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This Article Abstract Full Text (PDF) All Versions of this Article: 94/2/1385    most recent 00109.2005v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (6) Citing Articles via Google Scholar Google Scholar Articles by Kim, Y.-G. Articles by Heinen, S. J. Search for Related Content PubMed PubMed Citation Articles by Kim, Y.-G. Articles by Heinen, S. J.

Trajectory Interpretation by Supplementary Eye Field Neurons During Ocular Baseball

¹The Smith-Kettlewell Eye Research Institute, San Francisco, California; and ²School of Computer Engineering, Sejong University, Seoul, Korea

Submitted 31 January 2005; accepted in final form 19 April 2005

	ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
Good performance in the sport of baseball shows that humans can determine the trajectory of a moving object and act on it under the constraint of a rule. We report here on neuronal activity in the supplementary eye field (SEF) of monkeys performing an eye movement task inspired by baseball. In "ocular baseball," a pursuit eye movement to a target is executed or withheld based on the target’s trajectory. We found that a subset of neurons in the SEF interpreted the trajectory according to the task rule. Other neurons specified at a later time the command to pursue the target with the eyes. The results suggest that the SEF can interpret sensory signals about target motion in the context of a rule to guide voluntary eye movement initiation.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
An object that moves in the environment could be predator or prey, a threatening projectile such as a tossed stone, or it might have no consequence at all. The odds of an animal’s survival increase as its strategy to deal with moving objects becomes more sophisticated. Simple animals respond to moving objects reflexively. For example, the size of an object is sufficient for a toad to approach or to avoid it (Ewert 1980). However, the actions of primates are often guided by learned experience, as opposed to them being innate reflexes. Therefore to fully understand the neuronal control of primate behavior, it is critical to understand how the brain operates in the context of learned contingencies. This study was done to determine the role of the supplementary eye field (SEF), a structure involved in voluntary eye movement initiation, in interpreting a moving stimulus that signals an eye movement in the context of a rule.

Previous studies have shown that neurons in the SEF are active during saccadic (Schall 1991; Schlag and Schlag-Rey 1987) and smooth pursuit (Heinen 1995; Heinen and Liu 1997; Petit and Haxby 1999) eye movements. Stimulation here evokes saccades (Russo and Bruce 2000; Schlag and Schlag-Rey 1987; Tehovnik et al. 1999) and can facilitate pursuit initiation (Missal and Heinen 2001). These results suggest that the SEF participates in eye movement control. Other studies suggest a more specific role of the SEF in controlling voluntary eye movements. For example, it appears to participate in predictive and anticipatory smooth pursuit. Neuronal activity during pursuit of predictable target motion has been observed here to peak before the predictable target events (Heinen and Liu 1997). A related result is that electrical microstimulation of the SEF can cause anticipatory smooth pursuit to begin earlier (Missal and Heinen 2004). It has also been shown that SEF neurons are more active for voluntary saccades directed opposite the target’s location in the antisaccade task (Schlag-Rey et al. 1997).

Antisaccades, as well as predictive and anticipatory pursuit, are voluntary eye movements in the sense that they are executed without the direct guidance of a visual target and require learning. Because the SEF is involved in smooth pursuit, we wanted to know if this region might interpret the trajectory of a moving stimulus that may or may not become the target of an eye movement depending on a learned rule. The task we devised to test this is inspired by baseball, a sport that epitomizes interpreting a moving target in the context of a rule. A key feature of ocular baseball is the waiting period, during which the target moves and the animal must maintain fixation. A waiting period has been used before in laboratory go/nogo paradigms to study how eye or limb movements are planned in the SEF (Mann et al. 1988). In these paradigms, the animal plans the response while waiting and viewing a persistent stimulus. After the waiting period, a cue is given to move or not. In ocular baseball, the waiting period instead is imposed following the introduction of the cue, the moving target. Therefore neuronal activity related to interpreting the trajectory of that target can develop before activity related to the response occurs.

In ocular baseball, monkeys rotate their eyes and direct the fovea appropriately to "hit" and subsequently pursue with an eye movement a moving spot target (Fig. 1). Here, the animal must pursue the target if it crosses a visible strike zone ("strike" trials), and withhold eye movements if it does not ("ball" trials). Thus the trajectory of the target is a cue indicating whether the animal should make or withhold an oculomotor response. It was found that one population of neurons in the SEF reflected the state of the cue. At a later time, another population was activated before and during a movement on strike trials. The results suggest that the SEF can interpret a cue in the context of a rule to guide eye movement behavior.

View larger version (10K): [in this window] [in a new window]   FIG. 1. The ocular baseball paradigm. A: spatial layout. The animal fixates a red spot illuminated on the screen. Surrounding this spot is a visible, square "strike zone" that subtends 12°. An illuminated target begins to move from 1 of 2 20° eccentric positions in either the left or right periphery. If the target crosses the strike zone (strike trial, green), the animal must follow it with the eyes. If the target bypasses the strike zone (ball trial, red), the animal must withhold eye movements and maintain fixation. Order of presentation of trajectory angles was random in these experiments. The dotted line indicates in all plots when the target intersects the leading edge of the strike zone. B: sequence of events. Fixation point is illuminated and 500 ms after the monkey acquires it, the target appears and begins to move. Trajectory of the target is also the cue, specifying to the animal whether or not to follow it with the eyes. Waiting period overlaps time during which the cue evolves. Dashed and dotted lines define limits of the waiting period.

	METHODS

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Monkeys began the trial by fixating the red spot in the center of the screen. The baseball target appeared 20° eccentric, randomly on the left or right, and began to move toward the center of the screen. Possible angles were ±5, ±10, or ±15° (strike targets) and ±30, ±40, or ±45° (ball targets) with respect to horizontal. In an individual trial block, all strike angles had the same magnitude, as did all ball angles. Target speed was between 20 and 40°/s, and was also constant in a trial block. The waiting period was defined as the time between when the target began to move and when the target crossed the invisible vertical line defined by the leading edge of the plate (Fig. 1A). Hence the duration of the waiting period varied as a function of target angle and speed. Monkeys were required to maintain their gaze in a 3° electronic window centered on the fixation point during this time, or the trial was aborted. After the waiting period, in strike trials, the monkeys had to track the target and maintain eye position within a 5° window centered on the target. In ball trials, the animals had to maintain fixation within a 6° window. In either case, an error aborted the trial. On successful completion of the trial, monkeys received a few drops of liquid reward. Only data from correct trials are reported. The intertrial interval was 500 ms.

Eye movements were recorded with implanted scleral coils. Angular eye position was sampled at 1 KHz and stored on disk for off-line analysis. Eye velocity was obtained by off-line digital differentiation of the position records, and passed through a two-pole Butterworth filter (cut-off = 50 Hz). Pursuit onset time was calculated from eye velocity using a linear regression method (modified from Kao and Morrow 1994). Saccades were not removed from the records. Single neurons were recorded from the SEF using tungsten microelectrodes (FHC) with an impedance of 1.0–1.5 MOhm, tested at 1,000 Hz. To obtain a continuous representation of the instantaneous neuronal activity in time, spike occurrences were convolved with a Gaussian function (sigma = 30 ms) to yield spike density.

To determine the time that neuronal activity became different for ball and strike trials (separation time), we applied a Wilcoxon rank-sum test to the instantaneous spike density values at each time-point in the interval of 500 ms before to 1,000 ms after target motion onset. Separation time was defined as when the P value of the ball/strike activity difference reached significance (0.05) and remained significant for 100 consecutive ms.

	RESULTS

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We recorded 55 neurons from two monkeys performing the ocular baseball task. Thirty-four of these fell into two distinct classes and are analyzed here. Neurons of the first type were active in strike trials, but not ball trials, and therefore will be referred to as "strike neurons." The results from a typical strike neuron are shown in Fig. 2A. Note that the activity in the strike trials was strong but that the neuron was virtually silent in the ball trials when the animal had to maintain fixation. For each neuron, mean activity in strike and ball trials was calculated over the interval from target motion onset until reward onset. The strike to ball activity ratios are plotted in Fig. 2B. Asterisks indicate significance (Wilcoxon rank-sum test, P < 0.05).

View larger version (19K): [in this window] [in a new window]   FIG. 2. Neuronal activity and ocular behavior during the task for strike neurons. A: rasters show the activity of a single neuron from multiple trials, grouped together here for each of the 4 strike trajectories (±5°; top) and each of the 4 ball trajectories tested (±30°; bottom). Icons on the left indicate the trial type (strike or ball), and arrows on the right show the angle of target motion used to obtain the rasters in each group. Solid, continuous line superimposed on rasters shows activity averaged over the entire block as a spike density function (green for strike trials, red for ball trials). Dashed line represents time that the target appeared, and dotted line represents time that it crossed the leading edge of the strike zone. Trials were aligned on target appearance. This neuron had higher activity in strike trials than in ball trials. Below the neuronal data are displayed the raw horizontal eye velocity traces from only the 1st 2 trials tested at each angle for clarity. Small spike-like incursions represent saccades, which have been clipped at 50°/s, and smoother traces pursuit eye movements. Note that small eye movements can occur before the target crosses the strike zone, provided that eye position remains within an electronic window set equal in size to the strike zone. B: ratio of mean strike to ball activity for all cells. Asterisks indicate significance.

View larger version (22K): [in this window] [in a new window]   FIG. 3. Cue neurons. A: activity of a single cue neuron and accompanying eye movements. Note that the activity of this cell was greater during the waiting period for balls (±40°) than for strikes (±15°). Other cue cells showed higher activity for strikes. Details as in Fig. 2. B: activity ratios for all cue cells. For strike-preferring cells, the strike to ball activity ratio was calculated and plotted on the upper axis (green bars). For ball-preferring cells, the ball to strike ratio was used, plotted on the lower axis (red). Asterisks indicate significance.

View larger version (23K): [in this window] [in a new window]   FIG. 4. Tuning functions of cue neurons. A: mean activity during the waiting period of a cell that preferred strike trajectories. Note overall higher activity for strikes, regardless of target approach angle. Strike angles are shaded in green, whereas ball angles are shaded in red. B: neuron that preferred ball angles. Details as in A. Error bars indicate SE.

View larger version (19K): [in this window] [in a new window]   FIG. 5. Sequence of neuronal activation in the supplementary eye field (SEF) and behavior during ocular baseball. A: determining ball/strike separation time. Separation time was defined as when the instantaneous spike density values for strike and ball trials became significantly different and remained significantly different for 100 ms (see METHODS). Activity during ball trials (red line) separates and becomes significantly different from activity for strike trials (green line) when the P value (gray line) drops below 0.05. B: cumulative distributions of separation times for cue and strike neurons, as well as smooth pursuit latencies. Median separation time for cue cells (142.5 ms) preceded that of strike cells (400.5 ms), which in turn preceded median pursuit latency (463.0 ms). Dashed vertical line indicates beginning of waiting period. Cells that did not have a separation time within the analysis period do not appear in the cumulative plots (n = 7 cue cells and n = 5 strike cells).

View larger version (12K): [in this window] [in a new window]   FIG. 6. Pursuit latencies aligned with respect to plate crossing. Distribution is consistent with the monkeys timing their eye movements to coincide with when the target crossed the plate (dashed line) rather than waiting for the target to cross and generating a reflexive movement.

	DISCUSSION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

In a natural setting, after an animal has discriminated the trajectory of a moving object, it must decide whether or not to act on it. In primates, the decision is usually based on learned information regarding the potential benefits of avoiding or acquiring the object. Ocular baseball is designed to explore the neuronal substrate of this behavior. In the classic go/nogo task, where the waiting period occurs before the cue is given, the cue and movement activity are confounded.

In ocular baseball, the cue coincides with the waiting period. This allows cue-related activity and movement-related activity to be assessed independently. Ocular baseball imposes the added constraint over discrimination tasks that, not only must the animal discriminate a target’s trajectory, it must then make or withhold an eye movement after evaluating that trajectory in the context of a rule.

In this task, the activity of strike cells preceded the eye movements and continued during them. This type of cell is likely from the class of SEF neurons previously reported to be involved in movement preparation and execution. Movement-related activity here has been observed to accompany simple, visually guided saccades (Lee and Tehovnik 1995; Schall 1991; Schlag and Schlag Rey 1987). When tested with a go/nogo paradigm, preparatory set activity preceding saccades has been observed (Schall 1991). Movement-related activity also been reported to accompany smooth pursuit (Heinen 1995). When tested with predictable target motion, some SEF neurons have been shown to exhibit activity that precedes, or anticipates, predictable target events during pursuit (Heinen and Liu 1997). The SEF projects to the superior colliculus (Huerta and Kaas 1990), which is involved in saccade (for a review, see Sparks and Hartwich-Young 1989) and smooth pursuit generation (Krauzlis et al. 2000) and also projects to nucleus reticularis tegmenti pontis (NRTP) (Huerta and Kaas 1990), which plays a role in pursuit (Suzuki et al. 2003). Therefore movement planning and execution activity of the strike cells might trigger or modulate the movement command generated in these brain stem structures. Further evidence for this is that the strike cells became active on average 62.5 ms before the movement, similar to the latencies of saccades evoked from the SEF by microstimulation (Russo and Bruce 2000).

The cue cells that we recorded in this study were differentially active for strikes and balls and seem to be involved in interpreting target trajectory in a rule-governed framework for several reasons. Because the differential activity was limited to the waiting period, it was probably related to the cue and not the movement itself. Nor were these simply visual-motion neurons, because we found little evidence of selectivity for any specific direction of target motion (see Fig. 4), contrary to what is seen in motion processing areas such as MT (Maunsell and Van Essen 1983; Zeki 1974). Neurons in MT can make fine discriminations about the direction of motion of random dot patterns (Britten et al. 1996) and are likely used in the earliest phase of baseball, when trajectory angle must be discriminated before the rule is applied. The tuning functions of cue neurons were very different from MT neurons and remarkable in that the highest activity accompanied four different directions of target motion, as opposed to one as is usually observed (Maunsell and Van Essen 1983; Zeki 1974). Furthermore, these neurons interpreted the trajectory on average 258 ms before the strike cells, a sufficient lead time for them to convey the decision to the strike cells to become active. To shed more light on whether the strike cells, and the animal, were "reading out" the decision of the cue cells, it is important to know if cue cell activity agreed with the behavior on error trials. Unfortunately, the relatively low error rate (5%) precluded a meaningful analysis of this relationship.

There are other potential interpretations of our cue cell behavior in the context of activity recorded from the SEF in other studies. One study found that some SEF neurons were more involved in object-centered coding than in coding for rules (Olson and Gettner 1999). In this study, SEF activity was higher for saccades made to one end of a target, regardless of whether the "rule" of the task was to saccade to that end or to the other end of the target based on a color cue. The target trajectories in our experiment could be thought of as boundaries of a virtual object, and cue cells, which are active when the target starts to move at the periphery, might be coding the edge of the virtual object. However, our cue cells responded equally well for left and right target motion, evidence against this. Another interpretation is that the cue cells are fixation neurons (Bon and Lucchetti 1992; Lee and Tehovnik 1995; Schlag et al. 1992), because a majority of them are active during ball trials when the monkey must maintain fixation. This seems unlikely because the activity of cue cells during the waiting period is very different for strikes and balls, despite that the monkey is fixating in both cases. Furthermore, during the movement period in ball trials when the monkey continues to fixate, cue cells do not show a consistent pattern of activity, sometimes even decreasing to baseline levels (e.g., see Fig. 3).

The relative times of neuronal and behavioral events during ocular baseball hint at the sequence of processing that transpires during the task. Cue cell separation occurred before strike cell separation, suggesting that the cue cells might notify the strike cells that a movement was, or was not, needed. The difference in median separation time (258 ms) is quite large, and therefore the cue cells likely did not directly trigger the strike cells; rather, strike cell activity was delayed until the appropriate time. In future work, we plan to take advantage of this delay to test whether the cue cells take longer to interpret more difficult trajectories, resulting in a later median separation time. The difference in separation times for the strike cells and movement onset was 62.5 ms, suggesting that this is the time necessary for the strike activity to affect the response.

Two other regions, the prefrontal cortex (PFC) and a section of premotor cortex (PMC) located posterior to the arcuate sulcus, have been shown to be active during rule-guided behavior (Wallis and Miller 2003). In that study, monkeys performed in a matching and nonmatching sample task. In it, the monkey was shown a sample picture and was cued to select at a later time a picture that was either the same as or different from the sample. The monkey had to continue holding a lever if the picture did not conform to the same/different rule and release it if it did. Neurons were selective for various aspects of the task, but in both areas, cells were the most selective for one of the rules or one of the behaviors. Both areas are reciprocally connected with the SEF (Huerta and Kaas 1990). It is possible that the SEF could be reading out rule-related information from these prefrontal areas, or alternatively, be their functional analog in the control of eye movements. Whether in cooperation with prefrontal cortex or not, our results suggest that the SEF may provide a linkage between interpreting a rule and issuing a movement command.

	GRANTS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
This work was supported by National Eye Institute Grant R01 EY-011720-06.

	ACKNOWLEDGMENTS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
We thank R. M. McPeek, E. L. Keller, and S.-N. Yang for helpful comments on the manuscript and S. Pilkington for technical assistance.

	FOOTNOTES

 
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Address for reprint requests and other correspondence: S. J. Heinen, Smith-Kettlewell Eye Research Inst., 2318 Fillmore St., San Francisco, CA 94115 (E-mail: heinen{at}ski.org)

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This Article Abstract Full Text (PDF) All Versions of this Article: 94/2/1385    most recent 00109.2005v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (6) Citing Articles via Google Scholar Google Scholar Articles by Kim, Y.-G. Articles by Heinen, S. J. Search for Related Content PubMed PubMed Citation Articles by Kim, Y.-G. Articles by Heinen, S. J.