Units In Superior Colliculus Research Articles

Superior Colliculus: A Vision for Orienting

The superior colliculus contains neurons sensitive to motion direction. New research shows that these neurons are anatomically clustered: those representing the region of visual space 'seen' by both eyes preferentially respond to nasal motion directions and others to opposite directions.

Oscillatory Neural Synchronization Can Predict Intensity-Dependent Enhancement: A Bridge between Sensory Binding Theory and Multisensory Integration

Although conceptually similar, sensory binding theory is based on oscillatory synchronization while multisensory integration is largely grounded on multisensory neurons. Many multisensory neurons show strong enhancement of response when both senses are stimulated, but the mechanism is obscure. This is a potential bridge between binding and sensory integration because oscillatory synchronization can enhance synchronized firing rates. Consider two independent excitatory neurons, each driven by a different sensory input. For synaptic coupling with a small delay, they can synchronize at a firing rate that lies well above either of their independent activities. We use this model to simulate behavior of a pair of “Enhanced Single Modality” (ESM) neurons like those in rattlesnake optic tectum, driven by stimulation in the eyes and infrared pits (Newman & Hartline, 1981). If these units both drive a common third cell, it will behave like an “Enhanced OR” neuron: it could be driven by either infrared or visible, but will fire at a higher rate when both of its inputs are present. Although the rattlesnake binds two visual modalities, the binding model behaves like superadditive multisensory units in Superior Colliculus (Stein & Meredith, 1993) and exhibits the intensity-dependent enhancement of Meredith & Stein's (1983) Principle of Inverse Effectiveness.

Spatial and temporal visual properties of the neurons in the intermediate layers of the superior colliculus

Although the visual perception depends on the integration of spatial and temporal information, no knowledge is available concerning the responsiveness of neurons in the intermediate layers of the superior colliculus (SCi) to extended visual grating stimuli. Accordingly, we set out to investigate the responsiveness of these neurons in halothane-anesthetized cats to drifting sinewave gratings at various spatial and temporal frequencies. The SCi units responded optimally to gratings of low spatial frequencies (none of the analyzed SCi units exhibited maximal activity to spatial frequencies higher than 0.3 c/deg) and exhibited low spatial resolution and narrow spatial frequency tuning. On the other hand, the SCi neurons preferred high temporal frequencies and exhibited high temporal resolution. Thus, the SCi neurons seem to be good spatio–temporal filters of visual information in the low spatial and high temporal frequency domain. Based upon the above summarized results we suggest that the SCi units can detect large contours moving at high velocities well, but are unable to distinguish small details. This is in line with the generally held view that the SCi could possess visuomotor function, such as organizing the complex, sensory-guided oculomotor and skeletomotor responses during the self-motion of the animal.

Spectral receptive field properties of neurons in the feline superior colliculus

The spatio-temporal frequency response profiles of 73 neurons located in the superficial, retino-recipient layers of the feline superior colliculus (SC) were investigated. The majority of the SC cells responded optimally to very low spatial frequencies with a mean of 0.1 cycles/degree (c/deg). The spatial resolution was also low with a mean of 0.31 c/deg. The spatial frequency tuning functions were either low-pass or band-pass with a mean spatial frequency bandwidth of 1.84 octaves. The cells responded optimally to a range of temporal frequencies between 0.74 cycles/s (c/s) and 26.41 c/s with a mean of 6.84 c/s. The majority (68%) of the SC cells showed band-pass temporal frequency tuning with a mean temporal frequency bandwidth of 2.4 octaves, while smaller proportions of the SC units displayed high-pass (19%), low-pass (8%) or broad-band (5%) temporal tuning. Most of the SC units exhibited simple spectral tuning with a single maximum in the spatio-temporal frequency domain, while some neurons were tuned for spatial or temporal frequencies or speed tuned. Further, we found cells excited by gratings moving at high temporal and low spatial frequencies and cells whose activity was suppressed by high velocity movement. The spatio-temporal filter properties of the SC neurons show close similarities to those of their retinal Y and W inputs as well as those of their inputs from the cortical visual motion detector areas, suggesting their common role in motion analysis and related behavioral actions.

Somatosensory-Motor Neuronal Activity in the Superior Colliculus of the Primate

The superior colliculus (SC) in primates plays an important role in orienting gaze and arms toward novel stimuli. Here we ask whether neurons in the intermediate and deep layers of the SC are also involved in the interaction with objects. In two trained monkeys we found a large number of SC units that were specifically activated when the monkeys contacted and pushed a target that had been reached with either hand. These neurons, however, were silent when the monkeys simply looked at or reached for the target but did not touch it. The activity related to interacting with objects was spatially tuned and increased with push strength. Neurons in the SC with this type of activity may be involved in a somatosensory-motor feedback loop that monitors the force of the active muscles together with the spatial position of the limb required for proper interaction with an object.

Visual Field Loss in RCS Rats and the Effect of RPE Cell Transplantation

The consequences of progressive retinal degeneration on central visual function were studied by recording single and multiunit receptive fields (RFs) across the surface of the superior colliculus (SC) of pigmented dystrophic RCS rats. Retinal morphology was used to provide a correlation between function and histological appearance. In addition, the potential protective effect of retinal pigment epithelium (RPE) transplantation was studied in a similar manner in dystrophic animals in which RPE cells were injected into the subretinal space, or the vitreous humor, at between 21 and 28 days of age. The visual responsiveness of SC units in dystrophic rats differed markedly from those in nondystrophics. Dystrophic rats developed a relative scotoma beginning in the central visual field by 42–45 days of age and expanding to include 50% of the visual field by 97–107 days. In contrast, following subretinal RPE transplantation, there was photoreceptor rescue correlated with a partial to complete preservation of RF representation when examined at 85 to 108 days of age. The majority of photoreceptor rescue occurred in the region of graft placement with possible low level rescue across the central retina. Dystrophic animals that had received intravitreal RPE transplants showed poor photoreceptor survival as well as minimal functional preservation. Our results indicate that there is a progressive central to peripheral loss of visual responsiveness in the SC of dystrophic RCS rats which can be limited by subretinal injections of healthy RPE cells.

Alterations in visual receptive fields in the superior colliculus induced by amphetamine

Visual response properties were examined in the superficial layers of the superior colliculus (SC) of anesthetized, paralyzed cats before and after i.v. administration of d-amphetamine. Receptive fields (RFs) of single SC units were plotted using small spots of light presented to the contralateral eye. Within the first hour following d-amphetamine injections, RF size gradually increased, reaching a maximum 86 min post-injection. On average, the area of the RF increased by 5.6 times and RF expansion was observed in all single units examined in the superficial layers. Over the subsequent 4-8 h following the injection, RF area gradually decreased and returned to control dimensions. Most RFs displayed asymmetrical patterns of expansion, showing relatively more horizontal than vertical growth. As RF expansion developed, responses to stimuli flashed "on" and "off" at various locations both inside and outside the borders of the control RF became progressively more vigorous. In contrast, no significant changes were noted in direction-selective responses at any time after d-amphetamine injections. Using an array of light bar stimuli of different lengths, the strength of surround suppression was found to be significantly diminished by d-amphetamine. The reduction in surround suppression was especially clear for bar lengths which exceeded the diameter of the control RF. No RF expansion was observed in the superficial layers of the SC when d-amphetamine was injected intravitreally. Furthermore, d-amphetamine had no discernable effect on the RF sizes of cells in the visual cortex. These results suggest that the RF changes in the SC were not of either retinal or cortical origin. We conclude that the mean retinal area which can potentially influence the activity of RFs in the superficial layers of the SC may be on average over 5 times greater than the RF area determined using conventional methods and criteria. These findings raise the interesting possibility that the relatively small size and sharp borders characteristic of RFs in the superficial layers arise from local inhibitory networks which delimit a broader field of excitatory activity supplied by retinal and cortical afferent terminals. Thus, in order to generate the RF changes observed here, either these local inhibitory circuits are amphetamine sensitive, or more likely, these inhibitory networks are dynamically modulated by an, as yet unidentified, amphetamine-sensitive input affecting visual RFs in the superficial layers.

Visual thresholds in albino and pigmented rats.

Albino rats have recently been reported to have increment thresholds against dim backgrounds that are two log units higher than those of pigmented rats. We, on the other hand, have failed to confirm these differences using electroretinogram b-waves and pupillary light reflexes. This paper reports on experiments using evoked potentials from cortex and colliculus and single-unit recordings from colliculus. We recorded visual-evoked potentials from cortex and superior colliculus in the strains of albino (CD) and pigmented (Long-Evans) rats used in the earlier studies. Thresholds were determined on eight fully dark-adapted animals by extrapolating intensity-response curves to the point at which there was zero evoked potential. The average dark-adapted threshold for the visual-evoked cortical potential was -5.6 log cd/m2 in pigmented and -5.80 log cd/m2 in albino animals. The average dark-adapted threshold for the superior colliculus evoked response was -5.54 log cd/m2 in pigmented and -5.84 log cd/m2 in albinos. The differences were not statistically significant. On the same apparatus, the average absolute threshold for three human observers was -5.3 log cd/m2, a value close to the rat dark-adapted thresholds. Thus, visual-evoked cortical potentials and superior collicular evoked potentials failed to confirm the report of higher dark-adapted thresholds for albinos. In addition, we find that single units in superior colliculus in the albino rat respond to very dim flashes.

Changes in external ear position modify the spatial tuning of auditory units in the cat's superior colliculus.

This study examines the influence of external ear position on the auditory spatial tuning of single units in the superior colliculus of the anesthetized cat. Unit responses to broad-band stimuli presented in a free sound field were measured with the external ears in a forward symmetrical position or with one or the other ear turned 40 degrees to the side; the ears are referred to as contra- or ipsilateral with respect to the side of the recording site. Changes in the position of either ear modified the spatial tuning of units. The region of space from which a stimulus was most effective in activating a unit is referred to as the unit's "best area". Whenever the contralateral ear was turned to the side, best areas shifted peripherally and somewhat upward, roughly in proportion to the magnitude of the change in ear position. A turn of the ipsilateral ear to the side had more variable effects, but best areas generally shifted frontally. Best areas located between approximately 10 and 40 degrees contralateral when the ears were forward were least affected by changes in ipsilateral ear position. Changes in ear position also modified the maximum response rates of many units. Units with best areas located within approximately 20 degrees of the frontal midline when the ears were forward exhibited a pronounced decrease in responsiveness when either ear was turned. Units with more peripheral best areas tended to show no change or a slight increase in responsiveness. The influence of ear position on the directionality of the external ears was determined by mapping the cochlear microphonic response to tones or one-third-octave bands of noise before and after turning the ear. When the ears were forward, maximum interaural intensity differences (IIDs) were produced by high-frequency sound sources (greater than or equal to 20 kHz) located 20-40 degrees from the frontal midline and by lower frequency sources located further peripherally. The influence of ear position on the locations from which maximum IIDs were produced was similar to the influence of ear position on unit best areas. Changes in ipsilateral ear position had different effects on high- and low-frequency IIDs that were comparable with the effects of changes in ear position on frontally and peripherally located best areas, respectively.(ABSTRACT TRUNCATED AT 400 WORDS)

Auditory response properties and spatial response areas of superior collicular neurons of the FM bat,Eptesicus fuscus

1. Electrophysiological properties of 279 single units in the superior colliculus (SC) of the big brown bat,Eptesicus fuscus, were studied by recording their responses to pure tone pulses and frequency-modulated stimuli. 2. The SC units generally fired only a few impulses to acoustic stimulus. They are not tonotopically organized along the dorsoventral axis of the SC (Fig. 1). 3. The response latency of 276 units was between 3.6 and 20 ms, but most (253 units) were below 12.5 ms (Fig. 2). 4. Tuning curves of 164 units are either narrow, intermediate, or broad, according to the bandwidth of the tuning curves (Fig. 3). Q10 dB values range between 1.21 (best frequency (BF) =33.52 kHz) and 68.9 (BF=69.94 kHz), but the majority are below 20. The minimum thresholds (MTs) of these units were between 15 and 104 dB SPL, but most were above 40 dB SPL. 5. MTs to pure tone pulses and one octave upward and downward sweeping FM stimuli were compared (Fig. 4). SC units generally had their lowest MTs to downward sweeping FM stimuli and their highest MTs to pure tone pulses (Table 1). 6. Intensity-rate functions of 16 SC units were measured with both pure tone pulses and upward and downward sweeping FM stimuli. There was no correlation between the type of intensity-rate function obtained and the type of acoustic stimulus used (Fig. 5). 7. Auditory spatial response areas were measured for 47 units. The size of the spatial response area increases with stimulus intensity (Fig. 6). The auditory space is not orderly represented in the SC of a bat (Fig. 7).

Directional sensitivity of auditory neurons in the superior colliculus of the bat,Eptesicus fuscus, using free field sound stimulation

Electrophysiological recordings were made from 130 single neurons of the superior colliculus (SC) of big brown bats,Eptesicus fuscus, in order to test their general as well as directional auditory response properties. Bursts of constant frequency and frequency modulated signals were broadcasted through a condenser loudspeaker, which could be placed at any azimuth and elevation on a hemisphere in front of the bat's head. The SC units responded equally well to both types of signals. The best frequencies of SC neurons ranged from 25 up to 82 kHz, and their tuning curves appeared to be broad (compared to those of the main auditory nuclei of the same and other bats) with Q10dB values of 1.8–17.5. All units encountered revealed directional sensitivity and were classified in two groups: the majority of them had a constant best angle of response (BA) whatever the sound intensity was (unidirectional type); the others showed a shift in their BA towards the center of the stimulating hemisphere as the intensity decreased (pluridirectional type). In both response types, the BA results are corroborated by the properties of the receptive fields. The presence of an auditory ‘space map’ in the horizontal plane is not obvious for the superior colliculus of this bat.

Functional influences of the visuocortical projection on superior colliculus neurons in the rabbit

The effects of electrical stimulation of the visual cortex on superior colliculus neurons were investigated in adult Dutch-belted rabbits. Single units were recorded in the superior colliculus and classified as to receptive field type. Stimulation of the ipsilateral visual cortex activated 29% of the recorded superior colliculus units. No units were driven by stimulation of the contralateral visual cortex. Comparison of the relative proportional distributions of cortically driven and not driven cells having various receptive field types revealed an over-representation of driven motion type cells. The excitatory influence of the visuocortical projection to the superior colliculus in the rabbit shows a preference for neurons responsive to moving visual stimuli.

Effects of visual cortical lesions on receptive-field properties of single units in superior colliculus of the rabbit.

1. One hundred seventy-nine single units were studied in the superior colliculus of seven Dutch-belted rabbits following ablation of the ipsilateral visual cortex. The response characteristics of these units were compared with those of 284 single units recorded from the superior colliculus of 20 intact animals. 2. In both the upper and lower parts of the stratum griseum superficiale and in the stratum griseum intermediate, there were smaller proportions of direction-selective visual units in the decorticated animals than in normal ones. 3. In the upper stratum griseum superficiale, a larger proportion of units responded to stroboscopic illumination in the decorticated animals than in normal ones. Also, in the decorticated animals, there was a larger proportion of units whose responses to a small moving stimulus were inhibited by the simultaneous presentation of stroboscopic illumination. 4. In both the upper and lower parts of the stratum griseum superficiale, a larger proportion of visual units responded well to stationary stimuli and a smaller proportion of visual units showed habituation in decorticated animals compared to normal ones. 5. In the lower stratum griseum superficiale, the receptive fields of units were larger and were more elongated in the anterior-posterior dimension in the decorticated animals than in normal ones. 6. In the two preparations, units did not differ in responsiveness or spontaneous activity; and visual units did not differ in the sustained or transient nature of their responses, the selectivity for light or dark stimuli, the selectivity for onset or offset of the stimuli, or the selectivity for stimulus velocity. 7. This study provides evidence for the importance of the visual corticotectal projection in the elaboration of the visual receptive-field properties of units in the superior colliculus of the rabbit. In addition, this study shows that the subdivisions of the superior colliculus are differentially affected by the loss of the visual corticotectal projection.

Evidence for a GABAergic inhibitory nigrotectal pathway in the rat

The aim of the present study was to test the GABAergic nature of the inhibitory projection from substantia nigra, pars reticulata (SNr) to superior colliculus (SC) in the rat, through the use of extracellular recordings and microiontophoresis. The effect of SN stimulation on the spontaneous or glutamate-evoked firing of SC units was analyzed. Among 28 SC cells inhibited by SNr stimulation, 27 decreased their firing rate following iontophoretic application of either GABA or glycine. The effect of the iontophoretic administration of bicuculline on SNr-evoked inhibition was studied on 14 of these GABA- and glycine-sensitive neurons. Bicuculline reversibly blocked nigral inhibition on 12 neurons, with iontophoretic current which did not affect glycine depression. These results are consistent with the hypothesis that GABA is the inhibitory transmitter of the nigrotectal projection.

Response properties of superior colliculus units: effects of extra-receptive field stimuli

Response properties of superior colliculus units: effects of extra-receptive field stimuli

Discharge characteristics of single units in superior colliculus of the alert rhesus monkey.

ACCUMULATING EVIDENCE suggests that the superior colliculus plays an important role in orientation and eye movement. Ablation studies have shown that destruction of superior colliculi interferes with spatial orientation and eye movement (Z-29), although the evidence regarding the effects of such lesions in primates is conflicting (1, 7, 17, 18; and unpublished observations). Stimulation studies have disclosed that electrical or chemical stimulation of the superior colliculus elicits eye and head movement in several species (4, 1 I, 20, 22). While most single-unit studies centered on the visual information-processing role of the mammalian superior colliculi (12-16, 30, 32, 33; M. Cynader and N. Berman, unpublished observations), a few studies have recently appeared that demonstrate eye-movement related unit activity (22, 31, 35) The aim of the present study was to investigate the discharge characteristics of single units in the superior colliculus of the alert, unanesthe tized monkey. We wished to assess both the visual receptivefield characteristics of units and the possible relation of unit discharges to eye movement. To carry out this plan one eye of each monkey was immobilized prior to the experiment by transection of the 3rd, 4th, and 6th cranial nerves. This made it possible to study in the monkey, whose head was restrained, receptive fields of units of the immobilized eye, and to relate the discharge characteristics of collicular units to the movement of the normal eye during both saccadic and smooth pursuit eye movements. M. Cynader and N. Berman (unpublished data) recently have shown that nearly all units in the monkey

Electrical responses of cat superior colliculus in reticular formation activation and during natural sleep-wakefulness cycle.

Electrical responses of the superior colliculus (SC), elicited by single shock stimulation of the optic tract (CT), were studied in unanesthetized immobilized cats and in one chronic preparation. 1) When recorded from deep points of the SC, the electrical response con-sisted of an initial spike complex and a following positive-negative biphasic wave. Among these, the earliest spike with a latency of 0.6 msec was identified as representing a presynaptic volley. The onset latency of the positive wave was 3-6 msec. 2) In response to a single OT shock, units of the SC discharged singly or repetitively. The latency histogram of the unitary responses had two peaks, one at 2-3 msec and the other at 8-9 msec. The configuration of the latency histo-gram was about the same as the positive wave response. 3) Conditioning stimulation of the mesencephalic reticular formation (MRF) enhanced the positive wave response. This effect was maximum at 150 msec and lasted up to 500 msec after the MRF activation. With about the same time course as this, the reactivity of the SC units was increased. 4) The antidromic response of the OT was enhanced following the MRF activation, the maximum being reached at 40 msec. In association with this a slow negative potential change was found to occur at the optic chiasm. Its time course was similar to the facilitation curve of the antidromic CT response. 5) It was seen in one chronic preparation that the SC response was augmented during deep sleep as compared with those during light sleep and resting arousal.