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Single efferent fibers of the interstitial nucleus of Cajal (NIC) were characterized …

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- Anatomy and Physiology of the Primate Interstitial Nucleus of Cajal. II. Discharge Pattern of Single Efferent Fibers

The present study demonstrates that the firing rate (F) of efferent fibers of the NIC in alert, behaving monkeys is on the average related to the instantaneous vertical position (V) and the smooth-pursuit vertical velocity (Vsp) of the eyes, through the expression

<IT>F</IT>= 88 &plus; 3.1⋅<IT>V</IT>&plus; 0.8⋅<IT><A><AC>V</AC><AC>&dot;</AC></A></IT><SUB>sp</SUB> (1)
Additionally, NIC fibers emit ~0.6 spikes per degree of vertical displacement of the eyes during saccades. Note that parameters of discharge differ from one NIC unit to the next, often significantly. Differences between units can be qualitative rather than quantitative. For example, ~10% of the units demonstrated some sensitivity to the horizontal position of the eyes. Also, ~25% of the units modulated their discharge in relation to upward or downward eye position, but not both. Finally, the discharge of ~50% of the fibers was not affected by smooth pursuit, whereas ~25% of the fibers did not emit any bursts for saccades.

Comparison with previous studies

The present study focuses on the output of the NIC, whereas previous work emphasized the response properties of cells located in the NIC regardless of whether they were projection neurons or not. NIC neurons previously were divided into burst-tonic (BT), irregular tonic (IrT), vestibular-and-saccade (VSN), and burst (BN) neurons in the monkey and into BT, VSN, and pitch neurons in the cat (reviewed in Moschovakis 1997). There are several reasons to think that it is the previously described BT neurons that the fibers of the present study resemble most. First, the tonic discharge of the fibers we encountered was well correlated with the vertical position of the eyes during spontaneous saccades. Similar, excellent correlations between their tonic discharge and vertical eye position were described previously for BT neurons in both the rhesus monkey (King et al. 1981) and the cat (Fukushima et al. 1990). Further, the average vertical position sensitivity of the fibers we encountered (cf. Eq. 1) is quite similar to that of previously recorded NIC BT cells in rhesus monkeys (2.6 spikes·s-1· deg-1) (King et al. 1981) and cats (3.9 spikes·s-1·deg-1) (Fukushima et al. 1990). In contrast, primate IrT (King et al. 1981), primate VSN (Kaneko and Fukushima 1998), feline VSN (Fukushima et al. 1995), and feline pitch (Fukushima et al. 1990) neurons display little if any relationship with eye position, at least during spontaneous saccades.

Second, the NIC fibers we encountered discharged at a relatively high and regular rate when the animal was looking straight ahead. The average primary position firing rate of the fibers we encountered (cf. Eq. 1) agrees quite well with previous descriptions of BT NIC neurons of rhesus monkeys (79 spikes/s) (King et al. 1981) and cats (75 spikes/s) (Fukushima et al. 1990). In contrast feline pitch neurons (mean: 34 spikes/s; Fukushima et al. 1990) and VSNs (mean: 40 spikes/s; Fukushima et al. 1995) discharge at a lower rate. The same is true of primate IrT neurons (King et al. 1981). Also the units we studied discharged at a rather regular rate as indicated by their relatively low CV (mean: 0.09). Unfortunately, they cannot be compared with NIC neurons of the rhesus monkey because there is no information about the regularity of discharge of VSN, BT, and IrT cells in this species. On the other hand, the CV of the units we studied is similar to that of feline NIC BT neurons (mean: 0.15) (Fukushima et al. 1990). In contrast, feline pitch neurons (mean CV: 0.61) (Fukushima et al. 1990) and feline VSNs (mean CV: 0.5) (Fukushima et al. 1995) are quite irregular.

Finally, the majority of the NIC efferent fibers we encountered emitted bursts for vertical saccades. Consistent with previous descriptions of BT units in both the cat and the monkey, parameters of their bursts (number of spikes in the burst, duration, maximal rate of firing) were related to saccade parameters (saccade size, duration, and maximal eye velocity, respectively). BT neurons are not the only NIC cells that burst for saccades. More than half of the feline pitch cells also burst for saccades and quick phases (Fukushima et al. 1990) as do VSNs (Fukushima et al. 1995) in both the cat and the monkey (Kaneko and Fukushima 1998). However, the latencies of VSN bursts are in the long-lead range in both the cat (-35 ± 14 ms) (Fukushima et al. 1995) and the monkey (32.5 ± 21 ms) (Kaneko and Fukushima 1998). They are thus much longer than the latencies of NIC BT units documented in this study (-4.0 ± 3.4 ms), a previous study in the rhesus monkey (-4.0 ± 2.5 ms) (King et al. 1981), and a previous study in the cat (-10 ± 3 ms) (Fukushima et al. 1990). To conclude, this extensive comparison indicates that the NIC efferent fibers we encountered correspond to the previously described BT neurons of the NIC and not to its pitch, VSN, or IrT cells.

Besides conventional, well-behaved, BT discharges, we observed a number of less conventional discharge types. First we observed that ~25% of the primate NIC efferent fibers encountered are not bidirectionally modulated with vertical eye position. This property was first described for pursuit neurons and ~30% of the vestibular-plus-eye-position neurons of the primate vestibular nuclei (Chubb et al. 1984). Similarly, many upward vestibular cells of the cat increase their rate with the upward deviation of the eyes and discharge at a constant rate for downward eye positions (Iwamoto et al. 1990a). Horizontal cells also can behave in a similar manner; the discharge of ~30% of the neurons of the primate nucleus prepositus hypoglossi level off for off-direction eye positions (McFarland and Fuchs 1992). Previous documentation of this phenomenon in NIC neurons has been limited (e.g., Fig. 3D of Fukushima et al. 1990). Moreover, some NIC fibers had their saccade- and position-related signals increase in opposite directions (antiphase units). The existence of antiphase neurons had been predicted by a model of the neural integrator (the so called "rogue" cells) (Arnold and Robinson 1991) but previous documentation of discharge patterns such as this was limited to gaze velocity cells of the primate group Y (Tomlinson and Robinson 1984), eye and head velocity cells of the primate medial vestibular nucleus (Scudder and Fuchs 1992), and VSNs of the feline (Fukushima et al. 1995) and the primate (Kaneko and Fukushima 1998) NIC. The present study demonstrates that they are quite common among BT efferent fibers of the NIC (they amount to ~25% of the fibers in our sample).

To what extent can the discharge of vertical extraocular motoneurons be attributed to the input they receive from NIC fibers?

Assuming linear summation of inputs, a provisional answer can be had from comparisons between the discharge pattern of NIC efferent fibers and that of vertical motoneurons. In general, the rate-position curve of the NIC units we encountered is about two times shallower than that of vertical motoneurons (King et al. 1981; Robinson 1970). Unless the NIC output is amplified, some of the position sensitivity of vertical extraocular motoneurons must be due to sources other than the NIC, such as the vestibular nuclei (Chubb and Fuchs 1982; Iwamoto et al. 1990a,b; McCrea et al. 1987; Tomlinson and Robinson 1984). The importance of this additional input is shown by the fact that pontine MLF lesions interrupting the ascending projections of vertical secondary vestibular neurons cause vertical gaze nystagmus (Evinger et al. 1977).

The same is probably true of the bursts of NIC efferent fibers. Even when the sample is restricted to fibers that burst for saccades, these emit only ~0.6 spikes/deg of vertical eye displacement, which is equal to about half of the saccadic sensitivity of vertical oculomotoneurons (Hepp et al. 1989). Again this implies that much of the burst of vertical extraocular motoneurons is due to sources other than the NIC, such as vertical medium lead burst neurons of the riMLF (King and Fuchs 1979; Moschovakis et al. 1991a,b). However, the fact that many NIC efferent fibers emit saccade-related bursts could explain why human subjects generate hypometric vertical saccades after lesions of the NIC (Fukushima 1991).

On the other hand, the slope of the rate-velocity curve of vertical oculomotoneurons (King et al. 1981) and the intensity and regularity of discharge of presumed primate oculomotoneurons (Robinson 1970) and trochlear motoneurons (Fuchs and Luschei 1971) when the eyes are at primary position is similar to that of NIC efferent fibers. Accordingly, these aspects of motoneuronal discharge could be considerably influenced by the input they receive from the NIC.

Are there subpopulations of NIC efferent fibers?

Much of this study is devoted to a systematic exploration of a large number of parameters describing the discharge pattern of NIC efferent fibers. Each one of these parameters can be thought of as an axis of a multidimensional space, and every fiber in our sample can be described by its location in this space. The question we wish to consider is whether the units we studied fall into clusters corresponding to functionally distinct groups of neurons. To reduce the dimensions of the parameter space, we employed a principal component analysis. Figure 11 illustrates the cross-correlation between the nine variables we studied and the results we obtained. Each one of its boxes shows the location of each one of the units encountered in the plane formed by two of the variables studied. When one variable was discrete, such as in-phase/antiphase, we used analysis of variance (ANOVA) to compare the two classes in terms of the continuous variable. In the case where both variables were discrete, we used a chi2 test.

Examination of Fig. 11 shows that several correlations were significant. Burst latency (Lat) and Rv (the slope of the relation between vertical size and the number of spikes in the burst) are related to several other variables. We found that the earlier the onset of the bursts, the higher the fidelity with which they encoded saccade duration (r(Bd/Sd), row 6), the higher the slope between their maximal frequency and the maximal saccadic velocity (G(Fm/Vm), row 7), and the higher the Rv (row 5). Also, fibers emitting weaker bursts (small Rv) were more irregular (high CV, column 3). This is consistent with a previous description of feline NIC BT units (Fukushima et al. 1990). Moreover, the higher the Rv (column 6), the higher the fidelity with which the bursts of NIC efferent fibers encoded saccade duration and the higher the slope between their maximal frequency and the maximal velocity of saccades. The bursts of bidirectional units had longer latencies than those of unidirectional units (column 4), whereas antiphase units discharged more irregularly (higher CV) and emitted weaker bursts (shallower Rv) than in-phase units (row 8). Finally, the more reliably a neuron's bursts encoded saccade duration the higher the sensitivity with which they encoded the maximal vertical velocity of saccades (column 7). With the exception of the good correlation between F0 and CV, all other correlations were not significant. Units which did not modulate their discharge for saccades (tonic neurons) were analyzed separately. An ANOVA did not reveal differences between tonic and BT neurons in terms of regularity of discharge, firing rate at primary position, and rate-position slope. The monkey vertical neural integrator therefore differs from the cat horizontal neural integrator, the tonic neurons of which are thought to be more regular than BT neurons (Escudero et al. 1992).

For our principal component analysis, we elected to exclude the regression coefficients of the rate-velocity, rate-position, and Nb versus size curves as well as the gain of the curve relating burst duration with saccade duration from our cross-correlation analysis because the high correlations between the slopes and the correlation coefficients of these analyses rendered them redundant. We also did not include any of the smooth-pursuit variables because vertical smooth-pursuit eye velocity was not related to the discharge of ~50% of the units in our sample. Suffice it to say that sensitivity to vertical smooth-pursuit eye velocity was not correlated with any of the nine discharge parameters of Fig. 11. Finally, we restricted the parameter space to continuous variables and excluded units that had a zero value in any one of these variables. Following these restrictions, there were 45 BT units left in our sample; three factors were determined that accounted for almost 79% of the variance in this considerably restricted sample. The first factor (accounting for ~45% of the variance) was related to parameters of saccade-related bursts (i.e., latency, slope of the relationship between Nb and saccade size, regression coefficient of the relationship between burst duration and saccade duration, and slope of the relationship between maximal frequency and maximal saccadic velocity). The second factor (accounting for ~20% of the variance) was related to the regularity and intensity of discharge at primary position. The third factor (accounting for ~14% of the variance) was related to position sensitivity. These three factors ("burstiness," "regularity," "sensitivity") form the axes of the three-dimensional plot of Fig. 12. As shown here, NIC efferent fibers form a diffuse cloud one end of which is made of regular but relatively insensitive units that emit strong bursts. The cloud continues through units of average regularity and sensitivity that also emit fairly strong bursts and ends with units that emit weak bursts and vary in terms of regularity and sensitivity. Although the absence of bursts did not allow us to extend the principal component analysis to tonic NIC units, these can be thought of as a continuation of the same cloud on a plane orthogonal to the "burstiness" axis and located some distance away from its origin (such as the regularity-sensitivity plane that forms the floor of Fig. 12).

To summarize, the efferent fibers of the NIC encode a constellation of oculomotor variables in terms of a complex array of discharge parameters. Each of these variables has enough spread to serve as a basis for separating the units into classes, but whatever the variable chosen, the gulf between the extremes always is occupied by fibers of intermediate properties. Even using parameters of discharge that are inherently dichotomous to divide the population of NIC efferent fibers into bi- and unidirectionally modulated units or into in-phase and antiphase units does not break the NIC efferent fibers into meaningful functionally distinct groups because neither bidirectional nor antiphase units differ in other respects much from units with antithetical properties. Therefore we conclude that NIC efferent fibers occupy a functional continuum in the parameter space that defines their discharge. Further we conclude that each NIC efferent fiber sends a combination of eye-position, saccade-, and smooth-pursuit-related signals to targets of the vertical neural integrator (including extraocular motoneurons). To determine whether identical copies of these signals are sent simultaneously to all targets of the NIC, we must know the trajectories and patterns of termination of functionally identified axons that arise from individual NIC neurons. Their study will be the object of a future report.


The expert technical assistance of P. Keller and the comments of two anonymous reviewers are acknowledged gratefully.

This work was supported by Human Capital and Mobility Grant ERBCHRXCT-940559.


Address for reprint requests: A. K. Moschovakis, Dept. Basic Sciences, Faculty of Medicine, University of Crete, P.O. Box 1393, Crete, Greece 71110.

Received 2 February 1998; accepted in final form 10 September 1998.

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