Cortico-tectal and intertectal modulation of visual responses in the rat's superior colliculus

Summary In rats under urethane anesthesia, electrolytic destruction of one superior colliculus resulted in an increase in the amplitude of the light-evoked potential recorded in the remaining contralateral superior colliculus. In another group of rats, unilateral ablation of visual cortex produced a depression of the light-evoked potential recorded in the ipsilateral superior colliculus. However, in these same animals, subsequent destruction of the contralateral superior colliculus resulted in an increase in the amplitude of the tectal response to near normal levels. These findings suggest that the activity of the colliculus of the rat is subject to two opposing and tonic influences: 1. cortico-tectal facilitation, and 2. tectotectal inhibition.This study was supported by a grant from the National Research Council of Canada to Dr. A. Monjan. I would like to thank Dr. Monjan for his guidance and assistance in this work.     

Nociceptive responses of midbrain dopaminergic neurones are modulated by the superior colliculus in the rat

Midbrain dopaminergic neurones exhibit a short-latency phasic response to unexpected, biologically salient stimuli. In the rat, the superior colliculus is critical for relaying short-latency visual information to dopaminergic neurones. Since both collicular and dopaminergic neurones are also responsive to noxious stimuli, we examined whether the superior colliculus plays a more general role in the transmission of short-latency sensory information to the ventral midbrain. We therefore tested whether the superior colliculus is a critical relay for nociceptive input to midbrain dopaminergic neurones. Simultaneous recordings were made from collicular and dopaminergic neurones in the anesthetized rat, during the application of noxious stimuli (footshock). Most collicular neurones exhibited a short-latency, short duration excitation to footshock. The majority of dopaminergic neurones (92/110; 84%) also showed a short-latency phasic response to the stimulus. Of these, 79/92 (86%) responded with an initial inhibition and the remaining 14/92 (14%) responded with an excitation. Response latencies of dopaminergic neurones were reliably longer than those of collicular neurones. Tonic suppression of collicular activity by an intracollicular injection of the local anesthetic lidocaine reduced the latency, increased the duration but reduced the magnitude of the phasic inhibitory dopaminergic response. These changes were accompanied by a decrease in the baseline firing rate of dopaminergic neurones. Activation of the superior colliculus by the local injections of the GABA(A) antagonist bicuculline also reduced the latency of inhibitory nociceptive responses of dopaminergic neurones, which was accompanied by an increased in baseline dopaminergic firing. Aspiration of the ipsilateral superior colliculus failed to alter the nociceptive response characteristics of dopaminergic neurones although fewer nociceptive neurones were encountered after the lesions. Together these results suggest that the superior colliculus can modulate both the baseline activity of dopaminergic neurones and their phasic responses to noxious events. However, the superior colliculus is unlikely to be the primary source of nociceptive sensory input to the ventral midbrain.     

Neural correlates of the automatic and goal-driven biases in orienting spatial attention

How do stimuli in the environment interact with the goals of observers? We addressed this question by showing that the relevance of an abruptly appearing visual object (cue) changes how observers orient attention toward a subsequent object (target) and how this target is represented in the activity of neurons in the superior colliculus. Initially after the appearance of the cue, attention is driven to its locus. This capture of attention is followed by a second bias in orienting attention, where observers preferentially orient to new locations in the visual scene-an effect called inhibition of return. In the superior colliculus, these two automatic biases in orienting attention were associated with changes in neural activity linked to the appearance of the target-relatively stronger activity linked to the capture of attention and weaker activity linked to inhibition of return. This behavioral pattern changes when the cue predicts the upcoming location of the target-the benefit associated with the capture of attention is enhanced and inhibition of return is reduced. These goal-driven changes in behavior were associated with an increase in pretarget- and target-related activity. Taken together, the goals of observers modify stimulus-driven changes in neural activity with both signals represented in the salience maps of the superior colliculi.     

新生大鼠单眼摘除后双侧上丘浅灰层细胞色素氧化酶的组织化学研究

本实验用细胞色素氧化酶组织化学方法定量地研究了7只新生大鼠作单眼摘除对上丘浅灰层细胞色素氧化酶活性的影响,观察到与保留眼同侧的上丘浅灰层细胞色素氧化酶活性明显地低于对侧上丘浅灰层,说明保留眼发出的同侧视网膜顶盖投射纤维不足以维持同侧上丘浅灰层的正常氧化代谢机能     

Effects of superior colliculus lesions on rats' orienting and detection of neglected visual cues

Superior colliculus lesions generally result in a deficit in visual orienting described as sensory neglect. This observation was confirmed in this study: Rats with lesions did not orient to some stimuli that intact rats readily oriented to. However, rats with lesions did orient to stimuli that the intact rats treated as more salient. Also, when the less salient stimuli signaled aversive stimulation, the rats with lesions detected these stimuli. These findings suggest that superior colliculus lesions do not affect the detection of visual stimuli that have been neglected.     

Nociceptive neurons in rat superior colliculus: response properties, topography, and functional implications

1. Extracellular recordings were made from single superior colliculus neurons in urethane-anesthetized rats in response to mechanical and/or thermal stimulation of the skin. In addition to those activated by low-threshold (LT) tactile stimuli, many neurons responded preferentially, or solely, to noxious stimuli. Two functionally defined subtypes of nociceptive neurons were distinguished: wide-dynamic-range (WDR) neurons, which responded optimally to noxious stimuli but also to innocuous stimuli; and nociceptive-specific (NS) neurons, which responded solely to frankly noxious stimuli. The thermal thresholds were 42-45 degrees C, and the stimulus-response relationships were positively accelerating power functions with exponents of 2.9 (WDR) and 3.1 (NS). 2. WDR neurons also responded to cooling of the skin to temperatures below 24 degrees C. Like noxious heat responses, cold responses were monotonically graded as the intensity of the cold stimulus was increased. Thus the temperature sensitivity of thermal-sensitive neurons in the superior colliculus appeared to be tuned to detect large deviations from ambient skin temperature in either direction once threshold is reached. 3. LT neurons were somatotopically organized, with the head and forelimbs rostral and the trunk and hindlimbs caudal. The limbs were generally represented further lateral in the structure, whereas more proximal body parts were more medial. Nevertheless, there was extensive overlap of body parts especially in areas of transition. Thus, a "block-to-block" or "area-to-area" rather than a "point-to-point" representation of the body surface was evident. 4. The nociceptive representation did not violate the general LT somatotopy but neither was it coextensive. Virtually all nociceptive neurons had trigeminal receptive fields and were thus heavily represented in the rostral superior colliculus, where the LT face representation was also located. No nociceptive neurons were present in the caudal one-third of the structure. A general dorsal-to-ventral segregation of somatosensory neurons also was noted, so that in a given electrode penetration, LT neurons usually were the most superficial, WDR neurons were just below these, and NS neurons were deepest of all. 5. The presence of overlapping LT and nociceptive trigeminal representations in the superior colliculus seems particularly adaptive in view of the fact that rodents use their vibrissae for exploring their environment and thus put rostral body parts at risk during such behaviors.(ABSTRACT TRUNCATED AT 400 WORDS)     

Stimulus intensity modifies saccadic reaction time and visual response latency in the superior colliculus

Performance in a reaction time task can be strongly influenced by the physical properties of the stimuli used (e.g., position and intensity). The reduction in reaction time observed with higher-intensity visual stimuli has been suggested to arise from reduced processing time along the visual pathway. If this hypothesis is correct, activity should be registered in neurons sooner for higher-intensity stimuli. We evaluated this hypothesis by measuring the onset of neural activity in the intermediate layers of the superior colliculus while monkeys generated saccades to high or low-intensity visual stimuli. When stimulus intensity was high, the response onset latency was significantly reduced compared to low-intensity stimuli. As a result, the minimum time for visually triggered saccades was reduced, accounting for the shorter saccadic reaction times (SRTs) observed following high-intensity stimuli. Our results establish a link between changes in neural activity related to stimulus intensity and changes to SRTs, which supports the hypothesis that shorter SRTs with higher-intensity stimuli are due to reduced processing time.     

Cerebellar output exerts spatially organized influence on neural responses in the rat superior colliculus

The deep cerebellar nuclei project to largely segregated target regions in the contralateral superior colliculus. Single-unit recordings have previously shown that nuclear inactivation normally suppresses spontaneously active collicular target neurons. However, facilitation of activity has also been found in a proportion of collicular units. In the present study we tested the hypothesis that the type of effect is related to the cerebellotectal topography. We recorded simultaneously in the deep cerebellar nuclei and superior colliculus of 53 anaesthetized rats. GABA microinjections produced a complete, reversible, arrest of activity in the deep cerebellar nuclei. We investigated the effect of this inactivation on 292 sensory and non-sensory cells in the collicular intermediate and deep layers. Of these, 29% showed a reduced response to their preferred sensory stimulus or decreased their spontaneous firing rate in the case of non-sensory cells. However, 15% increased their sensory responsiveness and/or spontaneous firing rate following cerebellar inactivation. No effect was seen in the remaining 56% of cells. The distribution of these different effects was highly significantly related to the topography of the cerebellotectal terminal fields. Thus, 68% of the suppressive effects were obtained from cells lying in the terminal fields of the deep cerebellar nucleus inactivated. Conversely, 86% of the excitatory effects and 66% of the cells showing no effect were obtained from cells falling outside the terminal field. The results support the view that the superior colliculus is an important site for the functional integration of primary sensory information, not only with cortical and basal ganglia afferents, but also with cerebellar information. The contrasting physiological responses observed within the terminal cerebellotectal topography appear to map closely on to the known distribution of the cells of origin of the two major descending output pathways of the superior colliculus and are possibly mediated by intrinsic inhibitory connections within its intermediate and deep layers.These results provide evidence for a neural architecture in the superior colliculus whose function is the selection of appropriate actions in response to novel stimuli and the suppression of competing motor programmes.     

Early experience determines how the senses will interact

Multisensory integration refers to the process by which the brain synthesizes information from different senses to enhance sensitivity to external events. In the present experiments, animals were reared in an altered sensory environment in which visual and auditory stimuli were temporally coupled but originated from different locations. Neurons in the superior colliculus developed a seemingly anomalous form of multisensory integration in which spatially disparate visual-auditory stimuli were integrated in the same way that neurons in normally reared animals integrated visual-auditory stimuli from the same location. The data suggest that the principles governing multisensory integration are highly plastic and that there is no a priori spatial relationship between stimuli from different senses that is required for their integration. Rather, these principles appear to be established early in life based on the specific features of an animal's environment to best adapt it to deal with that environment later in life.     

Visual responses of pulvinar and collicular neurons during eye movements of awake, trained macaques.

1. We recorded from single neurons in awake, trained rhesus monkeys in a lighted environment and compared responses to stimulus movement during periods of fixation with those to motion caused by saccadic or pursuit eye movements. Neurons in the inferior pulvinar (PI), lateral pulvinar (PL), and superior colliculus were tested. 2. Cells in PI and PL respond to stimulus movement over a wide range of speeds. Some of these cells do not respond to comparable stimulus motion, or discharge only weakly, when it is generated by saccadic or pursuit eye movements. Other neurons respond equivalently to both types of motion. Cells in the superficial layers of the superior colliculus have similar properties to those in PI and PL. 3. When tested in the dark to reduce visual stimulation from the background, cells in PI and PL still do not respond to motion generated by eye movements. Some of these cells have a suppression of activity after saccadic eye movements made in total darkness. These data suggest that an extraretinal signal suppresses responses to visual stimuli during eye movements. 4. The suppression of responses to stimuli during eye movements is not an absolute effect. Images brighter than 2.0 log units above background illumination evoke responses from cells in PI and PL. The suppression appears stronger in the superior colliculus than in PI and PL. 5. These experiments demonstrate that many cells in PI and PL have a suppression of their responses to stimuli that cross their receptive fields during eye movements. These cells are probably suppressed by an extraretinal signal. Comparable effects are present in the superficial layers of the superior colliculus. These properties in PI and PL may reflect the function of the ascending tectopulvinar system.     

Tonic desynchronisation of cortical electroencephalogram by electrical and chemical stimulation of superior colliculus and surrounding structures in urethane-anaesthetised rats

Damage to the superior colliculus in rats impairs desynchronisation of the cortical electroencephalogram in response to light flashes. However, it is unclear which elements within the superior colliculus, and which efferent collicular pathways, might be involved in alerting cerebral cortex to visual stimuli. To investigate this problem, the superior colliculus and surrounding structures were stimulated either electrically (3 s trains of 0.2 ms 100 Hz cathodal pulses), or chemically (200 nl of 5 mM sodium L-glutamate), in rats anaesthetised with urethane. The cortical electroencephalogram was recorded bilaterally from frontal cortex. At each site tested with electrical stimulation the threshold current (up to 60 microA) required to produce tonic desynchronisation (outlasting stimulation-offset by at least 10 s) was determined. Comparison of the effects of electrical and chemical stimulation suggested the following: (1) stimulation of cells in the deep layers of the superior colliculus can desynchronise the cortical electroencephalogram. There may also be an additional effective area in the rostral part of the superficial layers, but this needs to be confirmed in unanaesthetised animals. (2) Stimulation of fibres in the deep white layers of caudal superior colliculus, and of cells in a wide area of caudal midbrain reticular formation, are also effective at desynchronising the cortical electroencephalogram. It is therefore possible that the ipsilateral descending pathway, that runs from the superior colliculus to terminate in the parabigeminal and cuneiform nuclei and surrounding reticular formation, is involved in mediating cortical desynchronisation initiated by the superior colliculus. Evidence from other studies indicates that some sites in this pathway may be part of a "defence arousal system". (3) Sites on the ascending pathways from the superior colliculus, to structures including dorsal thalamus, pretectum, zona incerta and rostral midbrain reticular formation, were relatively ineffective at tonically desynchronising the cortex. However, some of these pathways might mediate phasic, movement-related arousal of collicular origin.     

Age changes in electrophysiological measures of the superior colliculus and occipital cortex

Locomotor activity and electrophysiological recordings of the superior colliculus and the occipital cortex were measured for two age groups of rats (100-105 and 230-235 days old) tested in ambient light and dark sensory conditions. Age differences in response to ambient illumination were observed in both behavioral and electrophysiological data. While no age differences were found for the superior colliculus data, cortical activity of the older rats differed from that found in the younger rats. These results are interpreted in terms of potential cortical development and arousal functions.     

Auditory compensation of the effects of visual deprivation in the cat's superior colliculus

Neurones in the superior colliculus of normal and visually deprived cats were analyzed for their responses to visual, auditory and somatosensory stimuli. The percentage of auditory-responsive cells throughout all layers had increased from 11% to 42% after binocular deprivation. Some auditory responses were found even in superficial layers. The number of somatosensory responses, though not systematically tested, was also higher in the visually deprived animals. Visually responsive units did not significantly decrease in number, thus resulting in an increased proportion of multisensory neurones. The vigour of auditory responses had increased after visual deprivation, while the vigour of visual responses had decreased significantly. In addition to the auditory effects of visual deprivation found, our study confirms previous findings on the visual effects of visual deprivation in the superior colliculus. Since only qualitative changes of visual responses, but no suppression of visual by non-visual activity was found, the neuronal mechanisms responsible for these changes may be different from competition as present in the visual cortex.     

Superior colliculus lesions and environmental experience: Nonvisual effects on problem solving and locomotor activity

Bilateral lesions of the superior colliculus were produced in rats reared in either a restricted or complex environment. Problem solving ability in a Hebb-Williams closed field and activity in an open field were subsequently observed in conditions of either bright or dim illumination. Animals with superior colliculus lesions were deficient in problem solving ability and were hyperactive in the open field. Complex environment exposure during development increased problem solving ability and initial ambulation scores in all groups. Extent of pretectal damage and behavioral measures were significantly related for animals reared in the complex, but not in the restricted environment. There were no interactions with illumination level, suggesting that the deficits resulting from collicular lesions are not dependent upon the availability of visual cues.     

听源性惊厥易感性大鼠上丘神经元构筑的研究

用石蜡切片Nissl染色方法，光镜下计数、结合计算机图象分析系统观察、测量惊厥鼠与正常鼠土丘神经元的一些指标．结果显示：（1）在吻例段和中段上丘第Ⅱ层和吻侧段上丘第Ⅲ层的神经元胞体平均直径惊厥鼠显著小于正常鼠，说明惊厥鼠上丘上述部位神经元较小；（2）在吻侧段上丘第Ⅵ层，中段上丘第Ⅰ、Ⅱ层和屋倒段上丘第Ⅴ层，神经元剖面椭圆率惊厥鼠显著地小于正常鼠，说明惊厥鼠土丘上述部位神经元胞体较细长；（3）除第Ⅲ层外，土丘各板层神经元剖面面数密度惊厥鼠都大于正常鼠．本研究结果表明，惊厥鼠的土丘有神经元的形态学变化。这种变化与惊厥鼠惊厥易感性的形成之间是否存在着某种关系，有待深入研究．     

Influence of the superior colliculus on visual responses of cells in the rabbit's lateral posterior nucleus

Summary The lateral posterior-pulvinar (LP-P) complex of mammals receives a major input from the superior colliculus (SC). We have studied the response properties of LP cells and investigated the effects of reversible inactivation of the colliculus on the visual responses of LP units in anesthetized and paralyzed rabbits. Cells in LP had large receptive fields responsive to either stationary or moving stimuli. One third of the motion-sensitive cells were direction selective. The size of the receptive fields increased with eccentricity and there was a retinotopic organization along the dorso-ventral axis. Comparison of the LP and superior colliculus properties revealed substantial differences in visual response characteristics of these two structures such as the size of the receptive fields and the number of direction-selective cells. Electrical stimulation of the LP evoked antidromic action potentials in tectal cells that were motion sensitive. We found a dorsoventral gradient in the projections of collicular cells. Units located more dorsally in the colliculus sent their axons to LP while cells lying more ventrally sent axons toward the region lying posterior to LP. A micropipette filled with lidocaine hydrochloride was lowered into the superficial layers of the superior colliculus in order to reversibly inactivate a small population of collicular cells. Rendering the superior colliculus inactive produced a sharp attenuation of visual responses in the majority of LP cells. Some neurons ceased all stimulus-driven activity after collicular blockade while a few cells exhibited increased excitability following collicular inactivation. These experiments also indicate that the tecto-LP path is topographically organized. An injection in the colliculus failed to influence the thalamic response when it was not in retinotopic register with the LP cells being recorded. Our results demonstrate that the superior colliculus input to LP is mainly excitatory in nature.     

The projection from superior colliculus to cuneiform area in the rat

Summary To investigate the role of the projection from superior colliculus to the cuneiform nucleus in mediating collicular responses, the cuneiform area (including the cuneiform nucleus and immediately adjacent structures such as caudal central grey) was stimulated in rats with microinjections of glutamate (50 mM, 200 nl, 10 nmole) and the animals' head and body movements observed. The most common responses obtained from sites in the cuneiform area were freezing, darting or fast running, the form or direction of which did not appear to be strongly influenced by the laterality of the injection. These responses were only a subset of those that have been obtained in previous studies from stimulation of the superior colliculus itself: stimulation of the cuneiform area did not give contralaterally directed movements resembling orienting or approach, or ipsilaterally directed movements resembling cringing or shying. It therefore appears that the tectocuneiform projection is likely to be involved only in some of the behaviours appropriate to unexpected stimuli that are mediated by the superior colliculus, namely undirected defensive responses elicited normally by certain kinds of threatening or noxious stimulation. Involvement with such responses would be consistent with an apparent lack of topography in the tectocuneiform projection, and the connections of the cuneiform nucleus with parts of the brain concerned with nociception (see previous paper). It is unclear, however, whether the somatic responses occur in parallel with, or as a result of, autonomic changes that have also been evoked by stimulation of the cuneiform area. One striking feature of stimulating the cuneiform area with glutamate was that at many sites the intensity of the response appeared to increase with successive (one to three) injections. It is possible that this plasticity of response, which can also be obtained from the superior colliculus itself, is related to processes involved in sensitisation or learning of defensive responses.     

Projection neurons in the superficial layers of the superior colliculus in the rat: a topographic and quantitative morphometric analysis

The present study deals with qualitative and quantitative investigations in the superior colliculus of the rat. Tracer studies were correlated with Nissl staining to calculate the quantitative ratio between projection neurons and interneurons in the upper three layers of the superior colliculus. In order to reveal the projections from the superior colliculus, the first group of rats received injections of the tracer FluoroGold into the nucleus lateralis posterior thalami, the lateral geniculate body, the nucleus parabigeminalis, and the predorsal bundle. Commissural connections between the superior colliculus were traced in a second group of animals, which received Biocytin and FluoroGold injections in the upper layers of the right superior colliculus and small deposits of the carbocyanine tracer DiI in the deeper layers of the left superior colliculus. Additionally, double-labelling with FluoroGold tracing and the histochemical detection of NADPH-diaphorase activity was carried out to distinguish between projection neurons and interneurons.These experiments showed that 66% of the neurons within the superficial layers of the superior colliculus were represented by ascending projection neurons, whereas only 2-3% could be identified as descending neurons. Ascending neurons were scattered throughout the three laminae and descending neurons were localized in a cluster-like pattern. Approximately 2-3% of the neurons in the superficial layers were found to be commissural and interlayer neurons which were represented by an identical cell type, since both transcommissural and interlayer processes were originated from their somata. The somata of these commissural-interlayer neurons were all located in the mediorostral part of the superior colliculus and contained NADPH-diaphorase activity. The axon terminals of the interlayer-commissural neurons formed net-like structures which surrounded neuronal somata within the ipsilateral deep layers and within the contralateral upper layers of the superior colliculus, respectively.     

Increase by visual stimuli in turnover of 5-hydroxytryptamine in the superior colliculi of the rabbit.

1. Irregular light falshes were played on to one eye of dark adapted rabbits for periods of 20-80 min. The concentration of 5-hydroxyindol-3-ylacetic acid (5-HIAA) and of 5-hydroxytryptamine (5-HT) were estimated in left and right superior colliculi, thalami and hippocampi. 2. In rabbits exposed to such visual stimuli for 30-60 min, there was an increase in the 5-HIAA content of the colliculus contralateral to the stimulated retina which aberaged 17% (P = 0-02), but no rise was seen if the exposure was shortened to 20 or prolonged to 80 min. At no time was there a difference in 5-HIAA content between right and left thalamus or right and left hippocampus. 3. Stationary or strictly repetitive visual stimuli produced no difference between the 5-HIAA content of left and right superior colliculus. 4. No difference in 5-HT concentration between the two colliculi was found after any form of visual stimulation, nor did any changes occur in the other parts of the brain which were examined. 5. Irregular, prolonged visual stimualtion thus appears to activate tryptaminergic neurones terminating in the colliculi. The possibility is discussed that the 5-HT released at this site might act as a brake to neuronal activity under conditions when habituation to the stimuli is not yet complete.     

Projections of extraocular, neck muscle, and retinal afferents to superior colliculus in the cat: their connections to cells of origin of tectospinal tract.

Unit recordings were made in the superior colliculus of cats anesthetized with chloralose and with Pentothal. Electrical stimulation of extraocular muscle afferents and neck muscle afferents excited more units in the superior colliculus than did a variety of moving and stationary visual stimuli. Units responding to neck muscle afferent stimulation fell into three populations; one population firing with a short latency and following stimulus presentation up to 1/s, a second population with a long latency and following stimulus presentation at frequencies lower than 15/min, and a third population exhibiting paired firing. The latencies and firing patterns of the third population combined the characteristics of each of the first two patterns. It is suggested that these characteristics of unit discharges stem from the existence of two pathways from neck muscle afferents to the superior colliculus. The projection is predominantly bilateral. Units responding to neck muscle afferent stimulation are distributed throughout the superior colliculus on the basis of their latencies. Long-latency responses predominate in the superficial layers of the superior colliculus and short-latency responses, while more common in the intermediate and deep layers, predominate in the tegmentum. Extraocular muscle afferent projections to the superior colliculus constitute the single richest projection found in these experiments. While the response patterns and latencies are similar to those of the neck muscle afferents, long-latency responses are the most common and dominate in all collicular regions. Few units in the tegmentum could be excited by extraocular muscle afferents. Both extraocular muscle and neck muscle afferents show considerable convergence with one another and with retinal afferents within the superior colliculus. Cells of origin of the tectospinal tract were identified within the superior colliculus and tegmentum by antidromic excitation from the upper cervical cord. These cells were distributed predominantly within the intermediate and deep layers of the superior colliculus, and sparsely in the superficial layers and tegmentum. Almost 50% of the cells of origin of the tectospinal tract receive a convergent input from extraocular muscle and neck muscle afferents and from the retina. About 30% of the cells were inexcitable to the stimuli employed in these experiments. The significance of these projections is discussed with respect to superior collicular function in the cat and i