Activity Of Superior Colliculus Neurons Research Articles

Macaque frontal eye field input to saccade-related neurons in the superior colliculus.

Extracellular recordings were made simultaneously in the frontal eye field and superior colliculus in awake, behaving rhesus monkeys. Frontal eye field microstimulation was used to orthodromically activate the superior colliculus both to locate the depth of the strongest frontal eye field input to the superior colliculus and to identify superior colliculus neurons receiving direct frontal eye field input. The activity of orthodromically driven colliculus neurons was characterized during visuomotor tasks. The purpose of this study was to identify the types of superior colliculus neurons that receive excitatory frontal eye field input. We found that microstimulation of the frontal eye field did not activate the superficial layers of the superior colliculus but did activate the deeper layers. This pattern of activation coincided with the prevalence of visual versus saccade-related activity in the superficial and deep layers. A total of 83 orthodromically driven superior colliculus neurons were identified. Of these neurons, 93% (n = 77) exhibited a burst of activity associated with the onset of the saccade, and 25% (n = 21) exhibited prelude/build-up activity prior to the onset of a saccade. In addition, it was common to see some activity synchronized with the onset of a visual target (30%, n = 25). In single neurons, these activity profiles could be observed alone or in combination. Superior colliculus neurons that were exclusively visual, however, were not excited by frontal eye field stimulation. We compared the activity of superior colliculus neurons that received frontal eye field input to descriptions of saccade-related neurons made in earlier reports and found that the distribution of neuron types in the orthodromically driven population was similar to the distribution within the overall population. This suggests that the frontal eye field does not selectively influence a specific class of collicular neurons, but, instead has a direct influence on all preparatory, and saccade-related activity within the deep layers of the superior colliculus.

Competition between saccade goals in the superior colliculus produces saccade curvature.

When saccadic eye movements are made in a search task that requires selecting a target from distractors, the movements show greater curvature in their trajectories than similar saccades made to single stimuli. To test the hypothesis that this increase in curvature arises from competitive interactions between saccade goals occurring near the time of movement onset, we performed single-unit recording and microstimulation experiments in the superior colliculus (SC). We found that saccades that ended near the target but curved toward a distractor were accompanied by increased presaccadic activity of SC neurons coding the distractor site. This increased activity occurred approximately 30 ms before saccade onset and was abruptly quenched on saccade initiation. The magnitude of increased activity at the distractor site was correlated with the amount of curvature toward the distractor. In contrast, neurons coding the target location did not show any significant difference in discharge for curved versus straight saccades. To determine whether this pattern of SC discharge is causally related to saccade curvature, we performed a second series of experiments using electrical microstimulation. Monkeys made saccades to single visual stimuli presented without distractors, and we stimulated sites in the SC that would have corresponded to distractor sites in the search task. The stimulation was subthreshold for evoking saccades, but when its temporal structure mimicked the activity recorded for curved saccades in search, the subsequent saccades to the visual target showed curvature toward the location coded by the stimulation site. The effect was larger for higher stimulation frequencies and when the stimulation site was in the same colliculus as the representation of the visual target. These results support the hypothesis that the increased saccade curvature observed in search arises from rivalry between target and distractor goals and are consistent with the idea that the SC is involved in the competitive neural interactions underlying saccade target selection.

Superior colliculus firing changes after lesion or electrical stimulation of the subthalamic nucleus in the rat

Recent data have suggested a critical role for the basal ganglia in the remote control of epileptic seizures. In particular, it has been shown that inhibition of either substantia nigra pars reticulata or subthalamic nucleus as well as activation of the superior colliculus suppresses generalized seizures in several animal models. It was previously shown that high frequency stimulation of the subthalamic nucleus, thought to act as functional inhibition, stopped ongoing non-convulsive generalized seizures in rats. In order to determine whether high frequency stimulation of the subthalamic nucleus involved an activation of superior colliculus neurons, we examined the effects of subthalamic nucleus manipulation, by either high frequency stimulation or chemical lesion, on the spontaneous electrical activity of superior colliculus neurons. Acute high frequency stimulation of the subthalamic nucleus (frequency 130 Hz) induced an immediate increase of unitary activity in 70% of responding cells, mainly located within the deep layers, whereas a reduction was observed in the remaining 30%. The latter responses are dependent on the intensity and frequency of the stimulation. Unilateral excitotoxic lesion of the subthalamic nucleus induced a delayed and transient decrease of superior colliculus activity. Our data suggest that high frequency stimulation of the subthalamic nucleus suppresses generalised epileptic seizures through superior colliculus activation.

Expression of a re-centering bias in saccade regulation by superior colliculus neurons.

In previous studies of saccadic eye movement reaction time, the manipulation of initial eye position revealed a behavioral bias that facilitates the initiation of movements towards the central orbital position. An interesting hypothesis for this re-centering bias suggests that it reflects a visuo-motor optimizing strategy, rather than peripheral muscular constraints. Given that the range of positions that the eyes can take in the orbits delimits the extent of visual exploration by head-fixed subjects, keeping the eyes centered in the orbits may indeed permit flexible orienting responses to engaging stimuli. To investigate the influence of initial eye position on central processes such as saccade selection and initiation, we examined the activity of saccade-related neurons in the primate superior colliculus (SC). Using a simple reaction time paradigm wherein an initially fixated visual stimulus varying in position was extinguished 200 ms before the presentation of a saccadic target, we studied the relationship between initial eye position and neuronal activation in advance of saccade initiation. We found that the magnitude of the early activity of SC neurons, especially during the immediate pre-target period that followed the fixation stimulus disappearance, was correlated with changes in initial eye position. For the great majority of neurons, the pre-target activity increased with changes in initial eye position in the direction opposite to their movement fields, and it was also strongly correlated with the concomitant reduction in reaction time of centripetal saccades directed within their movement fields. Taking into account the correlation with saccadic reaction time, the relationship between neuronal activity and initial eye position remained significant. These results suggest that eye-position-dependent changes in the excitability of SC neurons could represent the neural substrate underlying a re-centering bias in saccade regulation. More generally, the low frequency SC pre-target activity could use eccentric eye position signals to regulate both when and which saccades are produced by promoting the emergence of a high frequency burst of activity that can act as a saccadic command. However, only saccades initiated within approximately 200 ms of target presentation were associated with SC pre-target activity. This eye-dependent pre-target activation mechanism therefore appears to be restricted to the initiation of saccades with relatively short reaction times, which specifically require the integrity of the SC.

Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus.

The frontal eye field (FEF) and superior colliculus (SC) contribute to saccadic eye movement generation, and much of the FEF's oculomotor influence may be mediated through the SC. The present study examined the composition and topographic organization of signals flowing from FEF to SC by recording from FEF neurons that were antidromically activated from rostral or caudal SC. The first and most general result was that, in a sample of 88 corticotectal neurons, the types of signals relayed from FEF to SC were highly diverse, reflecting the general population of signals within FEF rather than any specific subset of signals. Second, many neurons projecting from FEF to SC carried signals thought to reflect cognitive operations, namely tonic discharges during the delay period of a delayed-saccade task (delay signals), elevated discharges during the gap period of a gap task (gap increase signals), or both. Third, FEF neurons discharging during fixation were found to project to the SC, although they did not project preferentially to rostral SC, where similar fixation neurons are found. Neurons that did project preferentially to the rostral SC were those with foveal visual responses and those pausing during the gap period of the gap task. Many of the latter neurons also had foveal visual responses, presaccadic pauses in activity, and postsaccadic increases in activity. These two types of rostral-projecting neurons therefore may contribute to the activity of rostral SC fixation neurons. Fourth, conduction velocity was used as an indicator of cell size to correct for sampling bias. The outcome of this correction procedure suggested that among the most prevalent neurons in the FEF corticotectal population are those carrying putative cognitive-related signals, i.e., delay and gap increase signals, and among the least prevalent are those carrying presaccadic burst discharges but lacking peripheral visual responses. Fifth, corticotectal neurons carrying various signals were biased topographically across the FEF. Neurons with peripheral visual responses but lacking presaccadic burst discharges were biased laterally, neurons with presaccadic burst discharges but lacking peripheral visual responses were biased medially, and neurons carrying delay or gap increase signals were biased dorsally. Finally, corticotectal neurons were distributed within the FEF as a function of their visual or movement field eccentricity and projected to the SC such that eccentricity maps in both structures were closely aligned. We conclude that the FEF most likely influences the activity of SC neurons continuously from the start of fixation, through visual analysis and cognitive manipulations, until a saccade is generated and fixation begins anew. Furthermore, the projection from FEF to SC is highly topographically organized in terms of function at both its source and its termination.

T Immediate Neural Plasticity Shapes Motor Performance

The consolidation of motor skills necessitates long-lasting changes in the nervous system. For the most part, plasticity has been documented in motor systems after training and long-term adaptation. However, there has been no demonstration of immediate neural changes associated with the rapid adaptation of motor behavior required to interact with a dynamic environment. To address this issue, we explored the changes in performance (reaction time) of rhesus monkeys that executed saccadic eye movements to one of two visual stimuli while monitoring the preparatory activity of neurons in the superior colliculus, a structure close to the motor output. Similar to the well established sequential effects observed in human manual responses, each monkey displayed reaction times to target locations that were organized in a sequential pattern, becoming progressively shorter with each preceding repeated movement and longer with each preceding nonrepeated movement. This sequential pattern of performance modification was associated with concordant changes in the preparatory activity of superior colliculus neurons in advance of the saccadic target presentation. These data indicate that neural properties are continuously shaped by use-related experience in a manner consistent with the progressive adaptation of motor behavior.

Chapter 4 Serotonin modulates retinotectal and corticotectal convergence in the superior colliculus

A dense serotonin (5-HT)-containing projection to the superficial layers of the superior colliculus (SC) has been demonstrated in diverse mammalian species, but how 5-HT may affect visual signals within these laminae is largely unknown. This study undertook to investigate the distribution of 2 types of 5-HT receptors in the SC and to ascertain their physiological effects on transmission of visual signals to the SC from the retinotectal and corticotectual pathways. Autoradiography of tissue sections exposed to [3H]-8-OH-DPAT (8-hydroxy-dipropylaminotetraline) or to [125I]cyanopindolol plus isoproterenol showed that 5-HT1A and 5-HT1B receptors, respectively, were present in the superficial SC layers. In unilaterally enucleated animals, binding of ligand to 5-HT1B receptors was greatly reduced on the deafferented (contralateral) side, which is consistent with the possibility that these receptors are located on preterminal axons. Binding to 5-HT1A receptors was unaltered by enucleation. In recordings of superficial layer neurons from SC slices, application of 5-HT during blockade of 5-HT1A receptors with spiperone reduced the amplitude of EPSPs evoked by stimulation of the optic tract. The 5-HT concentration for a 50% reduction in EPSP amplitude was 6 microM. Under these conditions, there were no significant alterations in either membrane potential or input resistance concurrent with 5-HT mediated reduction in EPSPs. During extracellular in vivo recordings, 5-HT, applied by iontophoresis or micropressure or by endogenous release produced by electrical stimulation of the dorsal raphé nucleus, strongly suppressed visual activity in SC neurons. The effectiveness of 5-HT application was significantly stronger on responses evoked by electrical stimulation of the optic chiasm (an average response decrement of 92.2%) than on these evoked in the same neurons by stimulation of visual cortex (an average response reduction of 32.3%). These results support the following conclusions. The 5-HT1B receptors are located preferentially on optic axon terminals and exert presynaptic inhibition of retinotectal inputs. Secondly, 5-HT1A receptors probably have a postsynaptic localization and may affect activity of SC neurons irrespective of the source of input. The combined effect of 5-HT at both subtypes would bias SC visual activity toward information received from the corticotectal pathway.

Long-term changes in the activity of superior colliculus neurons isolated from corticofugal influences.

In acute experiments on nonnarcotized, immobilized cats, spike activity was studied in superior collicular neurons which were isolated from direct, descending cortical influences. Animals were taken for experimentation at various periods (from 3 to 20 months) after the operation which disconnected the cortical connections which projected from one hemisphere. An increase was noted in the regular forms of activity, and there was a decrease in the frequency of group discharges. Evoked activity of the cells was suppressed during the early periods after disconnection of corticocollicular connections. Later (after 9--12 months) its gradual restoration was observed. More than 70% of the neurons again began to respond to adequate stimuli. The sensitivity to moving photic stimuli was restored in only 17% of the neurons studied.