Evidence for Gaze Feedback to the Cat-Superior Colliculus: Discharges Reflect Gaze Trajectory Perturbations

Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada, H3A2B4.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 04/2004; 24(11):2760-73. DOI: 10.1523/JNEUROSCI.5120-03.2004
Source: PubMed


Rapid coordinated eye-head movements, called saccadic gaze shifts, displace the line of sight from one location to another. A critical structure in the gaze control circuitry is the superior colliculus (SC) of the midbrain, which drives gaze saccades by relaying cortical commands to brainstem eye and head motor circuits. We proposed that the SC lies within a gaze feedback loop and generates an error signal specifying gaze position error (GPE), the distance between target and current gaze positions. We investigated this feedback hypothesis in cats by briefly stopping head motion during large ( approximately 50 degrees ) gaze saccades made in the dark. This maneuver interrupted intended gaze saccades and briefly immobilized gaze (a plateau). After brake release, a corrective gaze saccade brought the gaze on goal. In the caudal SC, the firing frequency of a cell gradually increased to a maximum that just preceded the optimal gaze saccade encoded by the position of the cell and then declined back to zero near gaze saccade end. In brake trials, the activity level just preceding a brake-induced plateau continued steadily during the plateau and waned to zero only near the end of the corrective saccade. The duration of neural activity was stretched to reflect the increased time to target acquisition, and firing frequency during a plateau was proportional to the GPE of the plateau. In comparison, in the rostral SC, the duration of saccade-related pauses in fixation cell activity increased as plateau duration increased. The data show that the cat's SC lies in a gaze feedback loop and that it encodes GPE.

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Available from: Satoshi Matsuo, Jun 29, 2014
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    • "The spinal-like circuits described in [1], [3], [6]–[9], [23], [47], [48] served as inspiration in our previous robotic studies Fig. 2. The ASC. Hand-target errors are projected from the SC as input commands to the controller for each muscle group. The projected error to each muscle group is combined with an efference copy from RCs and a co-activation from the antagonist to produce a muscle activation which drives joint motion. "
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    ABSTRACT: We develop an adaptive controller for multi-joint, multi-muscle arm movements based on simplified spinal-like circuits found in the periphery, muscle synergies, and interpretations of gain-field projections from reach related neurons in the Superior Colliculus. The resulting innovation provides a highly robust sensory based controller that can be adapted to systems which require multi-muscle co-ordination. It provides human-like responses during perturbations elicited either internally or by the environment and for simple point-topoint reaching. We simulate limb motion and EMGs in Simulink using Virtual Muscle models and a variety of paradigms, including motion with external perturbations, and varying levels of antagonist muscle co-contractions. The results show that the system can exhibit smooth coordinated motions, without explicit kinematic or dynamic planning even in the presence of perturbations. In addition, we show by varying the level of muscle co-contractions from 0% to 40%, that the effects of external perturbations on joint trajectories can be reduced by up to 42%. The improved controller design is novel providing robust behavior during dynamic events and an automatic adaptive response from sensory-integration.
    Full-text · Article · Aug 2014 · IEEE transactions on neural systems and rehabilitation engineering: a publication of the IEEE Engineering in Medicine and Biology Society
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    • "Black trace is the average stimulation-induced saccade trajectory, which ends closely to the center of the movement field. d Close correspondence between the optimal saccade vectors of 13 different cells and the fixed-vector stimulation-induced saccades at the recording sites even be responsible for, the kinematic properties of saccades (Berthoz et al. 1986; Van Opstal and Van Gisbergen 1990b; Waitzman et al. 1991; Munoz et al. 1996; Stanford et al. 1996; Soetedjo et al. 2002; Matsuo et al. 2004). The precise nature of the collicular involvement in the dynamic control of saccades has been controversial, and will be the main topic of this paper. "
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    ABSTRACT: Recently, we proposed an ensemble-coding scheme of the midbrain superior colliculus (SC) in which, during a saccade, each spike emitted by each recruited SC neuron contributes a fixed minivector to the gaze-control motor output. The size and direction of this 'spike vector' depend exclusively on a cell's location within the SC motor map (Goossens and Van Opstal, in J Neurophysiol 95: 2326-2341, 2006). According to this simple scheme, the planned saccade trajectory results from instantaneous linear summation of all spike vectors across the motor map. In our simulations with this model, the brainstem saccade generator was simplified by a linear feedback system, rendering the total model (which has only three free parameters) essentially linear. Interestingly, when this scheme was applied to actually recorded spike trains from 139 saccade-related SC neurons, measured during thousands of eye movements to single visual targets, straight saccades resulted with the correct velocity profiles and nonlinear kinematic relations ('main sequence properties' and 'component stretching'). Hence, we concluded that the kinematic nonlinearity of saccades resides in the spatial-temporal distribution of SC activity, rather than in the brainstem burst generator. The latter is generally assumed in models of the saccadic system. Here we analyze how this behaviour might emerge from this simple scheme. In addition, we will show new experimental evidence in support of the proposed mechanism.
    Full-text · Article · Jul 2008 · Biological Cybernetics
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    • "Gaze and head amplitudes are not controlled in this framework. These competing hypotheses have been tested by observing behavioral and electrophysiological compensation to passive head perturbations (Choi and Guitton 2006; Coimbra et al. 2000; Matsuo et al. 2004; Sylvestre and Cullen 2006), microstimulation of numerous brain structures (Freedman and Quessy 2004; Pélisson et al. 1995), and naturally prolonged movements (Bergeron and Guitton 2000, 2002). The majority of studies have demonstrated gaze accuracy (see Freedman and Quessy 2004 for exception). "
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    ABSTRACT: Natural movements often include actions integrated across multiple effectors. Coordinated eye-head movements are driven by a command to shift the line of sight by a desired displacement vector. Yet because extraocular and neck motoneurons are separate entities, the gaze shift command must be separated into independent signals for eye and head movement control. We report that this separation occurs, at least partially, at or before the level of pontine omnipause neurons (OPNs). Stimulation of the OPNs prior to and during gaze shifts temporally decoupled the eye and head components by inhibiting gaze and eye saccades. In contrast, head movements were consistently initiated before gaze onset, and ongoing head movements continued along their trajectories, albeit with some characteristic modulations. After stimulation offset, a gaze shift composed of an eye saccade, and a reaccelerated head movement was produced to preserve gaze accuracy. We conclude that signals subject to OPN inhibition produce the eye-movement component of a coordinated eye-head gaze shift and are not the only signals involved in the generation of the head component of the gaze shift.
    Full-text · Article · Aug 2007 · Journal of Neurophysiology
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