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REPORT
1Division of Sensory-Motor Systems, Yerkes National Primate Research Center and 2Department of Neurology, Emory University, Atlanta, Georgia
Submitted 19 May 2006; accepted in final form 14 June 2006
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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0.10 spike/s/°/s). This combination of properties is compatible with classifying these neurons as gaze-velocity related. Absence of modulation during VORd testing could be caused by cancellation of head and eye movement sensitivity or dependence of neuronal firing on volitional SP commands. Our results support the suggestion that modulation of SP-related MSTd neurons reflects volitional SP commands rather then eye movements generated by reflex pathways. |
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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; Newsome et al. 1988). Previous studies have shown that smooth pursuit–related neurons in dorsal-medial MST (MSTd) continued firing during a target blink, showing that the neurons carry extraretinal signals (Ilg and Thier 2003; Newsome et al. 1988). It has not been determined whether the extraretinal signals reflect actual volitional smooth pursuit commands, corollary discharge of those commands (Sommer and Wurtz 2004), proprioceptive signals, prediction, or remembered target motion in space.
Recent studies have suggested extraretinal signals in MST may contribute to regulation of internal gain of pursuit (Churchland and Lisberger 2005). Extraretinal signals might be related to a reconstructed target motion, predictive, or "remembered" target motion in space. Such signals may help to maintain smooth pursuit as eye velocity matches target velocity. Although several studies have attempted to relate extraretinal signals in different brain regions to the metrics of smooth eye movements (Kawano et al. 1994; Newsome et al. 1988; Tanaka and Fukushima 1998), no studies have attempted to determine whether reflex driven eye movements might contribute to the MSTd pursuit neuronal response. The aim of this study was to determine whether modulation of MSTd pursuit neurons occurs during reflex driven smooth eye movements or volitional smooth pursuit commands per se. To resolve this question, we examined vestibular ocular reflex (VOR)-driven eye movements in complete darkness to eliminate volitional smooth pursuit commands and visual inputs but to produce eye motion with virtually identical dynamics to that associated with smooth pursuit conditions. Modulation of MSTd smooth pursuit neurons during VOR in darkness could indicate the presence of vestibular input or eye movement sensitivity because of proprioceptive feedback or efference copy of slow eye movements that might contribute to the extraretinal signals. Our studies were designed to examine some of the possible sources of signals related to extraretinal modulation of MSTd neurons.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Behavioral and single unit data were collected from three normal juvenile rhesus monkeys (Macaca mulatta), weighing 5–7 kg. A detailed description of most of our procedures can be found in earlier publications (Mustari et al. 1988, 1997, 2001; Ono et al. 2004). Surgical procedures, carried out under aseptic conditions using isoflurane anesthesia (1.25–2.0%), were used to stereotaxically implant a titanium head stabilization post and titanium or Cilux recording chambers (Crist Instruments). In the same surgery, a scleral search coil for measuring eye movements (Fuchs and Robinson 1966) was implanted underneath the conjunctiva of one eye using the technique of Judge et al. (1980). All surgical procedures were performed in strict compliance with National Institutes of Health guidelines, and the protocols were reviewed and approved by the Institutional Animal Care and Use Committee at Emory University.
Behavioral paradigms
During all experiments, monkeys were seated in a primate chair (Crist Instruments) with their head stabilized in the horizontal stereotaxic plane. Testing was conducted in a customized room that was made completely dark. We verified this by checking for any light leaks after 
20 min of dark adaptation. Our monkeys were not able to fully dark adapt because we regularly tested large-field visual responses. We also further controlled light exposure by conducting some of our recordings while the monkey was wearing ferro-electric LCD shutter goggles (Displaytech, Longmont, CO) customized to block any stray light from the sides. In the closed state these shutter attenuate visual stimuli by 3 log units. We verified this by calibration with neutral density filters (Melles-Griot, Rochester, NY). Neurons in the MSTd were tested during visual motion and smooth pursuit. All visual stimuli were rear projected on a tangent screen 57 cm away. Visual stimuli and smooth pursuit target motion were delivered using a computer controlled two-axis mirror galvanometers (General Scanning, Watertown, MA) and appropriate optic bench optics and hardware. Stimulus motion was controlled with custom Labview software and National Instruments hardware (Austin, TX). For an MSTd neuron to be included in our study, it must have been modulated during smooth pursuit of a small diameter (0.2°) target spot moving at low frequency (0.1–0.75 Hz; ±5–10°). Step-ramp target motion conditions (Morris and Lisberger 1987; Ono et al. 2005; Rashbass 1961) were typically used for testing smooth pursuit–related neurons during blink testing (Akao et al. 2005; Mustari et al. 1988). In this paradigm, the LED laser spot was extinguished for a period 100–200 ms during step-ramp tracking. Trials with and without blinks were randomly interleaved. Well-trained monkeys continue their smooth pursuit with little or no decrement in eye velocity during the target blink (Fig. 1). To quantify the contribution of visual inputs to pursuit related responses, we measured the average response beginning 100 ms after onset of the blink and lasting for the same duration as the target blink (Newsome et al. 1988). Neurons that evinced sensitivity to horizontal smooth pursuit motion were next subjected to VOR testing. Vestibular stimulation was delivered using a 60 ft-lb servo-controlled DC torque motor (Neurokinetics, Pittsburgh, PA) that oscillated the chair about the earth vertical axis. Note that our experimental setup permitted vestibular stimulation only in yaw rotation. We used sinusoidal, horizontal whole body oscillation over a speed and frequency range (0.25–0.75 Hz; ±5°) that produced eye motion similar to those during smooth pursuit testing conditions. VOR testing was conducted in three conditions including complete darkness (VORd), during cancellation of the VOR (VORx0), and during VOR viewing an earth-stationary target against a dark background (VORx1) (Ono et al. 2004). Including VOR testing in complete darkness is essential because MSTd neurons often have sensitivity to either small- or large-field visual motion. Our VORd testing was designed to completely eliminate retinal image motion during eye movements.
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Eye movements were detected using standard electromagnetic methods using scleral search coils (Fuchs and Robinson 1966) and precision hardware (CNC Electronics, Seattle, WA). Eye movements were calibrated by requiring the monkey to fixate a stationary target at known eccentricities. Monkeys were rewarded with juice for maintaining accurate fixation (reward window, ±1.5°). Eye and target position feedback signals were processed with anti-aliasing filters at 200 Hz using 6-pole Bessel filters before digitization at 1 KHz with 16-bit precision. Velocity data were generated by digital differentiation of position data using a central difference algorithm in Matlab (Mathworks, Natick, MA). Saccades were marked with a cursor on eye velocity traces and were removed. After desaccading, the missing eye data were replaced with a linear fit connecting the pre- and postsaccadic regions of data using custom Matlab routines (Mathworks, Natick, MA). Single unit activity was recorded from neurons in MSTd using customized epoxy-coated tungsten microelectrode (Frederick-Haer, Brunswick, ME). The impedance of our electrodes was in the 1- to 3-M
range. Single-unit action potentials were detected with either a window discriminator (Bak Electronics, Mount Airy, MD) or template matching algorithm (Alpha-Omega) and were represented by an electrical pulse that was registered at high precision as an event mark in our data acquisition system (CED Power1401, Cambridge, UK). We also saved the spike train (sampled at 25 KHz) to verify the reliability of unit isolation during off-line analysis. During analysis, neuronal response was represented as a spike-density function that was generated by convolving spike times with a 5-ms Gaussian function (Richmond et al. 1987). Sensitivity of neuronal response and eye velocity during smooth pursuit was calculated as the mean firing rate in the preferred direction divided by the mean eye velocity in the same direction. Sensitivity of neuronal response and eye velocity during VORd and VORx1 was calculated as the mean firing rate in the preferred direction of smooth pursuit divided by the mean eye velocity in the same direction. Sensitivity of neuronal response and head velocity during VORx0 was calculated as the mean firing rate in the preferred direction of VORx0 divided by the mean head velocity in the same direction. Sensitivity 0.10 spike/s/°/s was taken as significant modulation (Ono et al. 2004).
Localization of the MSTd
We verified that our neurons were located in MSTd by functional (e.g., response continues during a target blink), histological (Fig. 1A) and MRI (T1-weighted, fast spin-echo; Siemens, 3T magnet) criteria. Recording chambers were stereotaxically implanted (posterior = 5 mm; lateral = 15 mm). At the conclusion of our recording experiments, animals were deeply anesthetized and perfused with physiological saline followed by 4% paraformaldehyde. Frozen sections were cut at 50 µm, and every section was mounted on microscope slides and stained for Nissl substance to allow histological reconstruction of electrode tracks.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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We specifically targeted smooth pursuit–related neurons that continued their discharge during a target blink for inclusion in this study. We recorded from 40 such smooth pursuit–related neurons in the right MSTd of three monkeys. Figure 1Ba shows a smooth pursuit–related neuron tested during step-ramp tracking. The neuron was most sensitive to smooth pursuit speed during leftward tracking. To test for the presence of an extraretinal signal, we extinguished the laser spot for a period of 200 ms during step-ramp tracking (Fig. 1Bb). We programmed the target blink to occur at the same spatial location during target motion facilitating average multiple trials. Comparison of Fig. 1B, a and b, shows that neuronal response continued during all target blinks, as did smooth pursuit. Quantitative measurement showed that the firing rate during target blink was 94.5% of the value for the same periods of the control tasks. If the neuronal response was related to retinal image motion, we would expect a significant decrement in unit response during the target blink. Figure 1C shows ratios of responses during target blink and no blink conditions for each neuron. The mean value of response ratio was 91.6 ± 14.9 (SD). Neuronal response during the blink and no blink conditions were similar, indicating that these MSTd neurons encode aspects of smooth pursuit rather than retinal image motion. The distribution of response ratios for our blink-tested neurons was similar to that described by Newsome et al. (1988) in their pioneering MSTd studies.
Response properties during horizontal smooth pursuit and horizontal VOR
Smooth pursuit neurons in MSTd also showed significant modulation during sinusoidal pursuit, with peak firing rates increasing with eye velocity in the preferred direction. Figure 2 A shows such testing for a representative neuron during three different frequencies of sinusoidal smooth pursuit (0.25, 0.5, and 0.75 Hz). Peak firing rate remained in-phase with peak eye velocity. Although neuronal response continued during the target blink for all of our MSTd neurons, none were modulated during VORd. This was the case even though VOR eye velocity was over the same speed, position, and frequency range as occurred during volitional smooth pursuit (Fig. 2B). Figure 2C plots the velocity sensitivity of the neuronal responses during horizontal pursuit (abscissa) and VORd (ordinate) for each tested neuron. None of our MSTd neurons showed significant modulation during VORd (sensitivity 0.10 spike/s/°/s).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Existence of an extraretinal signal in MSTd
All of our MSTd smooth pursuit neurons continued firing during a target blink. Newsome et al. (1988) showed that MSTd neurons carry directional extraretinal signals independent of visual inputs. Maintenance of neuronal modulation during a target blink has been accepted as evidence for the existence of an extraretinal signal. Extraretinal signals have been revealed using target blink durations of 100–400 ms in specific cortical and brain stem sites. Similarly, visual dependence of neuronal response has been revealed by observing drops in neuronal firing in association with blink testing in other neurons of the same or different sites. For example, neurons that show maintenance of neuronal discharge have been reported in MSTd (Akao et al. 2005; Newsome et al. 1988), MSTl (Ilg et al. 2004; Kawano et al. 1994; Newsome et al. 1988), area 7a (Kawano et al. 1984), frontal eye fields (Tanaka and Fukushima 1998), and dorsolateral pontine neurons (DLPN) (Mustari et al. 1988). None of these studies have defined the exact nature or source of extraretinal signals in smooth pursuit–related neurons. It seems likely that different regions may carry different extraretinal signals including ones related to proprioception, prediction, remembered target motion, and attention. Smooth pursuit–related neurons that show a clear drop in modulation during a target blink testing have been reported in MT, MSTl (Ilg et al. 2004; Newsome et al. 1988), DLPN (Mustari et al. 1988), and neurons of pretectal nucleus of the optic tract (NOT) (Das et al. 2001; Mustari and Fuchs 1990). The drop in neuronal firing rate after a target blink (while pursuit is maintained) is consistent with direction selective, foveal, and parafoveal visual sensitivity of neurons in these areas (Das et al. 2001; Mustari and Fuchs 1990; Mustari et al. 1988).
Do MSTd extraretinal signals reflect slow eye movements of different origins?
If MSTd extraretinal signals are simply caused by smooth eye movements per se, we would expect significant modulation in unit response not only during smooth pursuit but also during reflex driven eye movements, such as VORd. Similarly, if an efference copy of eye velocity was relayed through VOR-related pathways, e.g., those involving the vestibular nucleus and distal circuits, we would expect to observe some modulation of MSTd neurons during VORd. However, none of our MSTd smooth pursuit neurons showed significant modulation during VORd, even though VOR eye velocity was over the same speed as occurred during volitional smooth pursuit. Furthermore, our neurons were not well modulated during VOR in light (VORx1) where gaze was stable. This suggests that extraretinal signals of MSTd pursuit neurons are not simply caused by proprioceptive feedback or efference copy of eye movements. Rather they more likely represent smooth pursuit or gaze commands. We would argue that MSTd neurons carry a partially formed volitional smooth pursuit command or a remembered target motion in space signal (Belton and McCrea 2000). Because we only tested horizontal smooth pursuit–related MSTd neurons during yaw rotation, we cannot exclude the possibility that our neurons were sensitive to either roll or pitch vestibular stimulation. It is possible that VOR and smooth pursuit direction preferences of MSTd neurons may not be aligned. Preferred directions for translatory VOR and optic flow stimuli are often opposed (Gu et al. 2006). Optic flow dominated the response of most MSTd neurons during combined visual-vestibular testing (Gu et al. 2006). Because we only tested neurons that were strongly modulated during horizontal smooth pursuit and cancellation of the rotational VOR, we cannot be sure that we recoded from the same class of MSTd neurons as those of Gu et al. (2006). Most of our MSTd smooth pursuit neurons had large-field visual responses that were opposite in direction to the pursuit response. We know from our own and other studies that there are multiple classes of neurons in MSTd including neurons sensitive to vergence and optic flow in depth but not smooth pursuit in the frontal plane (e.g., Akao et al. 2005). Our studies focused on specific class of MSTd smooth pursuit neuron.
Absence of response in some MSTd neurons during rotational VORd
Our MSTd smooth pursuit neurons have properties that resemble horizontal gaze-velocity Purkinje cells (HGVPCs) of the flocculus, first described by Lisberger and Fuchs (1978). The defining characteristic of HGVPCs is that they are modulated during smooth pursuit and cancellation of the VOR (when eye velocity is minimal) but poorly or not at all during VORd conditions. The lack of response during VORd was attributed to the HGVPCs having equal head (vestibular) and eye velocity sensitivity that simply cancel during VORd. The suggestion that neuronal modulation of HGVPCs was related not only to eye velocity but also head velocity was reasonable. This could in fact be the case for some neurons including flocculus Purkinje cells. Our MSTd pursuit neurons also modulated during cancellation of the VOR. Neuronal modulation during cancellation of the VOR (VORx0) could be caused by at least two different mechanisms. 1) The response is caused by actual head velocity sensitivity. 2) The response reflects volitional smooth pursuit eye velocity commands needed to cancel the VOR by tracking a target that moves with the head.
Our previous studies (Mustari et al. 2003) support the second alternative. We used unilateral injections of muscimol to inactivate the DLPN and found that ipsilateral smooth pursuit was impaired as was the ability to symmetrically cancel the VOR. For example, rightward head motion produces a leftward VOR, which could be canceled by rightward smooth pursuit commands. After inactivation of the right DLPN, rightward smooth pursuit and cancellation of the VOR during rightward head movements were both impaired. However, we found that the VOR (VORd, VORx1) remained symmetric and unimpaired after unilateral DLPN inactivation (Ono et al. 2003). This was the case even though DLPN pursuit neurons were well modulated during VORx0 (Ono et al. 2004). Therefore neuronal modulation during cancellation of the VOR may not always reflect head velocity sensitivity.
Recent studies by Belton and McCrea (2000) in squirrel monkey flocculus indicate that modulation of Purkinje cells was best correlated with smooth pursuit and not head movement. They examined P-cell sensitivity to head and eye movements during VORx0 conditions and found that gaze velocity Purkinje cells were most sensitive to smooth pursuit eye movements and not head movements. Therefore it seems unlikely that the lack of modulation seen during VORd conditions, even for some floccular Purkinje cells, is caused by cancellation of equal and opposite head and eye sensitivities.
In this study, we found that MSTd neurons were modulated for the same direction of smooth pursuit and head movements (during VORx0), similar to HGVPCs. It could be that different neurons classified as gaze-velocity related actually have quite different sensitivities depending on their location in the gaze pathways. For example, we reported that smooth pursuit–related neurons in the pretectal-NOT actually were modulated for ipsiversive smooth pursuit and ipsiversive head movements during cancellation of the VOR (Mustari and Fuchs 1990). These pretectal NOT smooth pursuit neurons were not modulated during VORd. This combination of response properties could allow classification of NOT pursuit neurons as gaze related. However, target blink testing during cancellation of the VOR resulted in a drop in unit firing. These findings coupled with foveal/parafoveal visual receptive fields of pursuit-related NOT neurons are most consistent with visually contingent modulation in all smooth pursuit conditions and cancellation of the VOR. Therefore different brain regions may actually have different neuronal mechanisms underlying a pattern of modulation that could lead to classification of a neuron as gaze-velocity related. We argue that the modulation of our MSTd neurons during VORx0 may depend on volitional smooth pursuit commands for canceling the VOR. This argument is supported by our finding that eye velocity sensitivity during pursuit and head velocity sensitivity during VORx0 show high correlation (Fig. 3B).
Complimentary studies by Ilg et al. (2004) in MSTl have identified a class of smooth pursuit–related neurons that carry extraretinal signals and respond during gaze pursuit. These neurons were tested during combined smooth pursuit and whole body rotational VOR but not during VORd conditions. By using different frequencies of head and target motion and spectral analysis of neuronal firing, these investigators found that MSTl neuronal response was strongly correlated with target and not head movement. Ilg et al. (2004) argued that the neuronal response of their MSTl neurons was correlated mostly with target motion in space and not head motion.
The lack of modulation of our MSTd neurons during VORd could be explained by an absent smooth pursuit command, no vestibular or reflex driven eye velocity sensitivity. Taken together, our findings support the suggestion that extraretinal signals of MSTd pursuit neurons are related to volitional smooth pursuit commands rather than proprioceptive or other feedback signals associated with reflex driven smooth eye movements. Further studies are required to determine the source and nature of extraretinal signals in different cortical and brain stem neurons that play a role in volitional smooth pursuit.
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests and other correspondence: M. J. Mustari, Yerkes National Primate Research Ctr., Div. of Sensory-Motor Systems, Emory Univ., 954 Gatewood Rd. NE, Atlanta, GA 30322 (E-mail: mjmustar{at}rmy.emory.edu)
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REFERENCES |
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