Parallel Morphological and Functional Development in the Xenopus Retinotectal System

The cytoarchitecture, fiber connections, and ultrastructure of the nucleus pretectalis superficialis pars magnocellularis (PSm) were studied in cypriniform teleosts (Cyprinus carpio). The PSm is an oval nucleus in the pretectum. Medium-sized cells and synaptic glomeruli are the main components of the nucleus. A lesser number of small cells are also present. Most of the medium-sized cells form one or two cell layers on the periphery of the nucleus, and some cells are scattered among synaptic glomeruli in the nucleus. Cell bodies in the peripheral cell layer are pyriform and sprout a thick dendrite directed inward. The dendrite gives off fine dendritic branches, which are postsynaptic elements in synaptic glomeruli. The PSm projects to the ipsilateral corpus mamillare (CM) and sends collaterals to the ipsilateral nucleus lateralis valvulae (NLV). Axons of the PSm neurons have terminals with many varicosities in the CM, and collaterals in the NLV have cup-shaped terminals around the cell bodies of the NLV neurons. Following horseradish peroxidase (HRP) injections into the PSm, HRP-labeled cells are found ipsilaterally in the optic tectum, the nucleus tractus rotundus of Schnitzlein, and the nucleus ruber of Goldstein. The tecto-PSm projections are topographically organized. The rostral optic tectum projects mainly to the rostral portion of the PSm, and the caudal tectum projects to the caudal portion of the PSm. The ventral tectum sends fibers mainly to the ventral part of the PSm. The dorsomedial tectum projects to the medial part of the PSm, and the dorsolateral tectum projects to the lateral part of the PSm. Tectal projection neurons to the PSm are of only one type. The tectal cell body is pyriform and is situated in the superficial part of the ipsilateral stratum periventriculare (SPV). The tectal neurons have a long perpendicular dendrite, which branches out in the stratum opticum (SO). An axon emerges from the branching site in the SO. Judging from the dendritic branching pattern of the tectal projection neurons, we concluded that the PSm receives visual information from the optic tectum.

Chick embryos and young hatchling chicks have undergone unilateral retinal ablation and the brains were subsequently prepared for modified Fink-Heimer staining to detect degenerating axoplasm. Additional animals have been injected with tritiated proline or combinations of tritiated proline and tritiated fucose. In examining the patterns of degeneration and labelling produced, it appears that during the stage 40-44 period of embryonic life there is a critical period during which damage to retinal axons produces degeneration not only in the direct targets of the optic tract (primary centers), but also in a number of nuclei not projected to by the optic tract (secondary centers). By examining various survival times following retinal ablation and animals of varying embryonic and post-hatch age, we have concluded that retinal ablation during the critical period causes a rapid and fulminant degeneration in the secondary centers because they are all targets of the projection from the optic tectum, itself a prime target of the optic projection. Presumably, interruption of the retino-tectal projection during the critical period disrupts some as yet undefined trophic relationship between these two sets of neurons. Our studies show that the observed degenerative reaction in the secondary centers occurs most strongly in chick embryos between stage 40 and stage 44. This period coincides with the onset of synaptogenesis in the retino-tectal system (Rager, '76a,b). We therefore hypothesize that during this period some property or influence is passing from the retinal to the tectal neurons such that interruption of this process leads to death of the tectal neurons.

Across the rostrocaudal (RC) axis of the Xenopus tadpole optic tectum exists a developmental gradient. This gradient has served as a useful model to study many aspects of synapse and dendrite maturation. To compliment these studies, we characterized how the intrinsic excitability, the ease in which a neuron can fire action potentials, might also be changing across the same axis. Whole-cell recordings from tectal neurons at different points along the RC axis revealed a graded increase in intrinsic excitability: compared with neurons at the caudal end of the tectum, neurons at the rostral end fired more action potentials in response to current injection and expressed greater peak Na⁺ and K⁺ currents, the major intrinsic currents in these neurons that underlie the action potential. We also observed, along the same axis and in the same direction, a previously described increase in the amount of synaptic drive received by individual neurons (Wu GY, Malinow R, Cline HT. Science 274: 972-976, 1996). Thus as synaptic activity ramps up across the RC axis, so does intrinsic excitability. The reduction of overall circuit activity induced a compensatory scaling up of peak Na⁺ and K⁺ currents only in the caudal portion of the tectum, suggesting a region-specific, compensatory form of plasticity.

Transorbital alternating current stimulation modifies BOLD activity in healthy subjects and in a stroke patient with hemianopia: A 7 Tesla fMRI feasibility study

Metaplasticity Governs Natural Experience-Driven Plasticity of Nascent Embryonic Brain Circuits

Postembryonic brain development is sensitive to environmental input and sensory experience, but the mechanisms underlying healthy adaptive brain growth are poorly understood. Here, we tested the importance of visual experience on larval zebrafish (Danio rerio) postembryonic development of the optic tectum (OT), a midbrain structure involved in visually guided behavior. We first characterized postembryonic neurogenic growth in OT, in which new neurons are generated along the caudal tectal surface and contribute appositionally to anatomical growth. Restricting visual experience during development by rearing larvae in dim light impaired OT anatomical and neurogenic growth, specifically by reducing the survival of new neurons in the medial periventricular gray zone. Neuronal survival in the OT was reduced only when visual experience was restricted for the first 5 d following new neuron generation, suggesting that tectal neurons exhibit an early sensitive period in which visual experience protects these cells from subsequent neuronal loss. The effect of dim rearing on neuronal survival was mimicked by treatment with an NMDA receptor antagonist early, but not later, in a new neuron's life. Both dim rearing and antagonist treatment reduced BDNF production in the OT, and supplementing larvae with exogenous BDNF during dim rearing prevented neuronal loss, suggesting that visual experience protects new tectal neurons through neural activity-dependent BDNF expression. Collectively, we present evidence for a sensitive period of neurogenic adaptive growth in the larval zebrafish OT that relies on visual experience-dependent mechanisms.SIGNIFICANCE STATEMENT Early brain development is shaped by environmental factors via sensory input; however, this form of experience-dependent neuroplasticity is traditionally studied as structural and functional changes within preexisting neurons. Here, we found that restricting visual experience affects development of the larval zebrafish optic tectum, a midbrain structure involved in visually guided behavior, by limiting the survival of newly generated neurons. We found that new tectal neurons exhibit a sensitive period soon after cell birth in which adequate visual experience, likely mediated by neuronal activity driving BDNF production within the tectum, would protect them from subsequent neuronal loss over the following week. Collectively, we present evidence for neurogenic adaptive tectal growth under different environmental lighting conditions.

Calretinin-like immunoreactivity in the optic tectum of the tench ( Tinca tinca L.)

The formation of fine retinotopic order by growing optic fibers in the goldfish is thought to be mediated by the correlated firing of optic fibers from neighboring retinal ganglion cells. Although the activity of the tectal cells must also be important for this activity-dependent refinement, few studies have analyzed the pattern and local correlation of the intrinsic activity of tectal neurons and the effect of denervation on this activity. To address this issue, spontaneous (nonoptic driven) activity was analyzed and cross-correlograms were computed between individual tectal neurons using single and double electrode extracellular recordings. Recordings were made in normally innervated tectum in which the contribution of optic activity was eliminated by short-term intraocular blockade with tetrodotoxin and in denervated tecta in which the optic nerve had been severed several weeks prior. Several observations were relevant to activity-dependent refinement: First, coupling between neighboring tectal cells is weak. Second, the time duration for local correlation is relatively long, as long as 200 ms. Third, tectal neurons exhibit spontaneous bursting. Fourth, denervation increased the level of spontaneous activity in the tectum. The increased spontaneous activity and bursting following denervation implies that tectal neurons are more excitable when optic fibers are beginning to reinnervate the tectum. This could make it possible for optic fibers to drive tectal neurons at a time when their input to individual neurons is severely weakened by a lack of spatial convergence. The weak coupling between tectal cells and the consequent long-time constant for correlated activity implies a constraint on the duration of correlated retinal activity that is used for activity-dependent refinement. Since optic fibers likely need to detect the postsynaptic activity of a local group of tectal neurons, rather than that of a single neuron, the long tectal time constant means that retinal activity need not be correlated with precision much better than 200 ms because the postsynaptic circuitry cannot generate shorter correlations.

Birds can rapidly and accurately detect moving objects for better survival in complex environments. This visual ability may be attributed to the response properties of neurons in the optic tectum. However, it is unknown how neurons in the optic tectum respond differently to moving objects compared to static ones. To address this question, neuronal activities were recorded from domestic pigeon (Columba livia domestica) optic tectum, responsible for orienting to moving objects, and the responses to moving and flashed stimuli were compared. An encoding model based on the Generalized Linear Model (GLM) framework was established to explain the difference in neuronal responses. The experimental results showed that the first spike latency to moving stimuli was smaller than that to flashed ones and firing rate was higher. The model further implied the faster and stronger response to a moving target result from spatiotemporal integration process, corresponding to the spatially sequential activation of tectal neurons and the accumulation of information in time. This study provides direct electrophysiological evidence about the different tectal neuron responses to moving objects and flashed ones. The findings of this investigation increase our understanding of the motion detection mechanism of tectal neurons.

Nucleus rotundus is the primary thalamic recipient of projections from the optic tectum in pond turtles. Although the projection of the retina to the optic tectum is known to be topographically organized, earlier studies suggest that the tectorotundal projection is not topographically organized. Three types of analyses are used in this paper to characterize the organization of the projection of the optic tectum to nucleus rotundus. First, large iontophoretic injections of horseradish peroxidase into the optic tectum anterogradely fill axons with reaction product after the use of a cobalt-enhanced diaminobenzidine procedure. These preparations show that shafts of axons in the tectothalamic tract give rise to thinner, primary collaterals that enter nucleus rotundus from its caudolateral aspect and form sparsely branching arbors within the nucleus. Very thin secondary collaterals branch from these collateral bear terminal collaterals with frequent varicosities. Although the total size of such arbors is unknown, the evidence suggests that each arbor is large in relation to the size of nucleus rotundus. Thus, injection sites restricted to central tectum label axons throughout nucleus rotundus. Second, subtotal lesions of the tectum produce degeneration throughout nucleus rotundus in silver degeneration preparations. Finally, analysis of electron microscopic degeneration material indicates that tectal boutons are distributed along the full lengths of the dendrites of rotundal neurons, but not on their somata. These boutons form asymmetric synaptic junctions and contain round synaptic vesicles. In view of the relatively large size of the dendritic fields of rotundal neurons, these data suggest that the tectorotundal projection is both strongly convergent on individual neurons and strongly divergent from single tectorotundal axons. This type of organization is consistent with physiological evidence that rotundal neurons have receptive fields that cover at least one-half of the contralateral visual field and often include the entire hemifield. It seems unlikely that nucleus rotundus can be involved in neuronal transactions that preserve detailed spatial information, but it may be involved in processing information on other visual parameters such as stimulus velocity or color.

In contrast to vision, where retinotopic mapping alone can define areal borders, primary auditory areas such as A1 are best delineated by combining in vivo tonotopic mapping with post mortem cyto- or myelo-architectonics from the same individual. We combined high-resolution (800 μm) quantitative T1 mapping with phase-encoded tonotopic methods to map primary auditory areas (A1 and R) within the ‘auditory core’ of human volunteers. We first quantitatively characterize the highly myelinated auditory core in terms of shape, area, cortical depth profile, and position, with our data showing considerable correspondence to post-mortem myeloarchitectonic studies, both in cross-participant averages and in individuals. The core region contains two ‘mirror-image‘ tonotopic maps oriented along the same axis as observed in macaque and owl monkey. We suggest that thee two maps within the core are the human analogues of primate auditory areas A1 and R. The core occupies a much smaller portion of tonotopically organized cortex on the superior temporal plane and gyrus than is generally supposed. The multi-modal approach to defining the auditory core will facilitate investigations of structure-function relationships, comparative neuroanatomical studies, and promises new biomarkers for diagnosis and clinical studies.

The avian optic tectum is composed of at least 15 separate laminae that are distinguishable on the basis of their morphological features and patterns of afferent and efferent connectivity. Layer 5b, a major retinorecipient layer, exhibits dense, dust-like, neuropeptide Y-positive (NPY+) immunoreactive labeling, whereas sparse, larger caliber NPY+ fibers are found in laminae 4 and 7. Anterograde and retrograde labeling techniques, immunohistochemistry, and retinal lesion studies were used to determine the source of this tectal NPY+ labeling. NPY+ was not detectable in cells of the optic tectum or in retinal ganglion cells, and retinal ablation did not diminish the abundance of tectal NPY+ fibers. Neurons of two nuclei previously shown to be sources of tectal input, the nucleus pretectalis (PT) and the intergeniculate leaflet (IGL; Brecha, 1978), were found to be NPY+. Unilateral injection of retrograde tracers into the tectum resulted in bilateral labeling of neurons within PT, and injections of anterograde tracer into PT confirmed that this nucleus projected bilaterally to layer 5b of the optic tectum. Unilateral lesions of PT nearly eliminated NPY+ fibers in the ipsilateral layer 5b and significantly reduced them in the contralateral layer 5b. Bilateral lesions of PT eliminated NPY+ fibers bilaterally in layer 5b. However, these PT lesions had little effect on the NPY+ fibers in layers 4 and 7. Combined retrograde and immunohistochemical studies showed that NPY+ neurons of the IGL project to the optic tectum, and anterograde studies demonstrated that IGL projects to layers 4 and 7. The NPY+ projection to laminae 5b from PT is one of many inputs, which include cholinergic afferents from the nucleus isthmi parvicellularis, terminals from retinal ganglion cells, and dendrites of layer 13 neurons (Karten et al., 1993). The NPY+ input to layer 5b may modulate visual information flow from retinal input to various tectal neurons, including those in layer 13.

PROJECTION OF THE RETINA ON SUPERIOR COLLICULUS OF CATS

OPINION article Front. Integr. Neurosci., 18 August 2011 Volume 5 - 2011 | https://doi.org/10.3389/fnint.2011.00040

Xenopus frogs have a prominent binocular field that develops as a consequence of the migration of the eyes during the remodeling of the head during and after metamorphosis. In the optic tectum, a topographic representation of the ipsilateral eye develops during this same period. It is relayed indirectly, via the nucleus isthmi. In the early stages of binocular development, the topographic matching of the ipsilateral input to the retinotectal input from the contralateral eye is largely governed by chemical cues, but the ultimate determinant of the ipsilateral map is binocular visual input. Visual input is such a dominant factor that abnormal visual input resulting from unilateral eye rotation can induce isthmotectal axons to alter their trajectories dramatically, even shifting their terminal zones from one pole of the tectum to the other. This plasticity normally is high only during a 3-4-month critical period of late tadpole-early juvenile life, but the critical period can be extended indefinitely by dark-rearing. N-methyl-D-aspartate (NMDA) receptors are involved in this process; plasticity can be blocked or promoted by chronic treatment with NMDA antagonists or agonists, respectively. Cholinergic nicotinic receptors on retinotectal axons are likely to play an essential role as well. Modifications in the polysialylation of neural cell adhesion molecule are correlated with the state of plasticity. The circuitry underlying binocular plasticity is not yet fully understood but has proved not to be a simple convergence of ipsilateral and contralateral inputs onto the same targets.