Tectal Output Research Articles

Dissecting the Tectal Output Channels for Orienting and Defense Responses.

Electrical stimulation and lesion experiments in 1980’s suggested that the crossed descending pathway from the deeper layers of superior colliculus (SCd) controls orienting responses, while the uncrossed pathway mediates defense-like behavior. To overcome the limitation of these classical studies and explicitly dissect the structure and function of these two pathways, we performed selective optogenetic activation of each pathway in male mice with channelrhodopsin 2 (ChR2) expression by Cre driver using double viral vector techniques. Brief photostimulation of the crossed pathway evoked short latency contraversive orienting-like head turns, while extended stimulation induced body turn responses. In contrast, stimulation of the uncrossed pathway induced short-latency upward head movements followed by longer-latency defense-like behaviors including retreat and flight. The novel discovery was that while the evoked orienting responses were stereotyped, the defense-like responses varied considerably depending on the environment, suggesting that uncrossed output can be influenced by top-down modification of the SC or its target areas. This further suggests that the connection of the SCd-defense system with non-motor, affective and cognitive structures. Tracing the whole axonal trajectories of these two pathways revealed existence of both ascending and descending branches targeting different areas in the thalamus, midbrain, pons, medulla, and/or spinal cord, including projections which could not be detected in the classical studies; the crossed pathway has some ipsilaterally descending collaterals and the uncrossed pathway has some contralaterally descending collaterals. Some of the connections might explain the context-dependent modulation of the defense-like responses. Thus, the classical views on the tectal output systems are updated.

Direction selectivity in the visual system of the zebrafish larva

Neural circuits in the vertebrate retina extract the direction of object motion from visual scenes and convey this information to sensory brain areas, including the optic tectum. It is unclear how computational layers beyond the retina process directional inputs. Recent developmental and functional studies in the zebrafish larva, using minimally invasive optical imaging techniques, indicate that direction selectivity might be a genetically hardwired property of the zebrafish brain. Axons from specific direction-selective (DS) retinal ganglion cells appear to converge on distinct laminae in the superficial tectal neuropil where they serve as inputs to DS postsynaptic neurons of matching specificity. In addition, inhibitory recurrent circuits in the tectum might strengthen the DS response of tectal output neurons. Here we review these recent findings and discuss some controversies with a particular focus on the zebrafish tectum’s role in extracting directional features from moving visual scenes.

A Cholinergic Gating Mechanism Controlled by Competitive Interactions in the Optic Tectum of the Pigeon

We describe the operation of a midbrain neural circuit in pigeons that may participate in selecting and attending to one visual stimulus from the myriad displayed in their visual environment. This mechanism is based on a topographically organized cholinergic signal reentering the optic tectum (TeO). We have shown previously that, whenever a visual stimulus activates neurons in a given tectal location, this location receives a strong bursting feedback from cholinergic neurons of the nucleus isthmi pars parvocellularis (Ipc), situated underneath the tectum. Here we show that, if a second visual stimulus is presented, even far from the first, the feedback signal to the first tectal location is diminished or suppressed, and feedback to the second tectal location is initiated. We found that this long-range suppressive interaction is mostly mediated by the nucleus isthmi pars magnocellularis, which sends a wide-field GABAergic projection to Ipc and TeO. In addition, two sets of findings indicate that the feedback from the Ipc modulates the ascending output from the TeO. First, visually evoked extracellular responses recorded in the dorsal anterior subdivision of the thalamic nucleus rotundus (RtDa), receiving the ascending tectal output, are closely synchronized to this feedback signal. Second, local inactivation of the Ipc prevents visual responses in RtDa to visual targets moving in the corresponding region of visual space. These results suggest that the ascending transmission of visual activity through the tectofugal pathway is gated by this cholinergic re-entrant signal, whose location within the tectal visual map is dynamically defined by competitive interactions.

Histological study on cytoarchitecture of tectal output pathway controlling prey orienting behavior in Rana catesbeiana

Histological study on cytoarchitecture of tectal output pathway controlling prey orienting behavior in Rana catesbeiana

Monoaminergic markers in the optic tectum of the domestic chick

The avian optic tectum has become a reliable model system to study the basic mechanisms that underlie the computation of visual stimuli. Many aspects of its cytoarchitecture, chemoarchitecture, connectivity and development are thoroughly characterized. However, knowledge about its monoaminergic innervation is still incomplete. As a prerequisite to understand a possible functional role of the monoaminergic neurotransmitters, the serotonergic, noradrenergic, and dopaminergic innervation of the optic tectum as well as the distribution of serotonin 2A receptors, the dopamine- and cAMP-regulated phosphoprotein DARPP-32 and calbindin D-28K was studied in domestic chicks by immunohistochemical techniques.Serotonergic, noradrenergic, and tyrosine hydroxylase positive axons and axon terminals were present in all layers of the optic tectum. Generally, the highest densities of serotonergic, noradrenergic, and tyrosine hydroxylase positive fibers were found in the superficial tectal layers 1–8, whereas only moderate densities of serotonergic, noradrenergic, and tyrosine hydroxylase positive fibers became obvious in the deep tectal layers 9–15. Serotonergic fibers were particularly abundant in layers 4, 5a and 7 and serotonin 2A receptors in layer 13. Noradrenergic fibers were densest in layers 4 and 5a, whereas tyrosine hydroxylase positive fibers showed a slightly different distribution pattern with additional dense labeling in layer 7. As revealed by double-labeling immunohistochemistry, serotonergic fibers were closely related to the cell bodies of calbindin-positive horizontal cells in layer 5b and tyrosine hydroxylase positive fibers often contacted DARPP-32+ dendritic shafts in layers 9 and 10.These findings indicate that the catecholaminergic innervation of the optic tectum consists of a noradrenergic and a dopaminergic component and that the noradrenergic, serotonergic, and dopaminergic system may be potentially involved in the modulation of retinal input in the superficial layers of the optic tectum as well as in the modulation of tectal output via the deep tectal layers.

Nucleus isthmi, pars semilunaris as a key component of the tectofugal visual system in pigeons

The avian isthmic nuclei are constituted by a group of structures reciprocally connected with the tectum opticum and considered to play a role in the modulation of intratectal processes. Although the two larger isthmic nuclei, the n. isthmi pars parvocellularis (Ipc) and the n. isthmi pars magnocellularis (Imc), have been studied in detail previously, the third and smallest of this group, the n. isthmi pars semilunaris (SLu), has been largely neglected. The present study demonstrates this isthmic component to be characterized by a unique connectivity and immunohistochemical pattern: 1) SLu receives tectal afferents and projects back onto the outer retinorecipient tectal layers; 2) it projects bilaterally onto the nucleus rotundus and thus modulates the ascending tectofugal system; 3) in addition, previous studies have demonstrated SLu projections onto the lateral spiriform nucleus (SpL), which mediates basal ganglia output onto the tectum. In that SpL projects onto the deep layers of the tectum, SLu indirectly modulates descending tectal output patterns. Taken together, the role of SLu goes far beyond a local modulation of intratectal processes. Instead, this isthmic structure is likely to play a key role in the topographically organized modulation of the ascending and, at least indirectly, also the descending projections of the optic tectum.

Dopaminergic modulation of visual responses in toads. II. Influences of apomorphine on retinal ganglion cells and tectal cells.

The behavioral studies of Part I have shown in common toads that after systemic administration of the dopamine agonist apomorphine the prey-directed orienting turning movements are suppressed while prey snapping is facilitated. Part II focuses on retinal and tectal single cell responses to moving objects. (1) After systemic administration of apomorphine, the discharge rates of retinal class R2 and R3 ganglion cell fibres--recorded from the retino-tectal projection--speeded up in response to visual objects traversing their excitatory receptive fields. This enhancing effect was independent of the recording site in the retino-tectal map. (2) The diameters of the excitatory receptive fields of R2 and R3 neurons doubled their sizes. Probably, apomorphine enhances the center-dominated excitatory responses at the expense of the strength of the inhibitory surround. (3) The apomorphine-induced effects were fully developed 20-35 min after drug administration. (4) At the same time the discharge rates of T5.1 and T5.2 tectal neurons were reduced under apomorphine. The effect was independent of the recording site in the retino-tectal map. The diameters of the excitatory receptive fields of these tectal neurons were not influenced. (5) To changes in configurational stimulus features, the basic pattern of discrimination was maintained. (6) It is suggested that tectal output to the turn-generating motor network--mediated by T5.1 and T5.2 neurons--is modulated by a pretecto-tectal pathway which involves dopaminergic pretectal cells. (7) The enhanced snapping can be interpreted in terms of a modulation of reticular/hypoglossal structures by dopaminergic preoptic/hypothalamic/solitary systems.

Apomorphine-induced suppression of prey oriented turning in toads is correlated with activity changes in pretectum and tectum: [ 14C]2DG studies and single cell recordings

In common toads, after systemic administration of the dopamine agonist apomorphine (APO), prey-oriented turning was suppressed. Searching for neural correlates, the present study shows APO-induced increases in glucose utilization in the retinorecipient pretectum and dorsal optic tectum and a decrease in the medial tectal output layers. This pattern of metabolic activity is resembled by neuronal discharge activities recorded in response to a prey stimulus; the discharge rates are increased in retinal ganglion cells and pretectal neurons and decreased in tectal output neurons. We suggest that an APO-induced enhancement of pretecto-tectal inhibitory influences contributes to the reduction of tectal output, thus suppressing prey-oriented turning behavior.

Laminar Distribution of the Cells of Origin of Ascending and Descending Tectofugal Pathways in Turtles: Implications for the Evolution of Tectal Lamination; pp. 264–273

The major outputs of the tectum appear fundamentally similar in all vertebrate species, suggesting that the major types of tectal output neurons have been evolutionarily conserved across a wide variety of vertebrate species. Nonetheless, tectal lamination patterns vary dramatically among vertebrates. To explore the basis of this variation in lamination at a neuronal level, the laminar distribution of the cells of origin of the major ascending and descending tectofugal pathways was determined in turtles using retrograde HRP labeling and the results compared to those from similar studies in diverse other species. Four major tectal outputs were studied: 1) the ipsilateral ascending projection to nucleus rotundus of thalamus; 2) the ipsilateral ascending projection to the dorsal and ventral lateral geniculate nuclei of the thalamus; 3) the crossed descending projection to paramedian regions of the pons and medulla; and 4) the ipsilateral descending projection to cell groups of the ventrolateral pons and medulla. The projection to nucleus rotundus was found to arise exclusively from multipolar neurons of the stratum griseum centrale, while the projection to the geniculate nuclei was found to arise from radial cells with long ascending dendrites in the stratum griseum periventriculare. The crossed descending projection to the paramedian hindbrain was found to arise almost exclusively from large multipolar neurons, the majority of which were located in the stratum griseum centrale and some of which were located in the stratum griseum periventriculare. This pathway was also found to give rise to a collateral projection that ascends in the ipsilateral hypothalamus. The ipsilateral descending projection was found to arise from multipolar neurons in the stratum griseum centrale and stratum griseum periventriculare, from radial and pyramidal neurons in the stratum griseum periventriculare, and from radial neurons in stratum griseum et fibrosum superficiale. These results show that the laminar distribution of the cells of origin of tectofugal pathways in turtles does not fit the simple notion that the midbrain roof is organized into superficial layers containing neurons with ascending projections and deep layers containing neurons with descending projections. Rather, individual layers in turtles appear to give rise to both ascending and descending projections, with there being evidence that each projection arises largely from a separate set of neurons. The pattern of distribution of the cells of origin of these various pathways is different in turtles than in either birds, mammals, frogs, salamanders or teleosts. Such results suggest that considerable interspecific variation occurs in the extent to which individual homologous neuronal populations migrate superficially during tectal development.

Laminar Distribution of the Cells of Origin of Ascending and Descending Tectofugal Pathways in Turtles: Implications for the Evolution of Tectal Lamination; pp. 254–263

The major outputs of the tectum appear fundamentally similar in all vertebrate species, suggesting that the major types of tectal output neurons have been evolutionarily conserved across a wide variety of vertebrate species. Nonetheless, tectal lamination patterns vary dramatically among vertebrates. To explore the basis of this variation in lamination at a neuronal level, the laminar distribution of the cells of origin of the major ascending and descending tectofugal pathways was determined in turtles using retrograde HRP labeling and the results compared to those from similar studies in diverse other species. Four major tectal outputs were studied: 1) the ipsilateral ascending projection to nucleus rotundus of thalamus; 2) the ipsilateral ascending projection to the dorsal and ventral lateral geniculate nuclei of the thalamus; 3) the crossed descending projection to paramedian regions of the pons and medulla; and 4) the ipsilateral descending projection to cell groups of the ventrolateral pons and medulla. The projection to nucleus rotundus was found to arise exclusively from multipolar neurons of the stratum griseum centrale, while the projection to the geniculate nuclei was found to arise from radial cells with long ascending dendrites in the stratum griseum periventriculare. The crossed descending projection to the paramedian hindbrain was found to arise almost exclusively from large multipolar neurons, the majority of which were located in the stratum griseum centrale and some of which were located in the stratum griseum periventriculare. This pathway was also found to give rise to a collateral projection that ascends in the ipsilateral hypothalamus. The ipsilateral descending projection was found to arise from multipolar neurons in the stratum griseum centrale and stratum griseum periventriculare, from radial and pyramidal neurons in the stratum griseum periventriculare, and from radial neurons in stratum griseum et fibrosum superficiale. These results show that the laminar distribution of the cells of origin of tectofugal pathways in turtles does not fit the simple notion that the midbrain roof is organized into superficial layers containing neurons with ascending projections and deep layers containing neurons with descending projections. Rather, individual layers in turtles appear to give rise to both ascending and descending projections, with there being evidence that each projection arises largely from a separate set of neurons. The pattern of distribution of the cells of origin of these various pathways is different in turtles than in either birds, mammals, frogs, salamanders or teleosts. Such results suggest that considerable interspecific variation occurs in the extent to which individual homologous neuronal populations migrate superficially during tectal development.

Tracing premotor brain stem networks of orienting movements

Methods allowing a direct matching of movement-related firing patterns and connectivity of individual neurons have been used in the analysis of premotor networks controlling orienting movements. Advances have been made in the description of coding properties of orienting-related tectal output neurons, as well as in specifying their distributed connections in the brain stem and possible modes of coupling to saccadic pattern generators in the reticular formation. New data on the properties of signals and connectivity patterns have also been obtained for the tecto-recipient reticulo-spinal neurons. At least a small portion of the network performing the spatio-temporal transformations of orienting-related tectal efferent signals can now be described both in functional and in morphological terms.

Chronic effects of NMDA and APV on tectal output in Xenopus laevis

In the South African clawed-toed frog Xenopus laevis, visual experience plays a crucial role in the formation of matching binocular maps in the tectum. The ipsilateral eye's projection, relayed through the crossed isthmotectal projection, displays marked plasticity in response to altered visual input during a critical period of development. This plasticity and the events responsible for the end of the critical period are mediated by N-methyl-D-aspartate (NMDA) receptor function. We have previously reported that chronic blockade of tectal NMDA receptors with the NMDA antagonist 5-amino-phosphonovaleric acid (APV) prevents plasticity of the crossed isthmotectal projection during the critical period, while chronic treatment with NMDA restores this plasticity after the end of the critical period. These results raise the question of whether the effects on plasticity are due to changes in electrical responsiveness of the treated tissue. In this study, we have quantitatively assessed the actions of APV and NMDA on certain aspects of tectal cell activity in Xenopus during and after the critical period by recording the output of the nucleus isthmi cells that are activated by the tectum after three weeks of treatment. We have found that chronic APV treatment does not alter tectal output, as indicated by the firing of isthmotectal axons, during the critical period and that chronic NMDA treatment increases tectal output in postcritical period Xenopus. Tectal output does not differ between normal Xenopus during and after the end of the critical period.(ABSTRACT TRUNCATED AT 250 WORDS)

Morphogenesis and physiogenesis of the retino-tectal connection in the chicken. II. The retino-tectal synapses.

The preceding paper (Eager 1976) was concerned with the development of retinal ganglion cells and the maturation of photoreceptors. Here we discuss the formation of retino-tectal synapses as studied in terms of both morphology and physiology. The early response characteristics of the first and second postsynaptic tectal cells were also studied. The first retino-tectal synapses, sparse in number, were found with the electron microscope on the eleventh day of incubation. Strict criteria for their identification were employed. At the same stage postsynaptic potentials could be recorded for the first time. These potentials could be recognized as postsynaptic by the application of various techniques: combined ortho- and antidromic stimulation, variation of stimulus intensities, surface mapping, field potential profiles, and application of double shocks of varying intervals. From day twelve onward single unit recordings were also possible and confirmed these results. We were able to establish that morphological criteria for recognition of optic nerve synapses are also criteria for when they start to function. Tectal cells first respond with long-lasting repetitive discharges. Only a few days later the response burst has become shorter and is followed by post-excitatory inhibition. When retino-tectal synapses start to function the excitation is not confined to the superficial tectal cells, but reaches deeper neurons which are possibly tectal output cells. The results of this and the preceding paper (Eager 1976) indicate that the development of the retino-tectal connection in the chicken differs from that in the frog in several fundamental respects.