Early monaural occlusion alters the neural map of interaural level differences in the inferior colliculus of the barn owl

Monaural occlusion during early life causes adaptive changes in the tuning of units in the owl's optic tectum to interaural level differences (ILD) that tend to align the auditory with the visual map of space. We investigated whether these changes could be due to experience-dependent plasticity occurring in the auditory pathway prior to the optic tectum. Units were recorded in the external nucleus of the inferior colliculus (ICx), which is a major source of auditory input to the optic tectum. The tuning of ICx units to ILD was measured in normal barn owls and in barn owls raised with one ear occluded. ILD tuning at each recording site was measured with dichotic noise bursts, presented at a constant average binaural level, 20 dB above threshold. The best ILD at each site was defined as the midpoint of the range of ILD values which elicited more than 50% of the maximum response. A physiological map of ILD was found in the ICx of normal owls: best ILDs changed systematically from right-ear-greater to left-ear-greater as the electrode progressed from dorsal to ventral. Best ILDs ranged from 13 dB right-ear-greater to 15 dB left-ear-greater and progressed at an average rate of 12 dB/mm. The representations of ILD were similar on both sides of the brain. In the ICx of owls raised with one ear occluded, the map of ILD was shifted in the adaptive direction: ILD tuning was shifted towards values favoring the non-occluded ear (the direction that would restore a normal space map). The average magnitude of the shift was on the order of 8-10 dB in each of 4 owls. In one owl, the mean shift in ILD tuning was almost identical on both sides of the brain. In another owl, the mean shift was much larger on the side ipsilateral to the occlusion than on the contralateral side. In both cases, the mean shifts measured in each ICx were comparable to the mean shifts measured in the optic tectum on the same sides of the brain. Thus, the adjustments in ILD tuning that have been observed in the optic tectum in response to monaural occlusion are almost entirely due to adaptive mechanisms that operate at or before the level of the ICx.     

Registration of neural maps through value-dependent learning: modeling the alignment of auditory and visual maps in the barn owl's optic tectum

In the optic tectum (OT) of the barn owl, visual and auditory maps of space are found in close alignment with each other. Experiments in which such alignment has been disrupted have shown a considerable degree of plasticity in the auditory map. The external nucleus of the inferior colliculus (ICx), an auditory center that projects massively to the tectum, is the main site of plasticity; however, it is unclear by what mechanisms the alignment between the auditory map in the ICx and the visual map in the tectum is established and maintained. In this paper, we propose that such map alignment occurs through a process of value-dependent learning. According to this paradigm, value systems, identifiable with neuromodulatory systems having diffuse projections, respond to innate or acquired salient cues and modulate changes in synaptic efficacy in many brain regions. To test the self-consistency of this proposal, we have developed a computer model of the principal neural structures involved in the process of auditory localization in the barn owl. This is complemented by simulations of aspects of the barn owl phenotype and of the experimental environment. In the model, a value system is activated whenever the owl carries out a foveation toward an auditory stimulus. A term representing the diffuse release of a neuromodulator interacts with local pre- and postsynaptic events to determine synaptic changes in the ICx. Through large-scale simulations, we have replicated a number of experimental observations on the development of spatial alignment between the auditory and visual maps during normal visual experience, after the retinal image is shifted through prismatic goggles, and after the reestablishment of normal visual input. The results suggest that value-dependent learning is sufficient to account for the registration of auditory and visual maps of space in the OT of the barn owl, and they lead to a number of experimental predictions.     

Tectal codification of eye movements in goldfish studied by electrical microstimulation. f

This work compares the tectal codification of eye movements in goldfish with those reported for other vertebrate groups. Focal electrical stimulation was applied in various tectal zones and the characteristics of evoked eye movements were examined as a function of (i) the position of the stimulation over the tectal surface, (ii) the initial position of the eyes and (iii) the parameters (pulse rate, current strength, duration) of the stimulus. In a large medial zone, stimulation within the intermediate and deep layers of the tectum evoked contraversive saccades of both eyes, whose direction and amplitude were roughly congruent with the retinotopic representation of the visual world within overlying layers. These saccades were minimally influenced by the initial position of the eye in the orbit. The topographical arrangement of evoked saccades and body movements suggests that this tectal zone triggers orienting responses in a similar way to those described in other vertebrates. Stimulations applied within the caudal tectum also evoked contraversive saccades, but in disagreement with the overlying retinotopic map--the vertical component was absent. Taken together with electrically evoked body movements reported in free-swimming fish, these saccades could reveal that this zone is involved in escape responses. When stimulations were applied within the anteromedial zone of the tectum, contraversive movements of both eyes appeared much more dependent on initial eye position. Saccades elicited from this area displayed characteristics of "goal-directed saccades" which were similar to those described in the cat. The generation of goal-directed movements from the anteromedial zone suggests that this portion of the goldfish optic tectum has a different intrinsic organization or is connected with the brainstem saccade generator in a different fashion than the medial zone. Finally, stimulation of the extreme anteromedial zone evoked convergent eye movements. These movements and those reported in free-swimming fish following electrical stimulation of this tectal area suggest that this zone could be involved in feeding responses. The relationships between the parameters of electrical stimulation and the characteristics of elicited saccades suggest that the stimulated location within the tectum determines a constant direction in the evoked saccade, whereas the amount and duration of tectal activity, as mimicked by changes in stimulus parameters, together with the tectal locus, determine the velocity and amplitude of the evoked saccade.     

Progress of topographic regulation of the visual projection in the halved optic tectum of adult goldfish

1. The patterns of re-established visual projections on to the rostral half-tectum are studied following excision of the caudal tectum at various intervals after section of either the contralateral optic nerve or the ipsilateral optic tract in adult goldfish. 2. The pattern of a newly restored retinotectal projection depends on the duration of the post-operative period given to the halved tectum before it is re-innervated by regenrating optic fibres from the retina. 3. When the duration is such that regenerating optic fibres invade the denervated rostral half-tectum at about 40 days or longer after excision of the caudal tectum, the remaining half-tectum is able to accommodate incoming optic fibres not only from the appropriate temporal hemi-retina but also from the foreign nasal hemiretina in an orderly compressed topographic pattern. 4. If the surgical operations are timed so that the halved tectum receive regenerating optic fibres earlier than 33 days after excision of the caudal tectum, the halved tectum initially accommodates only those optic fibres originating from the temporal half of the retina at this early stage. 5. This normal (uncompressed) pattern of the newly regenerated visual projection, however, eventually changes into an orderly compressed pattern at a later period. Post-operative dark-deprivation of the operated fish has no significant effect on the temporal transition. 6. The temporal transition from an initially normal pattern into an orderly compressed pattern may reflect the time course of progressive and systematic changes involved in topographic regulation of the halved tectum into a whole.     

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. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Development of the retinotectal system in the pigeon: a cytoarchitectonic and tracing study with cholera toxin

The optic tectum of the pigeon (Columba livia) is marked by morphological dorso-ventral and left-right differences. Both features seem to be related to functional specializations, but the responsible developmental mechanisms are unclear. Since the visual system becomes functional only after hatching, the developmental processes might be extended into the post-hatching period. The development of the asymmetries in the tectofugal system, however, depends on an asymmetric light stimulation acting already before hatching. As a first attempt to resolve this discrepancy, we examined the ontogeny of the retinotectal system by labeling the developing retinal projection with cholera toxin subunit B, in conjunction with an analysis of the cytoarchitectonic differentiation of the optic tectum. The data demonstrate that the first fibers to penetrate all retinoreceptive tectal layers could be observed from embryonic day 15 onwards, indicating that visual information could in principle be already processed before hatching. The afferent projection already exhibited the adult lamination pattern directly at the beginning of the invasion of the tectal layers; a surprising finding, since at that time the lamination pattern of the tectal layers did not have an adult appearance. The differentiation of the outer retinoreceptive laminae started only when the whole optic tectum was occupied by retinal fibers, 4 days after hatching, and was finished a week later. The dorso-ventral differences in the thickness of layers 4 and 5 were not apparent before the first week after hatching. The late appearance of these differences indicates that their maturation may be influenced by retinal input.     

Larval development of tectal efferents and afferents in Xenopus laevis (Amphibia Anura)

The development of tectal connections in Xenopus laevis had been investigated using the degeneration technique to demonstrate the efferent pathways and the retrograde HRP transport to label the afferent pathways. Bilateral tectal efferents were present as soon as the beginning of metamorphosis. Ascending efferents originated from the anterior tectal part terminate in the secondary visual thalamic centres whereas the descending efferents coming from the posterior tectal part reached the tegmentum and the medulla oblongata. At this same time, the optic tectum already received secondary visual afferents originating in the ipsilateral pretectum and non-visual afferents from the ipsilateral semicircular torus and tegmentum. Some sparse bilateral isthmotectal connections were also present. Later, efferent pathways showed an increasing number of fibres whereas the sites of origin of afferents became more diversified: the dorsal thalamus, the suprachiasmatic area, the tegmental nuclei and in the medulla oblongata, the reticular and octavolateral areas sent bilateral projections to the optic tectum. At the end of metamorphosis, we noted ipsilateral olivotectal fibres and reciprocal connections between the tectum and the area of the Vth nerve. These last findings and the presence of the following direct projections, not previously reported in Anurans: the reciprocal connections between the tectum and the semicircular torus or the octavolateral area, underline the implication of the optic tectum in the multisensory (visual, acoustic, vibratory) integration elicited during the larval behavior. Also, the relations between the optic tectum and the lateral line system are particularly examined in the discussion.     

Retinal projections in the electric catfish (Malapterurus electricus)

The poorly developed visual system of the electric catfish was studied with silver-degeneration methods. Retinal projections were entirely contralateral to the hypothalamic optic nucleus, the lateral geniculate nucleus, the dorsomedial optic nucleus, the pretectal nuclei including the cortical nucleus, and the optic tectum. The small size and lack of differentiation of the visual system in the electric catfish suggest a relatively small role for this sensory system in this species.     

Immunocytochemical localization of the GABAA/benzodiazepine receptor beta2/beta3 subunits in the optic tectum of the salmon

The optic tectum of the salmon is a primary visual center with direct input from the retina via the optic tract. The structure is homologous with the superior colliculus of the mammalian brain. We have studied the distribution of immunoreactivity against the GABAA/benzodiazepine receptor beta2/beta3 subunits with a monoclonal antibody (BD-17) in the optic tectum of the salmon brain. A weak immunoreactivity is found in the rostral stratum marginale (SM), strong labelling of the neuropil is shown in a thin band in stratum opticum (SO), two bands in stratum fibrosum et griseum superficiale (SFGS) and two bands in stratum griseum centrale (SGC). Immunoreactive perikarya with neurites that extend radially through the stratum album centrale (SAC) are located in the stratum periventriculare. BD-17 immunoreactivity is to a great extent located in tectal layers that receive direct retinal input, i.e. the SO, SFGS and SGC. These layers are known to receive input also from other visual centers, such as the pretectum (SO, SFGS), the nucleus isthmi (SO, SFGS, SGC), as well as non-visual regions as the telencephalon (SGC). High levels of 2-[125I]-iodomelatonin binding sites have previously been demonstrated in all layers of the salmon optic tectum except the SM and SPV. Thus it appears likely that GABA and/or benzodiazepines and melatonin play a role in visual processing in the optic tectum of teleost fish.     

Ocular motor abnormalities in Huntington's disease

We review here the eye movements in patients with Huntington's disease (HD), concentrating upon saccades as they show the most prominent abnormalities. Inability to suppress reflexive glances to suddenly appearing novel visual stimuli and delayed initiation of voluntary saccades, including predictive saccades, are early and consistent findings. These two abnormalities can be interpreted in the context of a model, based upon the idea that the frontal lobes and basal ganglia contribute more to the control of voluntary than to reflexive types of saccades. Most patients eventually also show slow saccades but they are most prominent when the disease is early-onset. Slowing of saccades may reflect involvement of both the higher-level cerebral centers that trigger saccades and the areas in the brain stem that produce premotor saccade commands. The study of eye movements in HD has led to a fruitful interaction between basic science and clinical investigation, and has served as a paradigm for examining higher-level defects in saccadic eye movement control in patients with various degenerative, neurological diseases or with focal cerebral hemispheral lesions.     

Glutamate receptor binding in juvenile and adult Rana pipiens CNS

Autoradiographic methods were used to map NMDA- and quisqualate-sensitive glutamate binding sites in the brain of mature and juvenile Rana pipiens frogs. NMDA- and quisqualate-sensitive sites were consistently co-localized in the CNS. The highest glutamate binding occurred in the telencephalon, hypothalamus, and cerebellum. Glutamate binding sites were also specifically localized in visual pathways, including the superficial neuropil of the optic tectum, consistent with glutamate being the retinal ganglion cell neurotransmitter. The distribution of glutamate binding sites in the brain of juvenile postmetamorphic frogs was similar to that in adults. In general, Quis binding increased about twofold in adults compared to juveniles, whereas NMDA binding did not show a comparable developmental increase. To test whether glutamate binding sites are located on retinal axon terminals or on tectal cell dendrites in the optic tectum, juvenile postmetamorphic frogs were enucleated unilaterally, and receptor binding was performed following 1, 3, 7, and 14 days survival. The denervated tectal neuropil showed a delayed decrease in NMDA- and quisqualate-sensitive binding, consistent with the receptors being located on postsynaptic tectal cell dendrites.     

Serotonin modulates induced synaptic activity in the optic tectum of the frog

The extent to which retinal signals are modulated at central sites is unknown. We sought to determine the effects of serotonin, a neurotransmitter present in the retinorecipient layers of the frog tectum, on retinotectal transmission. Acute electrical stimulation delivered to the retinorecipient layer of optic tectum brain slices was used to model the activation of tectal neurons by visual inputs. This stimulation evoked either a monosynaptic or a polysynaptic current response in patch-clamped tectal neurons. External application of serotonin blocked both of these induced currents as did 5-carbotryptamine (5-CT), a nonselective agonist of 5-HT1 receptors. Alpha-methylserotonin, a nonselective agonist of 5-HT2 receptors, also blocked polysynaptic responses but was less effective than either serotonin or 5-CT in blocking monosynaptic ones. Lateral synaptic interactions between tectal cells, modeled by acute electrical stimulation in the main cellular layer of the tectum, were also blocked by serotonin, 5-CT or alpha-methylserotonin. The presented data suggest that endogenous serotonin may strongly affect visual signal processing by modulating synaptic transmission between both the retina and the tectum as well as between tectal neurons. This modulation is likely to be due, at least in part, to a demonstrated outward current induced by serotonin in a subpopulation of tectal cells.     

Capacity for plasticity in the adult owl auditory system expanded by juvenile experience

In the process of creating a multimodal map of space, auditory-visual neurons in the optic tectum establish associations between particular values of auditory spatial cues and locations in the visual field. In the barn owl, tectal neurons reveal these associations in the match between their tuning for interaural time differences (ITDs) and the locations of their visual receptive fields (VRFs). In young owls ITD-VRF associations can be adjusted by experience over a wide range, but the range of adjustment normally becomes quite restricted in adults. This normal range of adjustment in adults was greatly expanded in owls that had previously learned abnormal ITD-VRF associations as juveniles. Thus, the act of learning abnormal associations early in life leaves an enduring trace in this pathway that enables unusual functional connections to be reestablished, as needed, in adulthood, even when the associations represented by these connections have not been used for an extended period of time.     

Roger Sperry and his chemoaffinity hypothesis

In the early 1940s, Roger Sperry performed a series of insightful experiments on the visual system of lower vertebrates that led him to draw two important conclusions: When optic fibers were severed, the regenerating fibers grew back to their original loci in the midbrain tectum to re-establish a topographical set of connections; and the re-establishment of these orderly connections underlay the orderly behavior of the animal. From these conclusions, he inferred that each optic fiber and each tectal neuron possessed cytochemical labels that uniquely denoted their neuronal type and position and that optic fibers could utilize these labels to selectively navigate to their matching target cell. This inference was subsequently formulated into a general explanation of how neurons form ordered interconnections during development and became known as the chemoaffinity hypothesis. The origins of this hypothesis, the controversies that surrounded it for several decades and its eventual acceptance, are discussed in this article.     

Gait characteristics of the anterior cruciate ligament-deficient varus knee

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.     

Synchronizing retinal activity in both eyes disrupts binocular map development in the optic tectum

Spatiotemporal correlations in the pattern of spontaneous and evoked retinal ganglion cell (RGC) activity are believed to influence the topographic organization of connections throughout the developing visual system. We have tested this hypothesis by examining the effects of interfering with these potential activity cues during development on the functional organization of binocular maps in the Xenopus frog optic tectum. Paired recordings combined with cross-correlation analyses demonstrated that exposing normal frogs to a continuous 1 Hz of stroboscopic illumination synchronized the firing of all three classes of RGC projecting to the tectum and induced similar patterns of temporally correlated activity across both lobes of the nucleus. Embryonic and eye-rotated larval animals were reared until early adulthood under equivalent stroboscopic conditions. The maps formed by each RGC class in the contralateral tectum showed normal topography and stratification after strobe rearing, but with consistently enlarged multiunit receptive fields. Maps of the ipsilateral eye, formed by crossed isthmotectal axons, showed significant disorder and misalignment with direct visual input from the retina, and in the eye-rotated animals complete compensatory reorientation of these maps usually induced by this procedure failed to occur. These findings suggest that refinement of retinal arbors in the tectum and the ability of crossed isthmotectal arbors to establish binocular convergence with these retinal afferents are disrupted when they all fire together. Our data thus provide direct experimental evidence that spatiotemporal activity patterns within and between the two eyes regulate the precision of their developing connections.     

Neurotrophins in the developing and regenerating visual system

The neurotrophins NGF, BDNF, NT-3 and NT-4 have a wide range of effects in the development and regeneration of neural circuits in the visual system of vertebrates. This review focuses on the localization and functions of neurotrophins in the retina, lateral geniculate nucleus, suprachiasmatic nucleus, superior colliculus/optic tectum, and isthmic nuclei. Research of the past 20 years has shown that neurotrophins and their receptors are localized in numerous visual centers from the retina to the visual cortex, and that neurotrophins influence proliferation, neurite outgrowth and survival of cells in the visual system in vitro and in vivo. A relationship between electrical activity and neurotrophic functions has been established in several visual centers in the CNS, and neurotrophins have been implicated in synaptic plasticity in the visual cortex. Besides functions of neurotrophins as retrograde, target-derived trophic factors, recent data indicate that neurotrophins may have anterograde, afferent as well as local, paracrine actions in the retina, optic nerve and the visual cortex. Some neurotrophins appear to regulate proliferation and survival of glial cells in the optic pathways. Neurotrophins increase the survival of retinal ganglion cells after axotomy or ischemia and they promote the regeneration of retinal ganglion cell axons in some vertebration. Neurotrophins also rescue photoreceptors from degeneration. These findings implicate the neurotrophins not only as important regulators during development, but also as potential therapeutic agents in degenerative retinal diseases and after optic nerve injury.     

When is it best to hear a verb? The effects of the timing and focus of verb models on children''s learning of verbs

Recent neurophysiological studies of the saccadic ocular motor system have lent support to the hypothesis that this system uses a motor error signal in retinotopic coordinates to direct saccades to both visual and auditory targets. With visual targets, the coordinates of the sensory and motor error signals will be identical unless the eyes move between the time of target presentation and the time of saccade onset. However, targets from other modalities must undergo different sensory-motor transformations to access the same motor error map. Because auditory targets are initially localized in head-centered coordinates, analyzing the metrics of saccades from different starting positions allows a determination of whether the coordinates of the motor signals are those of the sensory system. We studied six human subjects who made saccades to visual or auditory targets from a central fixation point or from one at 10 degrees to the right or left of the midline of the head. Although the latencies of saccades to visual targets increased as stimulus eccentricity increased, the latencies of saccades to auditory targets decreased as stimulus eccentricity increased. The longest auditory latencies were for the smallest values of motor error (the difference between target position and fixation eye position) or desired saccade size, regardless of the position of the auditory target relative to the head or the amplitude of the executed saccade. Similarly, differences in initial eye position did not affect the accuracy of saccades of the same desired size. When saccadic error was plotted as a function of motor error, the curves obtained at the different fixation positions overlapped completely. Thus, saccadic programs in the central nervous system compensated for eye position regardless of the modality of the saccade target, supporting the hypothesis that the saccadic ocular motor system uses motor error signals to direct saccades to auditory targets.     

Release of exqenous glycine in the pigeon optic tectum during stimulation of a midbrain nucleus

A pathway having an affinity for glycine has been investigated in the pigeon optic lobe; it originates in the nucleus isthmi pars parvocellularis (Ipc) and terminates in the tectum, In an attempt to obtain evidence that glycine plays a role as a transmitter in this system, the effect of electrical stimulation on release of labeled substances previously injected in the tectum was tested. By perfusing the upper strata of the optic tectum with a push-pull cannula the release of radioactive glycine was shown to be markedly increased by electrical stimulation of Ipc, but not by stimulation of other sites. Ipc stimulation did not affect the efflux of exogenous leucine or urea, whereas a GABA release was observed. With K+ (40 mM) stimulation all amino acids tested were released. It is suggested that the Ipc neuron terminals in the tectum take up glycine and release it upon stimulation of the Ipc nucleus.     

The central projections in the retina in Necturus maculosus

The projections of the retina in Necturus maculosus were studied by injecting radioactive proline into one eye. Labeling was seen in both the contralateral and ipsilateral diencephalon and tectum. The contralateral fibers are divided into three major tracts: the marginal, axial, and basal. The ipsilateral fibers separate into a marginal and an axial optic tract. The contralateral and ipsilateral axial optic tracts have a similar distribution. The contralateral and ipsilateral marginal optic tracts projecting to the diencephalon also have a similar distribution. However, in the tectum the ipsilateral marginal optic tract ends in the anterior third while the contralateral extends almost the entire length of the tectum. The retinotectal ipsilateral projection ends in clumps as has been described in other vetebrates. A direct ipsilateral retinotectal projection has not been described in any other amphibian.