Vergence neurons identified in the rostral superior colliculus code smooth eye movements in 3D space

Abstract

The rostral superior colliculus (rSC) encodes position errors for multiple types of eye movements, including microsaccades, small saccades, smooth pursuit, and fixation. Here we address whether the rSC contributes to the development of neural signals that are suitable for controlling vergence eye movements. We use both single-unit recording and microstimulation techniques in monkey to answer this question. We found that vergence eye movements can be evoked using microstimulation in the rSC. Moreover, among the previously described neurons in rSC, we recorded a novel population of neurons that either increased (i.e., convergence neurons) or decreased (i.e., divergence neurons) their activity during vergence eye movements. In particular, these neurons dynamically encoded changes in vergence angle during vergence tracking, fixation in 3D space and the slow binocular realignment that occurs after disconjugate saccades, but were completely unresponsive during conjugate or the rapid component of disconjugate saccades (i.e., fast vergence) and conjugate smooth pursuit. Together, our microstimulation and single-neuron results suggest that the SC plays a role in the generation of signals required to precisely align the eyes toward targets in 3D space. We propose that accurate maintenance of 3D eye position, critical for the perception of stereopsis, may be mediated via the rSC.

Figure 1.

Example of vergence eye movements evoked by electrical stimulation of the rSC. A, Schematic representation of the topographic map of the SC. *The location an example site of stimulation in the rSC that evoked vergence eye movements. Inset, Dorsal/ventral location of vergence compared with rSC visual neurons and small motor burst neurons. B, Distribution of the size of the first saccade evoked by stimulation in the rSC (N_MonkeyS = 105, N_MonkeyD = 89). C, Two examples of a series of staircase saccades evoked by stimulation (dark bar) during fixation of a far (top) and near (bottom) target. Stimulation during fixation of a far target evoked very small conjugate staircase saccades with no change in vergence angle. Conversely, stimulation during fixation of a near target (convergence ∼10 degrees) evoked small staircase saccades with a significant diverging eye movement. D, Average change in conjugate and vergence position over time during far (top) and near (bottom) viewing for all stimulation sites. E, Distribution of latencies calculated from the onset of stimulation to the onset of either a conjugate saccade (black bars) or the vergence movement (red bars) during far (left) and near (right) viewing. F, Regression between vergence latency and conjugate latency calculated during near viewing. contra, Contralateral eye; ipsi, ipsilateral eye position.

Figure 2.

Example of convergence eye movements evoked by electrical stimulation of the rSC. A, Two examples of a series of staircase saccades evoked by stimulation (dark bar) during far fixation that evoked very small conjugate staircase saccades with a significant converging eye movement. B, Average change in conjugate and vergence position over time. C, Distribution of latencies calculated from the onset of stimulation to the onset of either a conjugate saccade (black bars) or the vergence movement (red bars).

Figure 3.

Example neurons recorded in the rSC. A, Example of a typical parafoveal visual neuron recorded during the presentation of a visual target. Raster plots are aligned on target onset. Gray shaded area represents the time segment used to calculate average firing rate after the visual stimulus was presented. B, Example discharge of an rSC small motor burst neuron, recorded among the convergence and divergence neurons, during small contralateral saccades and smooth pursuit. Raster plot (left panel) aligned on saccade onset. C, Example raster plots of a divergence neuron during (C1) a visual paradigm and (C2) small conjugate saccades (left) and conjugate smooth pursuit (right). Average firing rate with SEs are superimposed on the unit activity, and average position trace with SEs is plotted below. conj, Conjugate.

Figure 4.

Example vergence neurons in the rSC. A1, Neuronal activity of a divergence neuron during a convergence step paradigm. Average firing rate with SE (gray shaded trace) is superimposed on corresponding raster plot, and average position trace with SEs is plotted below. Traces are aligned on vergence onset. A2, Linear regression between vergence angle and firing rate for divergence neurons. Regression line and data points for the example neuron shown in A1 are shown in black, and regression lines for the population of neurons are shown in gray. Inset, Plotting of slopes of conjugate position versus the slopes of vergence position for each individual divergence neuron. B1, Discharge rate of a convergence neuron recorded during convergence step paradigm aligned on vergence onset. B2, Linear regression between vergence angle and firing rate for convergence neurons. Example neuron regression and corresponding data points are plotted in black, and regression lines for the population of convergence neurons are plotted in gray. Inset, Plotting of slopes of conjugate position versus the slopes of vergence position for each individual convergence neuron.

Figure 5.

Neuronal activity of example vergence neurons during smooth pursuit. A, Discharge rate of a divergence (A1) and convergence neuron (A2) during conjugate smooth pursuit. B, Discharge rate of a divergence (B1) and convergence neuron (B2) during vergence smooth pursuit. Model fits, estimated using Equation 1, are superimposed in blue on the firing rate.

Figure 6.

Neural control of fast versus slow vergence. A, Illustration of an example disconjugate eye movement that has a period of fast vergence to quickly redirect the eyes (blue trace) as well as a period of slow vergence to binocularly position the eyes and ensure accurate visual perception (red trace). A1, A2, The onset on fast versus slow vergence. B, Example discharge rate of a convergence neuron during disconjugate saccades aligned on fast vergence (i.e., saccadic onset, left) and slow vergence onset (right). Average conjugate (conj, blue trace) and vergence (verg, red trace) velocity and vergence position traces are shown below the raster. Average firing rate with SE is superimposed on the raster plot. Model fit, predicted using Equation 2 is superimposed in red on the firing rate. Vertical dashed lines indicate segments used for the fits. C, Left, Correlation between the time of the neuronal activation and the time of slow vergence onset for the example neuron shown in B. Right, Distribution of latencies calculated from the onset of neuronal activation and either the onset of the saccade (blue) or the onset of slow vergence (red) for the population of neurons.