Macaque pontine omnipause neurons play no direct role in the generation of eye blinks

Abstract

We recorded the activity of pontine omnipause neurons (OPNs) in two macaques during saccadic eye movements and blinks. As previously reported, we found that OPNs fire tonically during fixation and pause about 15 ms before a saccadic eye movement. In contrast, for blinks elicited by air puffs, the OPNs paused <2 ms before the onset of the blink. Thus the burst in the agonist orbicularis oculi motoneurons (OOMNs) and the pause in the antagonist levator palpabrae superioris motoneurons (LPSMNs) necessarily precede the OPN pause. For spontaneous blinks there was no correlation between blink and pause onsets. In addition, the OPN pause continued for 40-60 ms after the time of the maximum downward closing of the eyelids, which occurs around the end of the OOMN burst of firing. LPSMN activity is not responsible for terminating the OPN pause because OPN resumption was very rapid, whereas the resumption of LPSMN firing during the reopening phase is gradual. OPN pause onset does not directly control blink onset, nor does pause offset control or encode the transition between the end of the OOMN firing and the resumption of the LPSMNs. The onset of the blink-related eye transients preceded both blink and OPN pause onsets. Therefore they initiated while the saccadic short-lead burst neurons were still fully inhibited by the OPNs and cannot be saccadic in origin. The abrupt dynamic change of the vertical eye transients from an oscillatory behavior to a single time constant exponential drift predicted the resumption of the OPNs.

Fig. 1.

Example of blink and associated eye transients. A: horizontal left eye transient. B: vertical left eye transient. C: right eyelid. Position traces are in green and velocity traces in black. It was a general feature, as in this example, to have the eye transients starting before the blink. How the single exponential fit of the monotonic drifts (in blue for the position traces, in red for the velocity traces) was computed is reported in the text. BL_ONS, HT_ONS, and VT_ONS indicate the onset of the blink, of the horizontal eye transient, and of the vertical eye transient, respectively. BLD_ONS, HTD_ONS, and VTD_ONS indicate the onsets of their exponential drifts.

Fig. 2.

Pontine omnipause neuron (OPN) pause onset: single trials. The first 3 panels illustrate movement position and velocity traces, OPN firing frequency, and OPN spike events as a function of time for subsets of single trials from cell c51026.A1. All traces are synchronized with the onset of the movement, identified with the vertical dotted lines labeled S_ONS (saccades) and BL_ONS (blinks). A: 9 to 11° rightward saccades. Top traces: right eye horizontal position (RE POS) and right eye horizontal velocity (RE VEL). Bottom traces: firing rate (FR) and associated spike events. B: trigeminal blinks. C: spontaneous blinks. The top traces in B and C are right eye eyelid position (EL POS) and right eye eyelid velocity (EL VEL). The pause leads, i.e., the time intervals between the last spike before the pause, identifying pause onset, and the movement onset clearly differ for saccades and blinks. D illustrates the distribution of the pause lead values for all the trials from this cell in 5 ms bins. The shift in time between saccadic pause leads and the pause leads for trigeminal blinks is quite evident. The pause lead distribution for spontaneous blinks was much wider and encompassed both saccadic and trigeminal distributions.

Fig. 3.

OPN pause and trigger onset leads: cell averages. A_A1 and A_A2 compare average saccadic pause leads (x-axis) and average blink pause leads (y-axis) for the OPN cells acquired from animal A1 and animal A2, respectively. Trigeminal blink averages are identified by the black dots and spontaneous blink averages are identified by the gray × symbols. Symbols below the 1:1 dotted lines indicate pause onset for blinks occurring, on average, later than pause onset for saccades. B_A1 and B_A2 compare, with the same layout of the top panels, saccadic trigger leads and blink trigger leads, as defined in methods. The bars on the bottom right corners are the averages of the SDs of each cell subset for the 3 types of pause (trigger) lead measures. The shift in time for all cells of the trigeminal pause (trigger) lead values when compared with the saccadic pause (trigger) lead values is quite remarkable, clearly indicating that OPN pause onset has different functions for saccades and trigeminal blinks. The 2 animals present evident differences in their spontaneous blink lead values.

Fig. 4.

OPN resumption leads: single trials. The first 3 panels illustrate movement position and velocity traces, OPN firing frequency, and OPN spike events as a function of time for subsets of single trials from cell c51026.A1, the same cell of Fig. 2. The layout of these 3 panels is identical to that of Fig. 2, with the following difference: the saccadic traces (A) are now synchronized with the offset of the saccade, identified with the vertical dotted line labeled S_OFF, and the blink traces are synchronized with respect to the time of maximum downward closing of the eyelid, identified with the vertical dotted line labeled BL_MAXCL. The cell resumed around the end of the saccade (A), which is also near when the saccadic short-lead burst neurons end their activity. For both trigeminal (B) and spontaneous (C) blinks, the cell resumed several 10 s of milliseconds after the maximum closing of the eyelid, which human electromyographic (EMG) data indicate it occurs near the end of the activity in the orbicularis oculi motoneurons (OOMNs). This striking difference is also evident in the histograms in D. Positive values mean that the cell resumed before the specific movement event. For the blink histograms, trigeminal and spontaneous data are pooled together. The third histogram illustrates that the OPN resumption occurred even after the time of the maximum positive velocity peak of the reopening phase, indicated by the asterisks in B and C. The human EMG data indicate that this event is reached upto 50 ms after the end of the activity in the orbicularis oculi muscle, as the result of passive elastic forces and the resumption of activity in the levator palpabrae superioris muscle.

Fig. 5.

Relative interspike interval (ISI) +1 firing: cell averages. The 2 panels illustrate the average relative firing with respect to baseline of the first ISI after the first resumption spike for saccades on the x-axis and for blinks on the y-axis for the 27 cells from animal A1 (A_A1) and for the 59 cells from animal A2 (A_A2) for which we have both average values (n ≥ 8). The 2 panels have different scaling factors for clarity. The bars on the bottom right corners report the average of the SDs of the resumption lead subsets, as indicators of the between-trials scatter of the data. The results of the linear regression are reported on the top left corners of the plots. Cells with faster initial resumption for saccades also showed faster initial resumption for blinks.

Fig. 6.

Eyelid exponential drifts: single trials. A_A1 illustrates, for the blinks (n = 34) of a cell data set from animal A1, the exponential fits of the eyelid position drifts, as defined in methods. A_A2 illustrates the fits for the blinks (n = 160) of a cell data set from animal A2. Both trigeminal and spontaneous blinks are included and only the trials with a clear breaking point in the eyelid velocity dynamics (56 and 63% of all eyelid traces, respectively) are reported. The traces are synchronized with respect to the first resumption spike after the pause. The default value (t → ∞) of the exponentials is artificially set to zero for clarity. The bottom panels are the distribution histograms of the associated resumption lead values. Positive values indicate that the onset of the exponential drifts followed the first resumption spike of the cell. Tc is the time constant average (±SD) of the exponential drifts.

Fig. 7.

OPN resumption leads from the onsets of the eyelid exponential drifts: cell averages. Histograms of the distributions of the OPN resumption leads with respect to the onset of the eyelid exponential drifts for the 29 cells from animal A1 (A_A1) and the 59 cells from animal A2 (A_A2) for which we have data. Positive values mean that the onset of the eyelid exponential drift followed, on average, the first resumption spike of the cell after the pause.

Fig. 8.

Horizontal exponential drifts of the eye transients: single trials. Same cells and layout as those in Fig. 6. A_HRA1 illustrates the horizontal exponential fits of the eye position drifts for the right eye in animal A1 (n = 58), whereas A_HLA1 illustrates the horizontal exponential fits of its left eye in the same trials (n = 58). A_HRA2 illustrates the horizontal exponential fits for the right eye in animal A2 (n = 243). Both trigeminal and spontaneous blinks are included and only the blinks with clear breaking points in both the horizontal and vertical eye velocity dynamics—and in both eyes in animal A1—(95% and 97% of all blinks, respectively) are reported. The traces are synchronized with respect to the first resumption spike after the pause. The default value (t → ∞) of the exponentials is artificially set to zero for clarity. The bottom panels are the distribution histograms of the associated resumption lead values. Positive values indicate that the onset of the exponential drifts followed the first resumption spike of the cell. Tc is the time constant average (±SD) of the exponential drifts.

Fig. 9.

Vertical exponential drifts of the eye transients: single trials. A_VRA1 illustrates the vertical exponential fits of the eye position drifts for the right eye in animal A1 (n = 58), whereas A_VLA1 illustrates the vertical exponential fits of its left eye (n = 58). A_VRA2 illustrates the vertical exponential fits for the right eye in animal A2 (n = 243). Same layout and same trials as those of Fig. 8. The vertical histograms were narrower and shifted later in time than the horizontal histograms in Fig. 8.

Fig. 10.

Comparison between saccadic and eye vertical drift resumption leads. For each cell, the average saccadic resumption lead is plotted on the x-axis and the average resumption lead of the vertical exponential drift on the y-axis. A positive value means that the OPN resumed its firing before saccadic offset and before the onset of the exponential drift of the vertical eye transient, respectively. VR_A1 illustrates the right eye data for the 29 cells from animal A1 for which we have data and VL_A1 the left eye data. VR_A2 reports the right eye data for the 59 cells from animal A2 for which we have data. We have no data for the left eye. The bars on the bottom right corners report the average of the SDs of the resumption lead subsets, as indicators of the between-trial scatter of the data. The results of the linear regression are reported on the top left corners of the plots. Cells that resumed their firing later with respect to saccadic offset also resumed their firing later with respect to the onset of the vertical eye drifts and vice versa.

Fig. 11.

Examples of intermediate spikes. The panels illustrate 3 examples of intermediate spikes, which randomly occurred in some blink trials in some cells. In the first 2 examples, from 2 different cells, an intermediate spike, most often alone (A), but sometimes followed by another one (B), was roughly centered at the time of maximum closing of the eyelid or soon after. The isolated single spike, like the example in A, was the most common pattern. Only 2 cells, one in animal A1 and one in animal A2, had the first intermediate spike following the maximum (negative) peak velocity of the closing phase by 10–15 ms, as in C. This first spike was followed by a low-frequency activity until the more typical resumption, which was easily seen as an abrupt increase in the firing rate. The vertical dotted lines indicate the onset of the right eye vertical exponential drift (REV_DONS).