Dynamic Ensemble Coding of Saccades in the Monkey Superior Colliculus

2006 ◽  
Vol 95 (4) ◽  
pp. 2326-2341 ◽  
Author(s):  
H.H.L.M. Goossens ◽  
A. J. Van Opstal
Keyword(s):  
Superior Colliculus ◽  
Brain Stem ◽  
Eye Movement ◽  
Displacement Vector ◽  
Quantitative Description ◽  
Linear Feedback ◽  
Movement Trajectory ◽  
Cumulative Number ◽  
Ensemble Coding ◽  
The Brain

The deeper layers of the midbrain superior colliculus (SC) contain a topographic motor map in which a localized population of cells is recruited for each saccade, but how the brain stem decodes the dynamic SC output is unclear. Here we analyze saccade-related responses in the monkey SC to test a new dynamic ensemble-coding model, which proposes that each spike from each saccade-related SC neuron adds a fixed, site-specific contribution to the intended eye movement command. As predicted by this simple theory, we found that the cumulative number of spikes in the cell bursts is tightly related to the displacement of the eye along the ideal straight trajectory, both for normal saccades and for strongly curved, blink-perturbed saccades toward a single visual target. This dynamic relation depends systematically on the metrics of the saccade displacement vector, and can be fully predicted from a quantitative description of the cell’s classical movement field. Furthermore, we show that a linear feedback model of the brain stem, which is driven by dynamic linear vector summation of measured SC firing patterns, produces realistic two-dimensional (2D) saccade trajectories and kinematics. We conclude that the SC may act as a nonlinear, vectorial saccade generator that programs an optimal straight eye-movement trajectory.

scholarly journals What the Brain Stem Tells the Frontal Cortex. I. Oculomotor Signals Sent From Superior Colliculus to Frontal Eye Field Via Mediodorsal Thalamus

2004 ◽  
Vol 91 (3) ◽  
pp. 1381-1402 ◽  
Author(s):  
Marc A. Sommer ◽  
Robert H. Wurtz
Keyword(s):  
Superior Colliculus ◽  
Frontal Cortex ◽  
Brain Stem ◽  
Signal Transmission ◽  
Frontal Eye Field ◽  
Visual Responses ◽  
Mediodorsal Thalamus ◽  
Visual Activity ◽  
Eye Field ◽  
The Brain

Neuronal processing in cerebral cortex and signal transmission from cortex to brain stem have been studied extensively, but little is known about the numerous feedback pathways that ascend from brain stem to cortex. In this study, we characterized the signals conveyed through an ascending pathway coursing from the superior colliculus (SC) to the frontal eye field (FEF) via mediodorsal thalamus (MD). Using antidromic and orthodromic stimulation, we identified SC source neurons, MD relay neurons, and FEF recipient neurons of the pathway in Macaca mulatta. The monkeys performed oculomotor tasks, including delayed-saccade tasks, that permitted analysis of signals such as visual activity, delay activity, and presaccadic activity. We found that the SC sends all of these signals into the pathway with no output selectivity, i.e., the signals leaving the SC resembled those found generally within the SC. Visual activity arrived in FEF too late to contribute to short-latency visual responses there, and delay activity was largely filtered out in MD. Presaccadic activity, however, seemed critical because it traveled essentially unchanged from SC to FEF. Signal transmission in the pathway was fast (∼2 ms from SC to FEF) and topographically organized (SC neurons drove MD and FEF neurons having similarly eccentric visual and movement fields). Our analysis of identified neurons in one pathway from brain stem to frontal cortex thus demonstrates that multiple signals are sent from SC to FEF with presaccadic activity being prominent. We hypothesize that a major signal conveyed by the pathway is corollary discharge information about the vector of impending saccades.

scholarly journals Simulations of Saccade Curvature by Models That Place Superior Colliculus Upstream From the Local Feedback Loop

2005 ◽  
Vol 93 (4) ◽  
pp. 2354-2358 ◽  
Author(s):  
Mark M. G. Walton ◽  
David L. Sparks ◽  
Neeraj J. Gandhi
Keyword(s):  
Superior Colliculus ◽  
Brain Stem ◽  
Feedback Loop ◽  
Two Dimensional ◽  
Initial Direction ◽  
Relative Level ◽  
Level Of Activity ◽  
Local Feedback ◽  
Visual Targets ◽  
The Brain

When humans or monkeys are asked to make saccades to visual targets accompanied by one or more distractors, the two dimensional trajectory of the saccade will sometimes display significant curvature. Port and Wurtz used dual electrode recordings to show that this phenomenon is associated with activity at more than one site in superior colliculus (SC). The timing and initial direction of the curvature could be predicted by computing a weighted vector average of the normalized activity of the two neurons. As these authors noted, however, this approach does not result in correct predictions of the final direction of curved saccades. We show that the final direction of these movements can be predicted by taking into account the brain stem saccade generator and the local feedback loop. If the output of SC is computed as a weighted vector average of the saccades requested by the activated sites, and this collicular output is interpreted by downstream structures as desired displacement, existing models that place SC upstream from the local feedback loop can generate realistic saccade trajectories, including the final direction. We propose that saccade curvature is the result of a change in the relative level of activity at the two sites, which the brain stem saccade generator interprets as a change in desired displacement.

Anatomy and physiology of saccadic long-lead burst neurons recorded in the alert squirrel monkey. II. Pontine neurons

1996 ◽  
Vol 76 (1) ◽  
pp. 353-370 ◽  
Author(s):  
C. A. Scudder ◽  
A. K. Moschovakis ◽  
A. B. Karabelas ◽  
S. M. Highstein
Keyword(s):  
Superior Colliculus ◽  
Brain Stem ◽  
Reticular Formation ◽  
Reticulospinal Neurons ◽  
Burst Neurons ◽  
Nucleus Reticularis ◽  
Discharge Patterns ◽  
The Brain ◽  
Saccade Generation

1. The discharge patterns and axonal projections of saccadic long-lead burst neurons (LLBNs) with somata in the pontine reticular formation were studied in alert squirrel monkeys with the use of the method of intraaxonal recording and horseradish peroxidase injection. 2. The largest population of stained neurons were afferents to the cerebellum. They originated in the dorsomedial nucleus reticularis tegmenti pontis (NRTP) including its dorsal cell group (N = 5), the preabducens intrafascicular nucleus (N = 5), and the raphe pontis (N = 1). Axons of all neurons coursed under NRTP and entered brachium pontis without having synapsed in the brain stem. Three axons sent collaterals to the floccular lobe, but other more distant targets of these and the other cerebellar afferents could not be determined. Movement fields of these neurons were intermediate between vectorial and directional types. 3. Four neurons had their somata in nucleus reticularis pontis oralis and terminations in the brain stem reticular formation. Each neuron was different, but all terminated in the region containing excitatory burst neurons, and most terminated in the region containing inhibitory burst neurons. Other targets include nucleus reticularis pontis oralis and caudalis, NRTP, raphe interpositus, and the spinal cord. Discharge patterns included both vectorial and directional types. 4. Two reticulospinal neurons had large multipolar somata either just rostral or ventral to the abducens nucleus. These neurons also projected to the medullary reticular formation, caudal nucleus prepositus hypoglossi, and dorsal and ventral paramedian reticular nucleus. 5. The functional implications of the connections of these LLBNs and those reported in the companion paper are extensively discussed. The fact that the efferents of the superior colliculus target the regions containing medium-lead saccadic burst neurons confirms the role of the colliculus in saccade generation. However, the finding that many other neurons project to these regions and the finding that superior colliculus efferents project more heavily to areas containing reticulospinal neurons argue for a diminished role of the superior colliculus in saccade generation but an augmented role in head movement control.

Some Experiments in the Chemistry of Normal Sleep

1966 ◽  
Vol 112 (485) ◽  
pp. 391-399 ◽  
Author(s):  
Ian Oswald ◽  
G. W. Ashcroft ◽  
R. J. Berger ◽  
D. Eccleston ◽  
J. I. Evans ◽  
...  
Keyword(s):  
Mental Health ◽  
Central Nervous System ◽  
Nervous System ◽  
Brain Stem ◽  
Eye Movement ◽  
Physical And Mental Health ◽  
Reticular Activating System ◽  
Normal Sleep ◽  
Biochemical State ◽  
The Brain

Sleep is essential for physical and mental health. In the last 15 years there has grown up the concept of the brain stem reticular activating system. Electroencephalographic studies have shown two qualitatively different and alternating kinds of sleep, the orthodox (“slow wave”, or “forebrain“) and the paradoxical (”hind-brain“, “rapid eye movement”, “activated“, or “dreaming”) phases (Akert et al., 1965). It may be predicted that in the next decade attention will turn increasingly to the chemical basis of sleep. If a man is deprived of sleep for 100 hours, it is extremely difficult to keep him awake and one may suppose that an abnormal biochemical state exists within his central nervous system.

Action of the Brain Stem Saccade Generator During Horizontal Gaze Shifts. I. Discharge Patterns of Omnidirectional Pause Neurons

1999 ◽  
Vol 81 (3) ◽  
pp. 1284-1295 ◽  
Author(s):  
James O. Phillips ◽  
Leo Ling ◽  
Albert F. Fuchs
Keyword(s):  
Brain Stem ◽  
Eye Movement ◽  
Head Movement ◽  
Head Movements ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Horizontal Gaze ◽  
Discharge Patterns ◽  
The Brain

Action of the brain stem saccade generator during horizontal gaze shifts. I. Discharge patterns of omnidirectional pause neurons. Omnidirectional pause neurons (OPNs) pause for the duration of a saccade in all directions because they are part of the neural mechanism that controls saccade duration. In the natural situation, however, large saccades are accompanied by head movements to produce rapid gaze shifts. To determine whether OPNs are part of the mechanism that controls the whole gaze shift rather than the eye saccade alone, we monitored the activity of 44 OPNs that paused for rightward and leftward gaze shifts but otherwise discharged at relatively constant average rates. Pause duration was well correlated with the duration of either eye or gaze movement but poorly correlated with the duration of head movement. The time of pause onset was aligned tightly with the onset of either eye or gaze movement but only loosely aligned with the onset of head movement. These data suggest that the OPN pause does not encode the duration of head movement. Further, the end of the OPN pause was often better aligned with the end of the eye movement than with the end of the gaze movement for individual gaze shifts. For most gaze shifts, the eye component ended with an immediate counterrotation owing to the vestibuloocular reflex (VOR), and gaze ended at variable times thereafter. In those gaze shifts where eye counterrotation was delayed, the end of the pause also was delayed. Taken together, these data suggest that the end of the pause influences the onset of eye counterrotation, not the end of the gaze shift. We suggest that OPN neurons act to control only that portion of the gaze movement that is commanded by the eye burst generator. This command is expressed by driving the saccadic eye movement directly and also by suppressing VOR eye counterrotation. Because gaze end is less well correlated with pause end and often occurs well after counterrotation onset, we conclude that elements of the burst generator typically are not active till gaze end, and that gaze end is determined by another mechanism independent of the OPNs.

Cholinergic Responses in Crossed Tecto-Reticular Neurons of Rat Superior Colliculus

2008 ◽  
Vol 100 (5) ◽  
pp. 2702-2711 ◽  
Author(s):  
Thongchai Sooksawate ◽  
Kaoru Isa ◽  
Tadashi Isa
Keyword(s):  
Superior Colliculus ◽  
Brain Stem ◽  
Nicotinic Receptor ◽  
Cholinergic Innervation ◽  
Receptor Subtype ◽  
Transient Pressure ◽  
Bath Application ◽  
Reticular Neurons ◽  
Specific Antagonist ◽  
The Brain

Neurons in the intermediate gray layer (SGI) of mammalian superior colliculus (SC) receive cholinergic innervation from the brain stem parabrachial region, which seems to modulate the signal processing in the SC. To clarify its role particularly in orienting behaviors, we studied cholinergic effects on the major output neuron group of the SGI, crossed tecto-reticular neurons (cTRNs), identified by retrograde labeling from the contralateral brain stem gaze center in SC slices obtained from rats (PND 17–22) by whole cell patch-clamp techniques. Bath application of carbachol induced either 1) nicotinic inward (nIN) + muscarinic inward (mIN) (11/24) or 2) nIN + mIN + muscarinic outward (mOUT) (13/24) current responses. Transient pressure application of 1 mM acetylcholine elicited nIN in all neurons tested ( n = 58). In a majority of these neurons (52/58), the nIN was completely suppressed by dihydro-β-erythroidine, a specific antagonist for α4β2 nicotinic receptor subtype. The remaining 6/58 neurons exhibited not only the slower α4β2 receptor-mediated component but also a faster component that was inhibited by a specific antagonist for α7 nicotinic receptor, α-bungarotoxin. cTRNs expressing α7 nicotinic receptors tended to be smaller in size than those lacking α7 receptors. Bath application of muscarine induced two response patterns: mIN only (17/38) and mIN+ mOUT (21/38). The mIN and mOUT were mediated by M3 (plus M1) and M2 muscarinic receptors, respectively. These results suggest that a major response to cholinergic inputs to cTRNs is excitatory. This would indicate the facilitatory role of the brain stem cholinergic system in the execution of orienting behaviors including saccadic eye movements.

Interaction of the Frontal Eye Field and Superior Colliculus for Saccade Generation

2001 ◽  
Vol 85 (2) ◽  
pp. 804-815 ◽  
Author(s):  
Doug P. Hanes ◽  
Robert H. Wurtz
Keyword(s):  
Superior Colliculus ◽  
Brain Stem ◽  
Neural Plasticity ◽  
Recovery Of Function ◽  
Frontal Eye Field ◽  
Indirect Pathway ◽  
Compensatory Mechanisms ◽  
Eye Field ◽  
The Brain ◽  
Saccade Generation

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.

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