Discharge Properties of Monkey Tectoreticular Neurons

Both the frontal eye field (FEF) in the prefrontal cortex and the superior colliculus (SC) on the roof of the midbrain participate in the generation of rapid or saccadic eye movements and both have projections to the premotor circuits of the brain stem where saccades are ultimately generated. In the present experiments, we tested the contributions of the pathway from the FEF to the premotor circuitry in the brain stem that bypasses the SC. We assayed the contribution of the FEF to saccade generation by evoking saccades with direct electrical stimulation of the FEF. To test the role of the SC in conveying information to the brain stem, we inactivated the SC, thereby removing the circuit through the SC to the brain stem, and leaving only the direct FEF-brain stem pathway. If the contributions of the direct pathway were substantial, removal of the SC should have minimal effect on the FEF stimulation, whereas if the FEF stimulation were dependent on the SC, removal of the SC should alter the effect of FEF stimulation. By acutely inactivating the SC, instead of ablating it, we were able to test the efficiency of the direct FEF-brain stem pathway before substantial compensatory mechanisms could mask the effect of removing the SC. We found two striking effects of SC inactivation. In the first, we stimulated the FEF at a site that evoked saccades with vectors that were very close to those evoked at the site of the SC inactivation, and with such optimal alignment, we found that SC inactivation eliminated the saccades evoked by FEF stimulation. The second effect was evident when the FEF evoked saccades were disparate from those evoked in the SC, and in this case we observed a shift in the direction of the evoked saccade that was consistent with the SC inactivation removing a component of a vector average. Together these observations lead to the conclusion that in the nonablated monkey the direct FEF-brain stem pathway is not functionally sufficient to generate accurate saccades in the absence of the indirect pathway that courses from the FEF through the SC to the brain stem circuitry. We suggest that the recovery of function following SC ablation that has been seen in previous studies must result not from the use of an already functioning parallel pathway but from neural plasticity within the saccadic system.

The superior colliculus (SC) is a multilayered structure in the mammalian midbrain. Even though the behavioral function of the SC has been studied for well over 30 yr, it continues to be a source of surprising new findings. Traditionally it has been assumed that the primate SC selects and generates

Express saccades represent the fastest possible eye movements to visual targets with reaction times that approach minimum sensory-motor conduction delays. Previous work in monkeys has identified two specific neural signals in the superior colliculus (SC: a midbrain sensorimotor integration structure involved in gaze control) that are required to execute express saccades: 1) previsual activity consisting of a low-frequency increase in action potentials in sensory-motor neurons immediately before the arrival of a visual response; and 2) a transient visual-sensory response consisting of a high-frequency burst of action potentials in visually responsive neurons resulting from the appearance of a visual target stimulus. To better understand how these two neural signals interact to produce express saccades, we manipulated the arrival time and magnitude of visual responses in the SC by altering target luminance and we examined the corresponding influences on SC activity and express saccade generation. We recorded from saccade neurons with visual-, motor-, and previsual-related activity in the SC of monkeys performing the gap saccade task while target luminance was systematically varied between 0.001 and 42.5 cd/m(2) against a black background (∼0.0001 cd/m(2)). Our results demonstrated that 1) express saccade latencies were linked directly to the arrival time in the SC of visual responses produced by abruptly appearing visual stimuli; 2) express saccades were generated toward both dim and bright targets whenever sufficient previsual activity was present; and 3) target luminance altered the likelihood of producing an express saccade. When an express saccade was generated, visuomotor neurons increased their activity immediately before the arrival of the visual response in the SC and saccade initiation. Furthermore, the visual and motor responses of visuomotor neurons merged into a single burst of action potentials, while the visual response of visual-only neurons was unaffected. A linear combination model was used to test which SC signals best predicted the likelihood of producing an express saccade. In addition to visual response magnitude and previsual activity of saccade neurons, the model identified presaccadic activity (activity occurring during the 30-ms epoch immediately before saccade initiation) as a third important signal for predicting express saccades. We conclude that express saccades can be predicted by visual, previsual, and presaccadic signals recorded from visuomotor neurons in the intermediate layers of the SC.

Saccades are rapid movements that reposition the eye in space. Several neural structures involved in saccadic control have been characterized, providing a unique opportunity for systems-level investigations of the premotor neural circuitry. This study focuses on the role of the superior colliculus (SC) in the planning and control of saccadic eye movements in monkeys. Saccade-related neural activity in the SC is highly distributed, with saccade displacement commands coded in a topologically-organized motor map. Downstream from the SC, this spatiotemporal code is transformed into the temporal code necessary to drive the oculomotor neurons. Researchers have postulated that this transformation is implemented in the projection weights between the SC and the brainstem saccadic burst generator. Here, an empirical neural network study is used to predict the topological variation of these projection weights. Estimates of the spatiotemporal neural activity in the SC were used as the open-loop inputs to the model. The projection weights from the SC to excitatory burst neurons (EBNs) in the brainstem were trained using a biologically plausible evolutionary learning rule (the chemotaxis algorithm), while well-known features of the downstream neural structures were fixed. The objective function was defined as the squared error between the model output and actual eye position trajectories for several magnitudes of horizontal saccades (integrated over time). Simulation results predict the excitatory connections from the SC to EBNs increase in strength or density with collicular location (from rostral to caudal).KeywordsSuperior ColliculusHebbian LearningBurst NeuronHorizontal SaccadeSaccadic SystemThese keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

1. Monkeys were trained to look to brief visual targets presented in a completely darkened room. On some trials, after the visual target disappeared but before a saccade to the target could be initiated, the eyes were driven to another position in the orbit by electrical stimulation of the superior colliculus. Retinocentric models of the saccadic system predict that a saccade with a predetermined distance and direction based entirely on retinal error will occur. If this were the case, gaze would miss the target location by a distance and direction equal to the vector of the stimulation-induced movement. Spatial models assume that the retinal error signal will be combined with information about the change in eye position produced by stimulation and predict that the animal will look to the position of the target in space. 2. Results confirm the predictions of spatial models. Animals compensated for the stimulation-induced perturbation by looking to the position of the target in space. The result predicted by retinocentric models-a saccade with a direction and amplitude based on retinal error alone-was never observed. 3. The eye movement that compensated for the change in eye position produced by stimulation was a saccade, not a passive, lowvelocity movement to an orbital position of mechanical equilibrium established by a tonic pattern of motoneuron activation specified by the visual target. This indicates that a new saccade command, based on stored information about the location of the retinal image and information about the new position of the eyes, had been issued. Computation of the vector of the compensatory saccade does not necessarily increase the latency of target acquisition. The interval between the end of a stimulation-induced saccade and the beginning of the compensatory saccade was frequently 20 ms or less, permitting the animal to acquire the target with a normal latency.

Stimulus-dependent differences in cortical versus subcortical contributions to visual detection in mice

Basal Ganglia and Oculomotor Control

Chapter 8 A possible role of the superior colliculus in eye-hand coordination

PROJECTION OF THE RETINA ON SUPERIOR COLLICULUS OF CATS

Chapter 2.1 - Neural circuits for triggering saccades in the brainstem

The superior colliculus is a critical brain region involved in processing visual information. It receives visual input directly from the retina, as well as via a projection from primary visual cortex. Here we determine which cell types in the superficial superior colliculus receive visual input from primary visual cortex in mice. Neurons in the superficial layers of the superior colliculus were classified into four groups - Wide-field, narrow-field, horizontal and stellate - based on their morphological and electrophysiological properties. To determine functional connections between V1 and these four different cell types we expressed Channelrhodopsin2 in primary visual cortex and then optically stimulated these axons while recording from different neurons in the superficial superior colliculus using whole-cell patch-clamp recording in vitro. We found that all four cell types in the superficial layers of the superior colliculus received monosynaptic (direct) input from V1. Wide-field neurons were more likely than other cell types to receive primary visual cortex input. Our results provide information on the cell specificity of the primary visual cortex to superior colliculus projection, increasing our understanding of how visual information is processed in the superior colliculus at the single cell level.

To understand the neural mechanism of fixation, we investigated effects of electrical stimulation of the frontal eye field (FEF) and its vicinity on visually guided (Vsacs) and memory-guided saccades (Msacs) in trained monkeys and found that there were two types of suppression induced by the electrical stimulation: suppression of ipsilateral saccades and suppression of bilateral saccades. In this report, we characterized the properties of the suppression of bilateral Vsacs and Msacs. Stimulation of the bilateral suppression sites suppressed the initiation of both Vsacs and Msacs in all directions during and approximately 50 ms after stimulation but did not affect the vector of these saccades. The suppression was stronger for ipsiversive larger saccades and contraversive smaller saccades, and saccades with initial eye positions shifted more in the saccadic direction. The most effective stimulation timing for the suppression of ipsilateral and contralateral Vsacs was approximately 40-50 ms before saccade onset, indicating that the suppression occurred most likely in the superior colliculus and/or the paramedian pontine reticular formation. Suppression sites of bilateral saccades were located in the prearcuate gyrus facing the inferior arcuate sulcus where stimulation induced suppression at < or =40 microA but usually did not evoke any saccades at 80 microA and were different from those of ipsilateral saccades where stimulation evoked saccades at < or =50 microA. The bilateral suppression sites contained fixation neurons. The results suggest that fixation neurons in the bilateral suppression area of the FEF may play roles in maintaining fixation by suppressing saccades in all directions.

1. Experiments in anaesthetized cats have shown that the superior colliculus receives deep afferent input from the forelimb and hindlimb, but not from the large superficial neck muscles. 2. Neuronal activity in the superior colliculus is readily elicited by electrical stimulation of C2 and C3 cutaneous nerves. A significant proportion of neurones so activated have multiple receptive fields and some with no identifiable receptive fields in regions innervated by C2 and C3 nerves have receptive fields elsewhere on the body surface. Many collicular neurones activated by C2 and C3 stimulation had no identifiable receptive fields. 3. Natural stimuli to the limbs, hitherto believed to activate only cutaneous receptors, are sufficient to activate deep receptors which contribute to the neuronal responses in the superior colliculus elicited by the natural stimulus. These same natural stimuli set up transmitted vibration adequate to excite receptors some distance from the applied stimulus. 4. No evidence was found for a rigorous somatotopy in the superior colliculus. The great majority of neurones received trigeminal input which is widely distributed throughout the superior colliculus. 5. Tactile stimuli to the face are most effective in eliciting unit activity in the superior colliculus and many neurones activated by these stimuli were shown to be tectospinal neurones. In particular, the specialized receptors of the face, including the glabrous skin of the snout (the planum nasale) and the vibrissae, are major sources of input to collicular neurones including tectospinal neurones. 6. It is suggested that a major role of the superior colliculus is in the organization of head movements associated with the use of the specialized receptor organs of the face in exploratory behaviours. The superior colliculus may also be involved in the organization of aversion movements of the head.

Fast saccadic eye movements result from the recruitment of a large population of cells in the midbrain superior collicular (SC). The SC transmits its output, which represents a desired vectorial eye displacement in a topographically organized motor map, to horizontal and vertical eye velocity generators in the brainstem. It is generally agreed, that saccade generation is under continuous feedback control. An important problem for models of the saccadic system is, how the spatial representation of the SC output is transformed into the temporal code of brainstem cell population. This problem is even more intriguing, when the possibility is considered of a dynamic feedback loop which includes the SC. Recent experimental findings support such a possibility. In this paper we analyse the properties of a two-dimensional neural network model for the monkey SC, which incorporates a number of realistic features known from neurophysiology and, in addition, is part of the dynamic feedback loop for saccade generation. Our analysis suggests that the feedback should be organized topographically in order to generate goal-directed saccades. Despite the fact that the neurons in their model are linear, several nonlinear properties of saccades, such as their main-sequence characteristic, as well as saccade averaging to electrical double stimulation, can be explained on the basis of the model's architecture.

The primate superior colliculus (SC) has long been known to be involved in saccade generation. However, SC neurons also exhibit fixation-related and smooth-pursuit-related activity. A parsimonious explanation for these seemingly disparate findings is that the SC contains a map of behaviorally relevant goal locations, rather than just a motor map for saccades and fixation. This explanation predicts that SC activity should reflect the behavioral goal, even when the behavioral response is not fixation or saccades, and even if the goal does not correspond to a visual stimulus. We tested this prediction by employing a tracking task that dissociates the stimulus and goal locations. In this task, monkeys tracked the invisible midpoint between two peripheral bars, such that the visual stimuli were peripheral but the goal was foveal/parafoveal. We recorded from SC neurons representing peripheral locations associated with the stimulus or central locations associated with the goal. Most neurons with peripheral response fields did not respond differently during tracking than during passive viewing of the stimulus under fixation; most neurons with central response fields responded more during tracking than during fixation, despite the lack of a visual stimulus. Moreover, the spatial distribution of activity during tracking was larger than that during fixation or tracking of a foveal stimulus, suggesting that the greater spatial uncertainty about the invisible goal corresponded to more widespread SC activity. These results demonstrate the flexibility with which activity across the SC represents the location - and also the spatial precision - of behaviorally relevant goals for multiple eye movements.