such that the right eye is stimulated by light shining through the shell. The lateralization of adult animals are induced by this prehatching asymmetric photic stimulation since dark incubation abolishes behavioral and anatomical asymmetries. It is conceivable that the asymmetrical embryonal light stimulation increases the release of neurotrophins in the developing avian visual system in an activity dependent matter. Neurotrophins play an important role in neuronal survival and morphology and thus might represent a molecular switch bridging the gap from embryonal light stimulation to asymmetries of visual cognition in adults.

On the Structure and Function of the Tectofugal Visual Pathway in Laterally Eyed Birds

On the Structure and Function of the Tectofugal Visual Pathway in Laterally Eyed Birds

Visual Lateralization in Birds: from Neurotrophins to Cognition?

Birds which are tested monocularly in visual discrimination tasks generally show higher performance levels with the right eye seeing. Due to the virtual complete decussation of the optic nerves, a right eye superiority is probably related to a left hemisphere dominance. If visual processes between the hemispheres differ, each half-brain might be differently prone to be deceived by visual illusions. Indeed pigeons tested with the herringbone illusions are deceived to a stronger extent with the right eye. These functional asymmetries are accompanied by anatomical left-right differences in the ascending thalamo- and tectofugal visual pathways in chicks and pigeons, respectively. The neuroanatomical and behavioral assymmetries result from an asymmetrical posture before hatching in which the embryo keeps his head turned to the right, such that the right eye is stimulated by light shining through the shell. The lateralization of adult animals are induced by this prehatching asymmetric photic stimulation since dark incubation abolishes behavioral and anatomical asymmetries. It is conceivable that the asymmetrical embryonal light stimulation increases the release of neurotrophins in the developing avian visual system in an activity dependent matter. Neurotrophins play an important role in neuronal survival and morphology and thus might represent a molecular switch bridging the gap from embryonal light stimulation to asymmetries of visual cognition in adults.

On the structure and function of the tectofugal visual pathway in laterally eyed birds.

Of the two visual systems in vertebrates, the tectofugal pathway has often been attributed to stimulus localization, while the thalamofugal pathway was thought to be involved in stimulus identification. This review provides evidence that the tectofugal pathway serves both functions. It is speculated that the initial task of the tectum is to localize an object and to guide the fixation movement. The object in focus is then analysed by the higher stations of the tectofugal system. The result of the analysis is fed into the optic tectum and is used for decision about the treatment of the object.