One hundred and forty-one oculomotor-related efferent fibers of the NIC were penetrated in and near the NIC and the PC of alert behaving squirrel monkeys. The intersaccadic discharge of 57 fibers was not modulated with eye position but rather was reminiscent of the upward medium lead burst neurons of the nucleus of the posterior commissure (Moschovakis et al. 1991a), of the downward medium lead burst neurons of the NIC (Moschovakis et al. 1991b), or of the long lead burst neurons located near the NIC (Scudder et al. 1996a). The remaining 84 fibers modulated their discharge in relation to eye position and are the topic of this report. Their intraaxonal injection with a tracer enabled us to confirm the recording site of all fibers in our sample (27 in the PC and 57 in the NIC) and the origin and projection of many of them. The trajectory of their axons has not been completely reconstructed and will be the object of a future report. Preliminary results show that 39 of the 48 fibers recovered so far project through the PC, whereas the remainder (n = 9) descend via the MLF. The somata of all but 12 PC fibers were recovered, and their location in the NIC was ascertained. Because there were no differences between recovered and not recovered fibers and somata in terms of discharge pattern, we describe them together as a single group of NIC efferents.
The fiber illustrated in Fig. 1A displayed tonic intersaccadic activity and bursts that preceded saccades with an upward component, whether rightward or leftward. Figure 1B is a plot of mean intersaccadic vertical eye position (V; abscissa) versus mean interburst frequency of discharge (F; ordinate) for the same unit. The slope (3.5 spikes/s per degree of upward ocular deviation) and the correlation coefficient (r = 0.96) of the linear regression between the two variables are indicative of the sensitivity and of the reliability with which this fiber encoded the vertical position of the eyes. The intercept (102 spikes/s) is indicative of the unit's intensity of discharge when the animal was looking straight ahead. The firing of this fiber was not correlated with the mean horizontal position of the eyes between saccades (right inset). To get an indication of the regularity of its tonic discharge during intersaccadic intervals, we determined the coefficient of variation (CV) of interspike intervals. Because the standard deviation of interspike intervals [SD(ISI)] increased in proportion to the mean ISI (Fig. 1B, left inset), we evaluated the CV for positions within 2° of primary position. Its value was low enough (0.06) to indicate that this unit was a regularly discharging one.
Other burst-tonic responses were much less precise. The fiber of Fig. 1C had a primary position firing rate of 66 spikes/s, increased its firing rate for downward eye positions, and decreased it for upward positions. The shallower slope of the rate-position curve (2 spikes·s1·deg1) indicates that this fiber was less sensitive to vertical eye position than the one of Fig. 1B, whereas the large scatter of the data around the linear regression line indicates that this unit was less reliable in encoding the vertical position of the eyes (r = 0.67). The SD(ISI) of this unit obtained much higher values than that of Fig. 1B for roughly the same values of meanISI (inset). As a consequence, its CV was rather high (0.19), which underscores the irregularity of the tonic intersaccadic discharges of this fiber. As with the fiber of Fig. 1B, the firing rate of this unit was not correlated with the mean horizontal eye position (Fig. 1C, right inset).
The eye-position-related discharge shown in Fig. 1 is typical of the responses of 66 of the fibers we studied. The discharge of 35 units increased for upward eye positions, whereas the remaining (n = 31) increased their discharge for downward eye positions. Because vertical and horizontal eye position can covary due to sampling biases, we employed multiple regression to estimate each unit's preferred direction (up or down, left, or right) as well as the slopes, intercepts, and correlation coefficients of their rate-position curves. Most of them (n = 61) modulated their tonic discharge only for vertical eye position. A small number of units (n = 5) had an oblique on-direction as indicated by the fact that their discharge was modulated for both vertical and horizontal eye position. Quantitative details of the relationship between the firing rate of NIC fibers and the vertical position of the eyes are summarized in Table 1. Figures 2A and 3A plot rate-position linear regressions for our 35 upward and 31 downward NIC efferents, respectively. In general, the two variables were well correlated for both upward (Fig. 2A, inset) and downward (Fig. 3A, inset) cells. The frequency histograms of the slopes of these relationships peaked at 4 spikes·s1·deg1 (Fig. 2B) and about 3.5 spikes·s1·deg1 (Fig. 3B) for upward and downward units, respectively, indicating similar sensitivities and considerable overlap (sign notwithstanding) for both types of fibers. Also, the frequency histogram of the primary position rate peaked at ~90 spikes/s for upward units (Fig. 2C) and between 70 and 80 spikes/s for downward units (Fig. 3C).
The slope of the rate-position curve and the primary position rate uniquely determine position threshold. In our sample, this was equal to
46.4 ± 52.7° (mean ± SD) for upward and 42.97 ± 45.6° for downward fibers, respectively. The majority of fibers were active well before primary position (Figs. 2D
). When its whole range is considered, the position threshold (T) of NIC fibers is related to their vertical gain (kV
) through a power function of the form 48·|T
= 0.84; Fig. 2E
) for upward cells and 28·T-0.71
= 0.9; Fig. 3E
) for downward cells. To enable comparisons with previous samples, we also evaluated the relationship between vertical gain and position threshold when the latter is restricted to less than ±40°. In this case, the two variables are related linearly through an expression of the form kV
= 6.9 + 0.11T
= 0.72) for upward cells and kV
4.7 + 0.05T
= 0.45) for downward cells. Finally, few upward fibers had a CV >0.1 (Fig. 2F
), and thus the population as a whole can be thought of as regular. Although a larger number of downward fibers had a CV >0.1 (Fig. 3F
), on average these were no less regular than upward units (1-tailed t-test
Other units (n = 12) modulated their discharge for upward but little or not at all for downward deviations of the eyes. Figure 4A illustrates the eye-position-related discharge of such a unit. As shown, upward deviation of the eyes was accompanied by increases of firing frequency; in contrast, the neuron did not fire less than ~75 spikes/s whatever the depression of the eyes. The same point is made by the plot of Fig. 4B, which illustrates the relationship between the mean intersaccadic vertical eye position (V) and the mean frequency of the same neuron's discharge. There is an excellent linear relationship between the two variables when V is restricted to upward positions. However, this cell had a very small sensitivity (4B). It is for this reason that we refer to fibers of this sort as "unidirectionally modulated." Nor was the same unit's tonic intersaccadic discharge related to horizontal eye position. The remaining six units modulated their discharge for downward but little or not at all for upward eye positions. Quantitative details of the relationship between the discharge of unidirectional fibers and eye position are summarized in Table 1.
In addition to eye position, NIC efferent fibers usually modulated their discharge for saccades. For example, the fiber of Fig. 5A emitted bursts the intensity of which varied in proportion to the size of upward saccades. In contrast, its discharge usually was depressed or even ceased for downward saccades. To evaluate whether parameters of this unit's bursts were related to parameters of saccades, the number of spikes in the burst (Nb; ordinate) was plotted against the size of the upward component of saccades (V; abscissa) in Fig. 5B. There was an excellent linear relationship between the two variables (r = 0.97), whereas no relationship was found between Nb and the size of the horizontal component of saccades (Fig. 5B, inset). Further, an excellent correlation (0.89) was found between the duration of this neuron's bursts (Bd) and the duration of saccades (Sd; Fig. 5C). Finally, the peak frequency during bursts (Fm) was well related (r = 0.93) to the peak vertical velocity of accompanying saccades (m; Fig. 5D).
As illustrated in Fig. 6A, the bursts that other fibers emitted for saccades were much less intense. Here again, burst intensity varied in proportion to the size of the upward component of saccades, whereas the discharge was depressed or ceased for downward saccades. The bursts of such fibers were less sensitive and often less precise in terms of the saccade metrics they encoded. Figure 6B plots the size of the upward component of saccades (V; abscissa) against the number of spikes in the bursts (Nb; ordinate) of the fiber illustrated in Fig. 6A. Although the two variables were well correlated (r = 0.9), the slope of the linear relationship is much more shallow (0.26 spikes/°). Here again, no relationship was found between Nb and the size of the horizontal component of saccades (Fig. 6B, inset). The duration of this fiber's bursts (Bd) was also well correlated (r = 0.81) to the duration of saccades (Sd; Fig. 6C). However, unlike the fiber of Fig. 5, modulation of the peak frequency (Fm) of its bursts could account for only ~15% of the variance (r = 0.4; Fig. 6D) of the peak velocity (m) of the saccades they accompanied.
The saccade-related responses illustrated in Figs. 5 and 6 are typical of the pattern of discharge of the 65 burst-tonic units we encountered. Thirty-eight of them emitted bursts for upward saccades and 27 emitted bursts for downward saccades. Bursts preceded saccades by 4.3 ± 3.3 ms on the average (n = 65). In the 40 cells where pauses for off-direction saccades could be consistently documented, pause onset preceded saccade onset by 3.2 ± 3.7 ms on the average. Figures 7 and 8 provide summary illustrations of the relationships between saccade and burst parameters in upward (Fig. 7) and downward (Fig. 8) units, respectively. Figures 7A and 8A are cumulative plots of the 38 upward and the 23 downward linear regression lines between the number of spikes in the burst and the vertical size of saccades (up or down) that attained statistical significance (P 7B and 8B are cumulative plots of the 36 upward and the 27 downward statistically significant linear regression lines of burst duration versus saccade duration. The fact that they cluster around the diagonal indicates that burst duration was roughly equal to saccade duration for both upward and downward cells. Finally, Figs. 7C and 8C are cumulative plots of the 36 upward and the 16 downward statistically significant linear regression lines between peak firing rate and peak saccade velocity. Frequency histograms of the slopes and correlation coefficients of these relationships are illustrated as insets in Figs. 7 and 8, whereas the range, average, and standard deviation of the values they obtain are summarized in Table 1. Note that relationships that did not attain statistical significance (P from the population averages of Table 1.
It is important to note that the majority (n = 50) of the burst-tonic NIC fibers we encountered had the same on-direction for saccades and eye position. We refer to such units as in-phase units. Other fibers (n = 15) behaved quite differently in that they had opposite on-directions for saccades and eye position and are for this reason referred to as antiphase units. Six antiphase units emitted bursts for upward saccades but increased their discharge for downward eye positions. Another nine units emitted bursts for downward saccades but increased their discharge for upward eye positions.
Figure 9, provides a third example of the saccade-related discharge we encountered among efferent fibers of the NIC. Fibers such as this (n = 19) neither burst nor paused for saccades and are for this reason referred to as tonic units. Nevertheless, tonic fibers are not as distinct from burst fibers as our name would imply. The saccade-related bursts of some burst-tonic neurons were small, whereas some tonic neurons emitted small bursts or paused for some saccades, particularly large ones.
To evaluate whether the discharge of efferent NIC fibers is related to smooth-pursuit eye movements, their firing rate was studied for short segments (lasting for ~7 ISIs) during which the monkey smoothly pursued a target of interest (novel objects and morsels of food that were displaced slowly in front of its eyes). Figure 10 illustrates the relationship between the mean vertical velocity of the eyes (sp) during such segments versus the mean firing rate (F) of a fiber after correcting for changes in firing rate that would be due to changes of eye position (from the rate-position curves of the same fibers). As shown in Fig. 10A, the two variables could be well correlated, in this case through the expression F = 0.64sp 2.99 (r = 0.95). Enough data were available to carry out this analysis in 67 NIC efferent fibers (36 upward and 31 downward). Quantitative details about the relationship between the discharge of NIC efferents and the vertical velocity of the eyes during smooth pursuit are summarized in Table 1. About 60% of the fibers we examined (24 upward and 17 downward) modulated their discharge in concert with the vertical velocity of the eyes during smooth pursuit. Their on-direction for smooth-pursuit eye velocity was the same as their on-direction for eye position. The slope of the linear regression line could be as low as 0.3 (0.1) spikes/s per deg/s or as high as 2.1 (2.2) spikes/s per deg/s for upward (downward) fibers (Fig. 10B). Correlation coefficients between F and sp ranged from 0.51 to 0.95 for upward units and from 0.44 to 0.97 for downward units (Fig. 10B, inset). The remaining fibers we tested (12 upward and 14 downward) did not modulate their discharge for vertical smooth-pursuit eye velocity.