Dynamic feedback to the superior colliculus in a neural network model of the gaze control system

The role of the superior colliculus (SC) has been explored in the context of the gaze control system, with the conclusion that recent data place it inside the control loop calculating gaze error. A neural network proposed for the SC achieves both spatial and temporal integration of gaze signals. When placing the SC inside a gaze control loop, linear time-space transformations can be achieved even with restricted feedback on the edges of the map. The proposed gaze control model can reproduce all of the properties of previous head-fixed models. However, for the first time, a collicular mechanism is shown to provide plausible explanations for conflicting results upon electrical stimulation of rostral versus caudal sites on the colliculus, and can generate reasonable trajectories for both eye and head platforms in the head-free condition. The key assumption is the distribution of a common motor (gaze) error to the platforms contributing to the movement.     

Visual-auditory interactions in cat superior colliculus: their role in the control of gaze

Superior colliculus cells that respond to a given sensory input (visual or auditory) were influenced by the presence of a stimulus in the other modality. This is a form of sensory-sensory integration which has previously been thought to be involved in initiating the orientation of receptor organs in response to such cues. The present results demonstrate directly that some neurons in cat superior colliculus exhibit premotor discharges which are facilitated when evoked by combinations of visual and auditory stimuli. Other neurons showed sensory interactions which were more difficult to relate directly to orienting behavior; these celpls might have a role in mediating attentional functions.     

Neural cartography: sensory and motor maps in the superior colliculus

The sudden onset of a novel or behaviorally significant stimulus usually triggers responses that orient the eyes, external ears, head and/or body toward the source of the stimulus. As a consequence, the reception of additional signals originating from the source and the sensory guidance of appropriate limb and body movements are facilitated. Converging lines of evidence, derived from anatomical, electrophysiological and lesion experiments, indicate that the superior colliculus is an important part of the neural substrate responsible for the generation of orienting responses. This paper briefly reviews the functional organization of the mammalian superior colliculus and discusses possible linkages between the sensory and motor maps observed in this structure. The hypothesis is advanced that the sensory maps are organized in motor (not sensory) coordinates and that the maps of sensory space are dynamic, shifting with relative movements of the eyes, head and body.     

Impairments in visual discrimination performance and gaze shifts in monkeys with superior colliculus lesions

Eye movements of monkeys were recorded while they performed a visual discrimination task before and after superior colliculus (SC) lesions or control surgery. The monkeys with SC lesions were impaired in orienting their eyes toward the visual stimuli when they were presented eccentrically 15 degrees to 32 degrees from the center of the display screen, toward which their heads were directed. This impairment in shifting the gaze to eccentric stimuli may account for the concomitant deficit in discriminating between these eccentric stimuli. The eye movement deficit appears to depend on destruction of the deep as well as more superficial layers of the SC and may reflect a disturbance in visual-oculomotor coordination.     

Connections of the paraflocculus of the cerebellum with the superior colliculus in the rat brain

The interconnections between the paraflocculus of the cerebellum and the superior colliculus (SC) of the adult male Wistar albino rat were traced utilising the retrograde and anterograde transport of horseradish peroxidase conjugated with wheatgerm agglutinin (WGA-HRP). The study comprises three series of experiments. In the first series designed to trace the connections between the paraflocculus and the pre- and deep cerebellar nuclei, microiontophoretic injections of WGA-HRP filled either the entire paraflocculus or one of its subdivisions (ventral or dorsal paraflocculus). The results showed that, the ventral and dorsal paraflocculus receive afferents from distinct and separate regions of pontine nuclei, nucleus reticularis tegmenti pontis (Rtp) and the inferior olive. The efferents from the ventral and dorsal parafloccular subdivisions project to circumscribed regions of the lateral and posterior interpositus cerebellar nuclei. In the second series of experiments, unilateral iontophoretic WGA-HRP injections were placed at varying depths, through the rostrocaudal extent of SC and the tectal connections with the brainstem, and deep cerebellar nuclei were traced. The SC projects to well circumscribed regions of the pontine nuclei. Rtp and the inferior olive and receives afferents from the lateral and posterior interpositus cerebellar nuclei. In the third series of experiments involving combined injections of WGA-HRP into SC and the ventral paraflocculus, the collicular and ventral parafloccular connections were traced. The ventral paraflocculus receives afferents from regions of pons and Rtp which in turn receive inputs from the SC and projects to the lateral and posterior interpositus cerebellar nuclei which in turn give rise to efferents to the SC. These findings demonstrate that the ventral paraflocculus is linked to the contralateral superior colliculus via (i) a crossed afferent tecto-ponto/Rtp-parafloccular pathway, and (ii) a crossed efferent paraflocculo-nucleo-tectal pathway.     

Age-associated changes in the serotonergic system in rat superior colliculus and pretectum

The purpose of this study was to investigate whether aging alters serotonergic innervation of the superior colliculus and pretectum in rats. The superior colliculus has one of the highest concentrations of serotonin in the rat central nervous system. Young and old male F344 rats (<6 months, and >18 months, albino and pigmented) were used in all experiments. Coronal sections through the superior colliculus and pretectum were incubated with antibodies to serotonin, the serotonin 2A receptor, and the serotonin transporter. Immunocytochemical staining was analyzed semi-quantitatively. The results indicate that with age there is an increase in serotonin immunoreactivity throughout the entire superior colliculus and pretectum, a decrease in levels of serotonin 2A receptor staining in select layers of superior colliculus, and no change in serotonin transporter immunoreactivity. Albino rats differ from pigmented rats in that they have enhanced serotonergic immunoreactivity in the superficial layers of superior colliculus, a region that receives direct retinal input. These data suggest that the age-related changes in the serotonergic system in the superior colliculus and pretectum may account for some of the alterations in light-mediated behaviors with aging.     

Spatial transformations between superior colliculus visual and motor response fields during head‐unrestrained gaze shifts

We previously reported that visuomotor activity in the superior colliculus (SC) – a key midbrain structure for the generation of rapid eye movements – preferentially encodes target position relative to the eye (Te) during low‐latency head‐unrestrained gaze shifts (DeSouza et al., 2011). Here, we trained two monkeys to perform head‐unrestrained gaze shifts after a variable post‐stimulus delay (400–700 ms), to test whether temporally separated SC visual and motor responses show different spatial codes. Target positions, final gaze positions and various frames of reference (eye, head, and space) were dissociated through natural (untrained) trial‐to‐trial variations in behaviour. 3D eye and head orientations were recorded, and 2D response field data were fitted against multiple models by use of a statistical method reported previously (Keith et al., 2009). Of 60 neurons, 17 showed a visual response, 12 showed a motor response, and 31 showed both visual and motor responses. The combined visual response field population (n = 48) showed a significant preference for Te, which was also preferred in each visual subpopulation. In contrast, the motor response field population (n = 43) showed a preference for final (relative to initial) gaze position models, and the Te model was statistically eliminated in the motor‐only population. There was also a significant shift of coding from the visual to motor response within visuomotor neurons. These data confirm that SC response fields are gaze‐centred, and show a target‐to‐gaze transformation between visual and motor responses. Thus, visuomotor transformations can occur between, and even within, neurons within a single frame of reference and brain structure.     

Astroglial differentiation in the opossum superior colliculus

Glial markers, namely, vimentin, glial fibrillary acidic protein (GFAP), and glycogen, as well as accumulation of axon-borne horseradish peroxidase (HRP), were used to visualize radial glial cells in the developing opossum superior colliculus (SC) and to follow changes in young astrocytes of the superficial layers. Vimentin, GFAP, and glycogen are relatively abundant in elements of the median ventricular formation (MVF), which persists at least as late as weaning time, i.e., postconception day 103, postnatal day 90 (PND90). Radial profiles and end-feet in the remaining collicular sectors (main radial system, MRS) are also vimentin-positive but show little or no glycogen or anti-GFAP staining. The numeric density of MRS profiles is very high at the final stages of neuronal migration (PND12) but falls to vestigial numbers by PND 56-60. Antivimentin staining and filling of MRS profiles by axon-borne HRP disappear in parallel. Before total regression of MRS profiles, young astrocytes of the superficial gray layer exhibit a transiently high GFAP expression that is not found in those of the subjacent layers. The results suggest that 1) radial glia at or near the collicular midline are well equipped for a mechanical supportive role, and their abundant glycogen accumulation may reflect their eventual transformation in cells with high glycolytic metabolism, including tanycytes; 2) in most collicular sectors, some radial glia cells persist for long periods after cessation of neuronal migration and may interact with afferent fibers coursing through the superficial neuropil; 3) radially oriented astrocytes of the superficial gray layer exhibit a transiently high GFAP expression that is temporally correlated with late transformations of the retinocollicular projections.     

Projections from the superior colliculus to the trigeminal system and facial nucleus in the rat

To determine the influence of the superior colliculus (SC) in orienting behaviors, we examined SC projections to the sensory trigeminal complex, the juxtatrigeminal region, and the facial motor nucleus in rats. Anterograde tracer experiments in the SC demonstrated predominantly contralateral colliculotrigeminal projections. Microinjections in the deep layers of the lateral portion showed labeled nerve fibers and terminals in the ventromedial parts of the caudal principal nucleus and of the rostral oral subnucleus and in the medial part of the interpolar subnucleus. Some terminals were also observed in the juxtatrigeminal region and in the dorsolateral part of the facial motor nucleus contralaterally, overlying the orbicularis oculi motoneuronal region. Verification by retrograde tracer injections into the trigeminal target regions showed labeled SC neurons mostly in lateral portions of layers 4-7. When the juxtatrigeminal region was involved, a remarkable increase of labeled neurons was observed, having a patch-like arrangement with a decreasing gradient from lateral to medial SC portions. Retrograde tracer injections in the dorsolateral VII nucleus showed bilateral labeled neurons mainly in the deep lateral SC portion. Retrograde BDA microinjections into the same trigeminal or juxtatrigeminal regions, followed by gold-HRP into the dorsolateral VII nucleus, demonstrated a significant number of SC neurons in deep layers 6-7 projecting to both structures by axon collaterals. These neurons are mediolaterally grouped in patches along the rostrocaudal SC extent; a subset of them are immunoreactive for glutamic acid decarboxylase (GAD). They could be involved in the coordination of facial movements. Simultaneous anterograde and retrograde tracer injections into the lateral SC portion and the VII nucleus respectively localized trigeminofacial neurons receiving collicular input in the trigeminal principal nucleus and pars oralis. Therefore the SC should play a crucial role in regulating motor programs of both eye and eyelid movements.     

Patterns of synchronization in the superior colliculus of anesthetized cats.

Sensorimotor transformations in the mammalian superior colliculus (SC) are mediated by large sets of distributed neurons. For such distributed coding systems, stimulus superposition poses problems attributable to the merging of neural populations coding for different stimuli. Such superposition problems could be overcome by synchronization of neuronal discharges, because it allows the selection of a subset of distributed responses for further joint processing. To assess the putative role of such a temporal binding mechanism in the SC, we have applied correlation analysis to visually evoked collicular activity. We performed recordings of single-unit and multiunit activity in the SC of anesthetized and paralyzed cats with multiple electrodes. Autocorrelation analysis revealed that collicular neurons often discharged in broad (20-100 msec) bursts or with an oscillatory patterning in the alpha- and beta-frequency range. Significantly modulated cross-correlograms were observed in 50% (128 of 258) of the collicular multiunit recording pairs, and for these pairs significant correlations occurred in 44% of the stimulation epochs. For the single-unit pairs, significant interactions were observed in 14 of 48 cases studied (29%). Collicular cross-correlograms were often oscillatory, and these oscillations covered a broad frequency range of up to 100 Hz, with a predominance of oscillation frequencies in the alpha- and beta-range. In the majority of the significant correlograms (64%) the phase lag of the center peak was <5 msec. The probability of collicular synchronization increased with the overlap of the receptive fields and the proximity of the recording sites. Correlations were also observed between cells in the superficial and deep SC layers. Collicular synchronization required activation of the respective cells with a single coherent stimulus and broke down when the neurons were activated with two different stimuli. These data are consistent with the notion that collicular synchrony could define assemblies of functionally related cells.     

Functional influence of interlaminar connections in the hamster's superior colliculus.

The aim of this study was to determine the functional importance of intrinsic connections within the hamster's superior colliculus (SC) in the development of the visual responses of neurons in the deep layers of this nucleus. We used localized injections of lidocaine to block action potentials of fibers that passed through the superficial layers and injections of CoCl2 to block synaptic transmission in these layers. We also determined the morphology of a number of the deep layer cells recorded in these experiments by intracellular injection of HRP. Injection of lidocaine into the superficial layers completely abolished the visual- and/or optic chiasm-evoked responses of all 40 deep layer cells tested. Thus, fibers that either pass through or synapse in the superficial layers are necessary for the visual responses of deep layer neurons. Injections of CoCl2 restricted to the superficial layers significantly reduced the visual responsivity of 86% of 92 deep layer neurons tested and abolished the visual responses of 68% of these cells. Superficial layer injections of CoCl2 were equally effective in reducing the responses of neurons with dendrites that ascended into the superficial layers (all seven cells tested and recovered) and those of cells with dendrites restricted to the deep layers (six of seven cells tested and recovered). Injections of CoCl2 into the deep layers, in the region of the cell being recorded, significantly reduced the visual responses of 59% of 37 cells and abolished the visual responses of 40% of the neurons tested. Deep CoCl2 injections abolished the visual responses of three of four cells with dendrites restricted to the deep layers and only one of four cells with dendrites that ascended into the superficial layers. These results indicate that descending interlaminar axons from visually responsive superficial layer cells may be responsible for the visual responsivity of most neurons in the deep SC layers of hamster. Also, some deep layer neurons in this species may receive effective visual input through their dendrites that ascend into the superficial layers, where they are likely to be contacted by retinal axons or axon collaterals of superficial layer cells.     

A theoretical study of multisensory integration in the superior colliculus by a neural network model

Neurons in the superior colliculus (SC) integrate stimuli of different modalities. In this work, a mathematical model of the integrative response of SC neurons is presented, to gain a deeper insight into the possible mechanisms involved, and on individual differences in integrative abilities. The model includes two unimodal areas (auditory and visual), which communicate via feedforward and feedback synapses with a third multisensory area. Each neuron is represented via a sigmoidal relationship and a first-order dynamic. Neurons in the same area interact via lateral synapses. Simulations show that the model, with a basal parameter set, can mimic various responses described in the literature: (i) multimodal enhancement in response to two cross-modal stimuli within the receptive field, according to the inverse-effectiveness principle; (ii) within-modality suppression and cross-modality suppression by a stimulus (of the same or other modality) placed outside the receptive field. Sensitivity analysis on model parameters demonstrate that different classes of neurons observed in the literature (such as, neurons which exhibit within modality suppression without cross-modality suppression, or neurons with asymmetrical cross-modality suppression) can be reproduced by simply modifying synaptic strengths in the multimodal area. Finally, exempla of the possible role of feedback mechanisms in ambiguous conditions (such as reinforcement of a poor perception by a second cross-modal stimulus, or ventriloquism) are shown and critically discussed. The model may be of value to assess the different mechanisms responsible for multisensory integration in the SC, and, in future, to study neural plasticity in multisensory systems during development or rehabilitation.     

Visual adaptation and novelty responses in the superior colliculus

The brain's ability to ignore repeating, often redundant, information while enhancing novel information processing is paramount to survival. When stimuli are repeatedly presented, the response of visually sensitive neurons decreases in magnitude, that is, neurons adapt or habituate, although the mechanism is not yet known. We monitored the activity of visual neurons in the superior colliculus (SC) of rhesus monkeys who actively fixated while repeated visual events were presented. We dissociated adaptation from habituation as mechanisms of the response decrement by using a Bayesian model of adaptation, and by employing a paradigm including rare trials that included an oddball stimulus that was either brighter or dimmer. If the mechanism is adaptation, response recovery should be seen only for the brighter stimulus; if the mechanism is habituation, response recovery ('dishabituation') should be seen for both the brighter and dimmer stimuli. We observed a reduction in the magnitude of the initial transient response and an increase in response onset latency with stimulus repetition for all visually responsive neurons in the SC. Response decrement was successfully captured by the adaptation model, which also predicted the effects of presentation rate and rare luminance changes. However, in a subset of neurons with sustained activity in response to visual stimuli, a novelty signal akin to dishabituation was observed late in the visual response profile for both brighter and dimmer stimuli, and was not captured by the model. This suggests that SC neurons integrate both rapidly discounted information about repeating stimuli and novelty information about oddball events, to support efficient selection in a cluttered dynamic world.     

Antipsychotics and single-cell activity in the rat superior colliculus

Schizophrenic patients have problems with saccadic eye movements that can be characterized as a loss of control over the saccadic system. Preliminary clinical results suggest that antipsychotics can either disrupt or improve saccadic performance. The brain mechanism through which antipsychotics might affect saccades is the subject of study. The superior colliculus (SC) is crucially involved in the generation of saccades. Previous experimental studies showed that the substantia nigra reticulata (SNr), a structure with profound inhibitory influence on the SC, is differentially affected by classical and atypical antipsychotics. In this study, we investigated the potential effects of atypical antipsychotics (clozapine, olanzapine, and risperidone) and a classical antipsychotic (haloperidol) on the firing rate of SC cells in the rat. In anesthetized rats, we performed extracellular recordings on spontaneous active neurons in the intermediate and deep layers of the SC. After subcutaneous injection of an antipsychotic drug, changes in firing rate were compared with responses upon saline injection. Olanzapine (1.0 mg/kg), risperidone (0.3 and 1.0 mg/kg), and haloperidol (0.5 mg/kg) did not significantly alter cell activity, but clozapine (10.0 mg/kg) induced a short-lasting but significant decrease. Except for clozapine, the effects of antipsychotics on the SC were nonsignificant and therefore independent of the effects in the SNr. Our results support the notion that clozapine is different from the other atypical antipsychotics.     

Coding for auditory space in the superior colliculus of the rat

Although the rat is often used to determine behavioural sound-localization capabilities or neuronal computation of binaural information, the representation of auditory space in the rat brain has not been investigated so far. We obtained extracellular recordings from auditory neurons in the superior colliculus of anaesthetized rats and examined them for spatial tuning characteristics and topographical order. Many neurons (73%) showed significant tuning, with a single peak in the azimuth response profiles based on spike rates and response latencies. Best azimuth values from neurons in one SC were generally tuned to contralateral and rarely to frontal or ipsilateral directions. Tuning width was mostly broad; at supra-threshold sound pressure levels (35 dB SPL), 55% of the units had a tuning width of > 120 degrees in contralateral space. Additionally, tuning width increased with stimulation intensity. A significant but considerably scattered topographical order of best azimuth directions was observed in the deep layers of the superior colliculus with frontal directions being represented closer to the rostral pole. Tuned auditory units in the intermediate layers of the superior colliculus, however, showed no systematic spatial arrangement. This pattern was confirmed by analysing best azimuth directions from simultaneously recorded units. Our results indicate that the rat superior colliculus contains a representation of auditory space which is similar to that described for other small mammals.     

Sensory and motor maps in the mammalian superior colliculus

The sudden onset of a novel or behaviorally significant stimulus usually triggers responses that orient the eyes, external ears, head and/or body toward the source of the stimulus. As a consequence, the reception of additional signals originating from the source, and the sensory guidance of appropriate limb and body movements are facilitated. Converging lines of evidence, derived from anatomical, electrophysiological and lesion experiments, indicate that the superior colliculus (SC) is an important part of the neural substrate for the generation of orienting responses, involved in both the localization of sensory stimuli and the initiation of orienting responses¹.     

Global visual processing in the monkey superior colliculus

Neurons were recorded in the superficial layers of the superior colliculus in anesthetized monkeys. As classically described, cells were non-selective for target direction and speed when the target moved through an empty visual field. However, these same cells were sensitive to target direction and speed relative to a textured moving background. The target's response was suppressed when its direction and speed were similar to that of the background, irrespective of the absolute direction of background movement.