Changing Views of the Role of Superior Colliculus in the Control of Gaze

Transcription

1 Chnging Views of the Role of Superior Colliulus in the Control of Gze Neerj J. Gndhi 1 nd Dvid L. Sprks 2 1 Deprtment of Otolryngology, University of Pittsurgh, Pittsurgh, PA USA 2 Division of Neurosiene, Bylor College of Mediine Houston, TX USA Running title: Chnging views of SC role in ontrol of gze Contt uthor: Dr. Neerj J. Gndhi Deprtment of Otolryngology University of Pittsurgh Shool of Mediine 200 Lothrop Street, 108 EEINS Pittsurgh, PA Voie: (412) FAX: (412) Emil: neg8@pitt.edu Gndhi NJ nd Sprks DL. "Chnging views of the role of the superior olliulus in the ontrol of gze." In: The Visul Neurosienes, edited y L. M. Chlup nd J. S. Werner. pp , 2004.

2 Gndhi & Sprks Pge 2 Chnging views of the role of the superior olliulus in the ontrol of gze Introdution Loted t the interfe etween sensory nd motor proessing, the superior olliulus (SC) serves s useful model system for studying numer of importnt prolems in integrtive neurosiene. Bsed on trditionl studies, the SC is known to ontin mps of ells responsive to sensory stimuli s well s motor mp of neurons involved in generting ommnds for sdes, short-durtion nd high pek veloity eye movements tht rpidly hnge fixtion etween meningful stimuli. Sine the lst detiled review of the ontrol of sdes y SC (Sprks nd Hrtwih-Young 1989), our view of its prtiiption in generting movements hs hnged signifintly. Advnes in understnding the role of the SC in the trnsformtion of sensory signls into ommnds for orienting movements re reviewed here nd y Wurtz & Sommer (Chpter 98). The first two prts of this hpter riefly review progress in our knowledge of the ntomil orgniztion nd oding mehnisms of the SC. Susequent setions disuss seleted ontemporry issues out olliulr prtiiption in hieving ury of sdes nd in ontrolling other oulomotor nd skeletomotor movements. Antomil orgniztion in the superior olliulus The superior nd inferior olliuli form the roof of the midrin. In mmmls the SC is omposed of 7 lternting firous nd ellulr lyers. On the sis of ntomil nd ehviorl dt, these lyers re grouped into two funtionl units: (1) superfiil nd (2) deep omprtments. The superfiil lyers (strtum zonle, strtum griseum superfiile nd strtum optium) reeive inputs devoted lmost exlusively to vision. Cells in the superfiil lyers of eh olliulus re tivted y stimuli ppering in the ontrlterl visul field nd re topogrphilly orgnized ording to reeptive field lotion (Cynder nd Bermn 1972). Neurons with reeptive fields ner the enter of the visul field re loted nteriorlly, those with reeptive fields in the periphery re loted posteriorly. Cells with reeptive fields in the upper visul field re loted medilly; those with reeptive fields in the lower visul field re loted lterlly. The perifovel representtion is enlrged with over one third of the olliulr surfe devoted to the entrl 10 deg of the visul field. The representtion of the horizontl meridin runs from nteriolterl to posteriomedil. The visul signls oserved re in retinl oordintes; ells respond to visul stimuli if, nd only if, prtiulr regions of the retin re tivted. The outputs of the superfiil lyers re primrily sending nd terminte, for the most prt, in vrious regions of the thlmus, inluding the pulvinr (see Sprks nd Hrtwih-Young (1989) for review). In ontrst, the intermedite (strtum griesum intermedium, strtum lum intermedium) nd deeper (strtum griseum profundum nd strtum lum profundum) lyers olletively, the deep lyers reeive sensory inputs of severl modlities (for exmple, visul, uditory, nd somtosensory) nd ontin neurons with motor properties. In their erly desription of SC neurons dishrging efore sdi eye movements, Wurtz nd Golderg (1972) noted tht the neurons hve movement fields, i.e., eh neuron dishrges efore or during sdes hving prtiulr rnge of diretions nd mplitudes. The size of the movement field is funtion of the mplitude of the optiml movement. Some neurons tht dishrge prior to sdes lso hve visul reeptive fields, while other neurons hve only movement fields. Neurons dishrging in response to visul stimuli nd prior to eye movements hve overlpping, ut not neessrily o-extensive movement nd reeptive fields (Wurtz nd Golderg 1972; Anderson et l. 1998). Bsed on oth neurl reording nd mirostimultion experiments in hed-restrined nimls, it hs een estlished tht sde diretion nd mplitude re topogrphilly orgnized in the deep lyers of the SC (Roinson 1972; Shiller nd Stryker 1972). Neurons dishrging prior to smll sdes re loted nteriorly nd those firing efore lrge sdes re found posteriorly. Cells ner the midline dishrge prior to movements with up omponents nd those on the lterl side dishrge mximlly efore movements with down omponents. Mirostimultion of the deep lyers produes sdi eye movement with n mplitude nd diretion similr to the optiml vetor enoded y the neurons ner the tip of the eletrode. Despite the generl orrespondene etween the motor nd the overlying sensory mps, there is no essentil funtionl linkge etween retinotopillyoded visul tivity in the superfiil lyers nd sde-relted pre-motor tivity in the deep lyers of the SC. Vigorous tivity my our in the superfiil lyers nd not e trnslted into sde-relted dishrge in underlying ells in the deep lyers. Conversely, sde-relted tivity reorded from neurons in the intermedite nd deeper lyers my not e triggered y tivity of the overlying visul neurons oding retinl error, i.e., the distne nd diretion of the trget imge from the fove. Thus, the tivity of visul neurons in the superfiil lyers is neither neessry nor suffiient to produe tivtion of sde-relted neurons in the deep lyers of the underlying olliulus (Mys nd Sprks 1980). Yet, hemil intivtion in hmster SC (Mooney et l. 1992) nd in vitro experiments in SC

3 Gndhi & Sprks Pge 3 Chnging views of the role of the superior olliulus in the ontrol of gze slies using whole-ell pth-lmp methods (Lee et l. 1997; Is et l. 1998) hve demonstrted synpti trnsmission from the superfiil to intermedite lyers. Exittory postsynpti potentils, evoked with mono- nd polysynpti ltenies, were reorded from neurons in the intermedite lyers when the overlying superfiil lyer ws stimulted. In the presene of iuulline, neurons in the intermedite lyers even exhiited urst upon stimultion of the superfiil lyers, suggesting tht the signl trnsmission is suppressed y GABAergi inhiition. The urst property of intermedite lyer neurons ws lso filitted y tivtion of niotini etylholine reeptors (Is et l. 1998). Behviorlly, the ourrene of short-lteny, express sdes inresed fter miroinjetions of the etylholinergi gonist niotine in the SC of wke, ehving monkeys (see Koyhsi et l. (2001) for review). Thus, this interlminr iruitry my ply ritil role in reduing sdi retion time nd triggering express sdes, whih re sent following ltion of the SC (Shiller et l. 1987). A desription of SC prtiiption underlying sdi initition hs een reviewed reently (Munoz et l. 2000; see Sprks et l. (2000) for slightly different perspetive). Unlike the inter-lminr orgniztion, the neurons within the deep lyers likely use lol exittion nd distnt inhiition mehnisms to shpe the evolution of the popultion tivity tht leds to the genertion of eh sde. The eletrophysiologil (MIlwin 1982; Munoz nd Istvn 1998) nd phrmophysiologil (Meredith nd Rmo 1998; Pettit et l. 1999) experiments tht provide redene for suh onnetivity monitored extrellulr tivity while stimultion pulses were delivered to different prts of the olliulr mp. Thus, introlliulr onnetions likely shpe the sptil nd temporl profile of tivity, lthough potentil onfound my e introdued y stimultion of fiers of pssge. Before nd during eh sde, neurons in pproximtely 25-30% of the olliulr mp dishrge, nd the size of the tive re remins reltively invrint ross sdes of ll mplitudes nd diretions (MIlwin 1975; Munoz nd Wurtz 1995; Anderson et l. 1998). The SC neurons projet predominntly to rinstem strutures tht proess the olliulr ommnds to produe n pproprite movement. Popultion oding Eh SC neuron in the deep lyers dishrging prior to wide rnge of movement vetors trnsltes into lrge popultion of neurons tive efore nd during ny sde. The lrge movement field hrteristi of these ells led to popultion oding shemes for speifying the metris of the desired movement (MIlwin 1975, 1991; Sprks et l. 1976). Indeed, results of experiments in whih smll suset of the popultion of neurons tive efore sde ws reversily intivted support the hypothesis tht eh memer of the tive popultion prtiiptes in speifying the diretion nd mplitude of sde. The evidene indites tht sdi ury results from the verging of the movement tendenies produed y eh unit in the tive popultion (Lee et l. 1988; Sprks et l. 1990). Smll hnges in the diretion or mplitude of sdes re produed y slight shifts in the lotion of the popultion of tive ells within the motor mp. Thus, the lrge movement fields of olliulr neurons my ontriute to, rther thn detrt from, the ury of sdi eye movements (Bldi & Heiligenerg 1988). Beuse the ontriution of eh neuron to the diretion nd mplitude of the movement is reltively smll, the effets of vriility or noise in the dishrge frequeny of prtiulr neuron re minimized. Lesion dt inditing tht the SC is not essentil for sde genertion (Shiller et l. 1987) does not neessrily indite tht it does not ply ritil role in the initition nd exeution of sdes in norml nimls. Lrge defiits in sde ury nd lteny re oserved following reversile intivtion of SC (e.g., Hikosk nd Wurtz 1985, 1986; Lee et l. 1988; Aizw nd Wurtz 1998; Qui et l. 1988). Metris of eye movements evoked y stimultion of the frontl eye fields following intivtion of the SC lso support the hypothesis tht olliulr neurons ply n importnt role in ontrolling the diretion nd mplitude of sdes (Hnes nd Wurtz 2001). Neurons in the intermedite nd deeper lyers of SC lso exhiit lrge reeptive fields, nd popultion oding shemes my lso ontriute to the urte loliztion of sensory stimuli. Mny neurons re responsive to uditory, somtosensory or visul stimuli nd re orgnized in ntomil mps (see Stein nd Meredith (1993) for review). In nesthetized or prlyzed preprtions, the visul, somtosensory, nd uditory mps pper to e ligned, implying tht the sensory signls hve een trnslted into ommon oordinte system. Before dt from lert nimls were ville, it ws ommonly ssumed tht this lignment llowed generl, modlity independent mp of the externl environment to e formed. In suh mp, stimuli originting from prtiulr region of the externl world, regrdless of sensory modlity, would tivte prtiulr suset of multimodl neurons (neurons tht respond to visul, uditory, or ttile stimuli). The tivtion of these sensory neurons, in turn, ould initite orienting responses y exiting djent ells with movement-relted tivity orgnized in motor mp ligned with the multimodl

4 Gndhi & Sprks Pge 4 Chnging views of the role of the superior olliulus in the ontrol of gze mp of sensory spe. But, retinotopilly orgnized visul signls, ousti signls lolized in hed oordintes, nd ttile signls orgnized in ody oordintes will not e ligned when the eyes nd lims move with respet to the hed. A rempping is required to ount for hnges in the position of the relevnt effetor. For exmple, the sptil lotions of the reeptive fields of oustilly responsive ells shift with hnges in eye position. This dynmi updte of the site of oustilly driven tivity enodes the diretion nd mplitude of the movement required to look to the uditory stimulus rther thn the lotion of the trget in spe (Jy nd Sprks 1987; Pek et l. 1995; Populin nd Yin 1998). Groh nd Sprks (1996) reported tht the response of olliulr neurons to ttile stimuli ws signifintly modulted y the position of the eyes in the orits. Sensory signls in SC seem to e oding the diretion nd mplitude of the movement required to look to stimulus rther thn the lotion of tht stimulus in spe. This trnsformtion of sensory signls into motor frme of referene is neessry euse the motor mp in the superior olliulus is orgnized in reltive oordintes - the signls speify the hnge in gze position required to look to trget. Input signls tht initite movement must lso speify the lotion of the trget with respet to the urrent gze position, not the lotion of the trget in ody or hed oordintes. Inorportion of feedk signls in the SC As the short-durtion of sdes preludes visul feedk from ontriuting to their trjetory, these rpid eye movements one were onsidered llisti. However, Roinson (1975) proposed model in whih lol feedk signl enles instntneous ontrol of sdes. While his originl version hs undergone vrious revisions, the skeleton of the models hs remined the sme: orollry dishrge signl is sutrted from the desired eye movement ommnd to ompute dynmi motor error tht speifies the metris of the remining eye movement; the ongoing eye movement ontinues until the feedk drives the motor error to zero. Aording to some models (see Moshovkis et l for review), the ommnd speifying the metris of the desired eye movement origintes in the SC, the feedk signl stems from the pontomedullry retiulr formtion in the rin stem, nd the neurl omprtor performing the sutrtion resides downstrem of the SC. Therefore, the SC is in the feedforwrd pthwy of the neurl iruit ontrolling sdi eye movements. This trditionl view, however, hs een hllenged y two, non-exlusive hypotheses tht ple the SC inside the feedk loop. To mintin ontrol of sdes, one theory employs the temporl dynmis of SC neuron dishrge while the other exploits the topogrphi orgniztion of the SC. In this setion, we desrie the experiments used to support nd dispute these hypotheses. Temporl ontrol sheme Spikes were reorded s monkeys mde sdes of the optiml mplitude oded y the movement field of the isolted neuron. The spike trins were onverted into ontinuous wveform representing spike rte y onvolving eh spike with Gussin kernel nd then summing the individul signls s funtion of time (Rihmond et l. 1987). Superior olliulus neurons in the intermedite nd deeper lyers were lssified into one of three tegories sed on the level of tivity t the end of the sdi eye movement (Witzmn et l. 1991). Neurons with sde-relted ursts tht ended ompletely y sde offset were termed lipped ells. Neurons with sde-relted ursts tht delined signifintly ut mintined low level tivity fter the end of sde where onsidered prtilly lipped ells. Neurons tht filed to dishrge urst during the sde ut exhiited low-level tivity efore, during nd fter the movement were leled unlipped ells. A quntittive index indited tht SC neurons, in tulity, spred into ontinuum ross the three tegories. The dishrge rte of lipped nd prtilly lipped neurons deresed monotonilly during the sde nd, therefore, ws linerly relted to the motor error of the eye movement. This evidene led to the hypothesis tht sde dynmis re ontrolled y the dishrge profiles of the SC neurons (Witzmn et l. 1991). In this model, the lous of tivity on the SC enodes the desired eye movement nd the level of tivity represents the dynmi motor error. Thus, the sutrtion of the feedk signl from the desired movement ommnd ours t the level of the SC, pling it in the feedk loop. How roust is the orreltion etween neurl tivity nd dynmi motor error when the dynmis of sdes re ltered from their stereotypil short durtion? Interrupted sdes n e produed y stimultion of the omnipuse neurons (OPNs), whih gte the rinstem neurons tht deliver the drive to the extroulr motoneurons to produe the sde (see Moshovkis et l. (1996) for n exhustive review of rinstem physiology of the sdi system). The stimultion, triggered on the onset of sde direted to riefly flshed trget, hlted the ongoing movement in mid-flight, nd shortly fter the offset of the stimultion trin, resumed sde ws generted to ring the eyes to the lotion of the extint trget (see Keller et l. 1996). Sine the dynmi motor error remins onstnt during the interruption durtion

5 Gndhi & Sprks Pge 5 Chnging views of the role of the superior olliulus in the ontrol of gze (euse the eyes re not moving), the temporl ontrol sheme predits tht SC neurons enoding dynmi motor error should exhiit sustined dishrge rte during the interruption. To test this hypothesis, Keller nd ollegues (Keller nd Edelmn 1994; Keller et l. 2000) reorded tivity of udl SC neurons during sdes generted to the enter of the movement field ut interrupted y stimultion of the OPN region. As in the ontrol ondition, the ell exhiited premotor urst prior to the onset of movement. Stimultion of the OPN region t the onset of the sde ttenuted SC tivity, to vrious degrees in different ells, with the lrgest suppression oserved in lipped nd prtilly lipped neurons. During the interruption durtion, the tivity did not stilize t firing rte orresponding to the remining motor error. At the onset of the resumed movement, the sme neuron tive for the initil sde dishrged gin, provided tht the interruption durtion did not exeed pproximtely 100 mse; thus, for short interruption durtions, the lous of olliulr tivity ws not updted prior to the seond eye movement. The pek tivity ssoited with the seond urst ws signifintly greter thn the expeted firing rte ording to the temporl oding sheme. Also, the orreltion etween the firing rte nd motor error of the resumed movement ws weker thn for ontrol sdes. These results suggest tht lipped nd prtilly lipped neurons do not quntittively ode dynmi motor error. However, it is possile tht striter dynmi ontrol my e exerted only towrds the end of sde euse the temporl reltionship ppers stronger for the lter prt of the movement, even in the se of interrupted sdes (ompre the solid nd dotted urves in Figure 11 in Keller nd Edelmn (1994)). For lrger interruption durtions, the initil nd resumed movements ppered to e treted s two seprte sdes, s the popultion of neurons tivted for the resumed sdes ws the sme ensemle of ells tht dishrged for ontrol eye movement of the sme mplitude. Thus, the desired eye movement signl my e updted during the longer durtion interruption. Another study delivered ir puffs into the eye to pertur the sdi trjetory nd nlyzed the orresponding tivity in SC neurons (Goossens nd Vn Opstl 2000). The dynmis of the eye movements were grossly pertured. The motor error nd neurl tivity were not linerly orrelted for mny neurons, rguing ginst the temporl ontrol mehnism. The tivity of SC neurons ws lso evluted when the stereotyped trjetories of sdes were ltered y injetion of musimol in the OPN region (Soetedjo et l. 2002). The resulting sdes, lthough urte, exhiited lower pek veloity nd longer durtion. Corresponding tivity of SC neurons onsistently inresed in durtion, leding the uthors to propose tht the SC reeives feedk signl tht regultes the durtion of their dishrge. Soetedjo et l. (2002) lso nlyzed the pek dishrge rte of the SC neurons. The uthors resoned tht the pek rte of SC neurons should remin the sme for ll sdes of the sme metris nd, presumly, the sme motor error. Tht less thn hlf of the SC neurons in their smple of 11 ells showed derese in pek tivity led them to onlude tht the feedk signl does not result in olliulr neurons oding dynmi motor error. Proponents of the temporl dynmi ontrol sheme my rgue with the expettion tht olliulr firing rte should e the sme fter intivtion of OPNs. As reviewed ove, mirostimultion of OPNs produes drmti ltertions in the sptiotemporl pttern of olliulr tivity nd intivtion ould similrly modify the dishrge. A more diret test would hve een to perform phse plne nlyses of neurl tivity nd dynmi motor error. A filure to demonstrte liner reltionship, prtiulrly towrds the end of the sde, would e more onvining rgument ginst the temporl oding sheme Sptil ontrol sheme Advotes of the sptil ontrol hypothesis use different nomenlture to lssify SC ells (Munoz nd Wurtz 1995). Burst neurons reside dorslly within the deep lyers of the SC, hve irumsried movement field, nd dishrge shrp urst for sdes mde to lotions within the movement field. Buildup neurons typilly reside ventrl to the urst neurons nd generlly hve movement fields without peripherl oundry (ut see Freedmn nd Sprks 1997). Fixtion neurons onstitute n extension of the uildup lyer within the rostrl pole of SC. They exhiit low-level tivity during visul fixtion nd re silent during sdes (Munoz nd Guitton, 1989; Pek 1989; Munoz nd Wurtz 1993, 1995). The region of the fixtion neurons within the SC hs een leled the fixtion zone nd is hypothesized to inhiit the urst nd uildup neurons in the sde zone in the reminder of the SC. Aording to the sptil enoding hypothesis (Munoz et l. 1991; Munoz nd Wurtz 1995), popultion of urst nd uildup neurons within the udl SC is tive round the onset of lrge sde. As the eye movement progresses, uildup neurons rostrl to the initil site eome tivted sequentilly. It hs een hypothesized tht the neurl network in SC integrtes the eye veloity feedk signl nd shifts the popultion of tive uildup neurons rostrlly. Aording to this proposl, the lous of tivity within

6 Gndhi & Sprks Pge 6 Chnging views of the role of the superior olliulus in the ontrol of gze the uildup neuron lyer of the SC mp indites dynmi motor error, while the site of tivity of the urst neuron lyer enodes desired movement. As the tivity in the uildup lyer rehes the rostrl pole, fixtion neurons re retivted, whih in turn inhiit the sde zone of the SC s well s the premotor iruitry in the rin stem. In relity, SC neurons fll long ontinuum ording to the presdi dishrge prmeter used to lssify them into urst or uildup tegory (Anderson et l. 1988). Also, loser exmintion of the dishrge properties of the so-lled fixtion neurons (Munoz nd Wurtz 1993) revels tht they only puse during ipsiversive sdes. Mny fixtion neurons typilly dishrge presdi urst during smll ontrversive sdes generted to fixte prfovel trgets; some neurons inrese their tivity for movements s lrge s 15 deg in mplitude. Thus, the onept of the fixtion zone nd fixtion neurons hs een disputed (Gndhi nd Keller 1999). Insted, it hs een suggested tht fixtion neurons re the rostrl extension of uildup neurons nd tht the rostrl SC still onstitutes sde zone (Kruzlis et l. 1997). Alterntively, Bergeron nd Guitton (2000) proposed tht eh fixtion neuron hs hrteristi motor error, whih when rehed during movement, will resume the ell s dishrge. Consequently, some fixtion neurons will not puse for sdes smller thn prtiulr mplitude, potentilly explining the lk of puse in fixtion neurons during smll ontrversive sdes. Support for the sptil enoding model ws sed on qulittive ssessments of the popultion response of SC neurons in oth t (Munoz et l. 1991) nd monkey (Munoz nd Wurtz 1995). However, nother evlution of the evidene (Sprks 1993) nd other quntittive nlyses hve disputed the notion of systemti nd sequentil shift from udl to rostrl SC. A si requirement of this hypothesis is tht neuron must dishrge for ll sdes in the optiml diretion nd for ll mplitudes lrger thn the one ditted y its lotion within the topogrphi mp. Moreover, the loser the uildup neuron is to the rostrl end of the SC, the lter its tivtion must our reltive to sde onset (nd loser to sde end). Results of nlyses tht mesured prmeters of the neurl dishrge nd orrelted them with movement metris hve refuted the sptil enoding hypothesis (Anderson et l. 1998; Kng nd Lee 2000; Soetedjo et l. 2002). When tivity of pirs of uildup neurons, seprted on verge y over 1 mm long the rostroudl xis of the SC, ws reorded during lrge sdes (Port et l. 2000), udl to rostrl tivtion ws oserved in pproximtely hlf of the pirs; severl pirs exhiited the opposite, rostrl to udl, sequene of tivtion. This nlysis, however, ws limited to the rostroudl dimension, s it ould not determine the spred of tivity long the mediolterl extent. Exmintion of the popultion tivity in oth dimensions, ross the surfe of the SC, depits more omplited piture (Anderson et l. 1998). Ativity spred medilly, lterlly nd rostrlly during the sde; no signifint trnsition of tivity ws oserved udl to the initilly tive site. While the enter of grvity of the tivity in the uildup lyer showed smll, rostrlly direted shift y the end of the sde, the shift ws rndom, not sequentil, on mse-y-mse sis. Another study (Moshovkis et l. 2001) used [ 14 C]-deoxygluose utordiogrphy to visulize the two-dimensionl tivity in the intermedite lyers of the SC during sdes nd oserved no indition of rostrlly direted spred of tivity, lthough whether this method hs the sensitivity required to detet the proposed rostrl spred of olliulr tivity remins unler. The sptil enoding mehnism hs lso een tested y hemil intivtion experiments (Aizw nd Wurtz 1998; Qui et l. 1998). It ws resoned tht temporry intivtion y injetions of musimol to lol region of the SC would prevent or ompromise the rostrlly direted spred of tivity during lrge sdes. Thus, the ongoing sde ws predited to overshoot the trget. The oserved postlesion sdes either undershot or lnded ner the trget lotion. Thus, the notion of rostrlly direted spred of tivity s dynmi ontrol mehnism for sdes hs een refuted y mny studies. Stti feedk The two leding hypotheses of the role of SC in dynmi ontrol of sdes hve een tested extensively. Relevnt experiments hve rised vrious levels of dout out eh theory nd, onsequently, the ontroversy over dynmi role of the SC in the ontrol of sdes still exists. However, the notion of stti feedk, one tht does not ompute the instntneous motor error, hs een supported y lmost every experiment tht hs exmined the tivity of SC neurons during perturtions of the eye trjetory. Referring to the interrupted sde experiments desried ove (Keller nd Edelmn 1994; Keller et l. 2000), for exmple, the udl region tive t the onset of lrge sde dishrges nother urst t the onset of the resumed movement. If the SC does not reeive feedk out the perturtion, i.e., the SC resides upstrem of the feedk loop, seond urst would not e oserved during the resumed movement. Of ourse, the dynmis of the movement need not e ontrolled y the temporl dishrge pttern. Similr oservtions hve een mde when sdes were pertured y

7 Gndhi & Sprks Pge 7 Chnging views of the role of the superior olliulus in the ontrol of gze stimultion of ortil (frontl eye fields: Shlg-Rey et l. 1992) nd other suortil (SC: Sprks nd Porter 1983; Munoz et l. 1996) strutures. Goossens nd vn Opstl (2000) proposed oneptul model in whih the SC plys feedforwrd role in the ontrol of sdes. They found tht the numer of spikes dishrged y SC neurons during ontrol nd ir-puff-indued perturtion trils ws remrkly similr. Despite the ltered urst dynmis, SC neurons exeuted the desired numer of tion potentils. Thus, these uthors suggested tht the role of the SC is to output n pproximtely fixed numer of spikes to produe desired hnge in the line of sight. But how does the SC know tht its dishrge hs een ltered? Either non-metri sed feedk signl must e trnsmitted to the SC to ount for the hnge in urst properties (Keller nd Edelmn 1994; Soetedjo et l. 2002) or intrinsi properties within the SC ensures tht more thn enough spikes re generted nd trnsmitted to downstrem strutures (Goossens nd Vn Opstl 2000). Contriution of the SC during other orienting responses In the pst, experiments tht explored the neurophysiologil sustrte of oulomotor systems typilly investigted eh oulomotor susystem (e.g., sdes, smooth pursuit, vergene) in isoltion. In ddition, the hed ws restrined s nimls performed eye-movement tsks. In the nturl environment, however, we often orient from one trget to nother y integrting severl types of eye movements. For instne, hed movements n often ompny the eye rottion, sdes nd smooth pursuit re oordinted when trking moving ojet, nd sdi eye movements n hve vergene omponent. As reviewed ove nd elsewhere (Sprks nd Hrtwih-Young 1989), the SC is onsidered key struture in sensorimotor proesses tht ontrol sdes. More reently, the role of the SC hs een exmined during sdes oordinted with hed movements (hed-unrestrined gze shifts), eye movements other thn sdes (smooth pursuit, vergene, ommodtion), nd rehing movements of the rm. In the reminder of this hpter, we will review reent studies suggesting tht the SC is involved in the genertion of eye movements other thn sdes s well s ommnds for movements of the hed nd rm. Coordinted eye-hed movements Gze is defined s the diretion of line of sight nd is mesured s eye position in spe y omputing the sum of eye-in-hed nd hed-in-spe positions. When the hed is free to move ut the trunk is restrined in the stright-hed position, oordinted movements of the eyes nd hed shift the diretion of gze. Gze shifts re usully hrterized y the mplitudes of the gze, eye nd hed movements nd the ontriutions of the eye nd hed to the hnge in gze. The onset nd offset of gze, eye nd hed movements re typilly determined y veloity riteri. Their mplitude vlues re omputed y sutrting onset nd offset positions, nd eye nd hed ontriution metris re mesured s the eye nd hed displements, respetively, during the durtion of the gze shift (Freedmn nd Sprks 1997). In generl, the hed ontinues to move for severl hundred mse fter the end of gze shift, nd the eyes ounter-rotte in the orits during this period to mintin stility of gze. Thus, the ontriution omponent, prtiulrly for the hed movement, should e less thn the mplitude mesure. The eye nd hed ontriutions for desired hnge in gze depend on the oulomotor rnge, whih is speies-dependent, s well s the initil eye-in-hed nd hed-on-trunk positions. Beuse of their smll oulomotor rnge (~25º), ts hve higher propensity to generte hed movements nd, therefore, hve een exellent sujets for exmining the role of SC in ontrolling hed-unrestrined gze shifts. Stimultion of the SC produed effets tht were dependent on the stimultion site, stimultion prmeters nd initil position of eyes in the orits (Guitton et l. 1980; Rououx et l. 1980; Pré et l. 1994). Eletril pulses delivered to the nterior SC primrily produed sdes, even when the hed ws free to move. Hed movements, when they ourred, were initited round or fter the end of sdes, thus minimizing their ontriution to gze shifts. Thus, the hnge in gze evoked y stimultion of the nterior SC ws similr in the hed-restrined nd hed-unrestrined onditions. In ontrst, gze shifts evoked y stimultion of more udl regions of the SC produed different effets in the hed-restrined nd hed-unrestrined modes. When the hed ws prevented from moving, stimultion drove the eyes towrd speifi oritl position. Thus, oth ontrversive nd ipsiversive sdes were evoked when the initil eye position ws ipsilterl or ontrlterl, respetively, to the desired oritl position. When the hed ws llowed to move, stimultion evoked reltively onstnt mplitude gze shifts exeuted y oordinted movement of the eyes nd the hed. The eye movement in the orit, however, ppered similr to the movement oserved in the hed-restrined ondition; tht is, the eyes moved to speifi oritl positions, independent of their initil positions (Rououx et l. 1980; Pré et l. 1994). To support the mirostimultion studies, the movement fields of feline SC neurons were ompred in the hed-restrined nd hed-unrestrined onditions

8 Gndhi & Sprks Pge 8 Chnging views of the role of the superior olliulus in the ontrol of gze (Munoz et l. 1991). The neurl dishrge ws etter modulted y gze (eye-in-spe) mplitude thn either eye-in-hed or hed-in-spe omponents. Furthermore, the movement fields sed on gze prmeters overlpped for the hed-restrined nd hed-unrestrined onditions, suggesting tht the phsi ursts of SC neurons enode gze displement. Colletively, the neurl reording nd mirostimultion experiments hve led to the hypothesis tht SC enodes prmeters of the gze shift, s opposed to the eye-inhed or hed-in-spe omponents. Unlike for the non-primte models, the SC in monkeys ws trditionlly onsidered to prtiipte in the ontrol of sdes only the neurl mehnism of the hed omponent of oordinted eye nd hed movements ws thought to e of extrolliulr origin. This ssumption ws sed on studies tht exmined the effets of stimultion of the nterior SC only (Stryker nd Shiller 1975), whih primrily evoked sdes, nd ws further supported y neurl reording experiments tht filed to find hed movement signls in the SC (Roinson nd Jrvis 1974). This topi ws reently revisited (Segrves nd Golderg 1992; Cowie nd Roinson 1994; Freedmn et l. 1996; Freedmn nd Sprks 1997), nd it is now ssumed tht the primte SC lso ontrols oordinted eye-hed movements. Like the feline SC, the properties of stimultion-evoked gze shifts in nonhumn primtes were funtion of the site nd prmeters of stimultion (Freedmn et l. 1996). Gze mplitude initilly inresed with stimultion durtion nd then rehed plteu level ditted y the site of stimultion (site-speifi mximl mplitude). The pek veloity of the gze shift inresed nd the vriility in the onset deresed s the frequeny of stimultion ws rised. Inreses in the stimultion intensity hd modest effets on gze pek veloity without hnging the site-speifi mximl mplitude, provided tht the stimultion durtion ws extended to omplish the entire movement. In generl, the dynmis of stimultion-indued nd visully-guided gze shifts were similr. [Stimultion prmeters hve similr effets on sdes evoked in the hedrestrined monkey (Vn Opstl et l. 1990; Stnford et l. 1996).] The hed omponent of stimultion-evoked gze shifts ws lso dependent on the stimultion prmeters. For stimultion of middle nd udl sites, the hed ontinued to move for the durtion of the stimultion, nd even fter the end of the stimultionevoked gze shift (Freedmn et l. 1996). Presumly, the hed would hve stopped moving one it rehed the mehnil limits, lthough stimultion durtions long enough to test this hypothesis were not pplied. Hed mplitude nd durtion were linerly relted to stimultion durtion within the tested rnge. Similrly, verge hed veloity lso inresed linerly with stimultion frequeny, lthough the effet ws modest ompred to tht on gze veloity. Thus, the hed movement did not exhiit ny site-speifi mximl mplitude for the tested rnge of stimultion durtions. Even though signifint proportion of the hed movement ontinued fter gze offset, hed ontriution remined reltively independent of stimultion prmeters (Freedmn et l. 1996). Chnging the site of stimultion long the rostrl-udl dimension produed qulittively similr effets in hed-unrestrined monkey nd t. Stimultion of the nterior SC produed gze shifts tht were omplished primrily y the eye (Freedmn et l. 1996). Hed movement, if oserved, ws usully initited round gze offset nd, therefore, hed ontriution ws negligile. In ontrst, stimultion of middle nd udl regions produed oordinted movements of the eyes nd hed (Freedmn et l. 1996). Aross ll sites, however, the eye movements oserved in the hed-restrined nd hed-unrestrined onditions were similr fixed vetor for nterior sites nd gol direted for udl regions. Thus, it ppers tht the movements oserved during SC stimultion in the hed-restrined niml were redued y the mount the hed would ontriute if stimultion were pplied to the sme site in the hed-unrestrined preprtion. As onsequene, the mplitude xis of the (hedrestrined) sde motor mp, prtiulrly in the udl end, is distorted y eing more ompressed thn the mp would e if it were onstruted from hedunrestrined experiments (Freedmn et l. 1996). Anlyses evluting the effet of initil eye position in hed (IEP h ) hve deomposed the vetor of the stimultion-evoked movement nd IEP h into horizontl nd vertil omponents (Freedmn et l., 1996). Alterntively, Klier et l. (2001) trnsformed the oordinte system to nlyze the orthogonl omponent of the movement nd initil gze position (IGP). Gze mplitude, prtiulrly the horizontl omponent, evoked y stimultion remined reltively onstnt while eye nd hed ontriutions vried inversely s funtion of IEP h. [An ssessment of Figure 13A-C in Freedmn et l. (1996), however, suggests tht the gze mplitude s well s its horizontl omponent my depend on IGP.] When the IEP h ws devited in the diretion of the stimultionevoked gze shift, hed ontriution inresed nd eye mplitude deresed for given hnge in gze. Conversely, if the IEP h ws ontrlterl to the diretion of the stimultion-evoked movement, hed ontriution deresed nd eye mplitude inresed for given gze shift. Furthermore, the hed onset reltive to gze onset deresed (inresed) s the IEP h ws ipsilterl (ontrlterl) to the diretion of the ensuing

9 Gndhi & Sprks Pge 9 Chnging views of the role of the superior olliulus in the ontrol of gze gze shift. Unlike the IEP h, the effets of hed position on stimultion-evoked gze shifts nd on eye nd hed ontriutions still remin to e exmined systemtilly. Unlike the horizontl omponent, the vertil nd orthogonl omponents of the stimultion-indued gze shift were linerly relted to the vertil IEP h nd orthogonl IGP, respetively. Suppose stimultion of speifi SC site produed gze shift with n upwrd omponent when the eyes were initilly entered in the orits nd the hed ws pointed stright-hed. Stimultion of the sme site with n upwrd IEP h or IGP generted smller upwrd, nd sometimes even downwrd, omponent of gze ompred to the orresponding omponent produed with downwrd IEP h or IGP. Thus, vrying IEP h while stimulting udl site nd mintining identil stimultion prmeters does not produe gze shifts of sme mplitude nd diretion. The slope of the liner regression, desriing the reltionship etween the orthogonl gze shift omponent nd orthogonl IGP, hnged with stimultion site (Klier et l. 2001). At rostrl sites, the slope ws ner zero, inditing tht the stimultionevoked gze shifts remined onstnt ross ll IGP nd, presumly, IEP h. As the stimultion eletrode ws positioned t inresingly udl sites, the slope deresed grdully to negtive one s the stimultionevoked gze shifts eme gol-direted. The dt otined from stimultion of the rostrl nd udl ends of the SC re onsistent with the preditions of the onstnt gze-displement nd desired gzeposition models, respetively. However, Klier et l. (2001) demonstrted tht the distriution of the slopes re lso onsistent with nother model tht omputes gze displement in retinl oordintes, s opposed to sptil oordintes (see Crwford nd Guitton (1997) for theoretil foundtion). By ounting for the geometry of the eyell, ll gze shifts evoked y mirostimultion eome onstnt vetor ross ll initil gze position, therey voiding the need to explin the trnsition from gze-displement to gzeposition. Hene, the updted view is tht the SC ontrols oordinted movements of the eyes nd hed nd, furthermore, the metris of the gze shifts re enoded in retinl oordintes. These mirostimultion experiments suggest tht SC neurons issue single signl to disple gze y desired displement ( gze displement hypothesis). Alterntively, one popultion of SC neurons n provide eye displement signls nd nother group of neurons my sumit hed displement ommnds ( seprte hnnel hypothesis). If these neurons re intermingled, stimultion ould evoke gze shifts similr to those expeted from tivtion of neurons enoding gze displement. If stimultion seletively tivted eye or hed movement neurons, the movement would e isolted to just one of the pthwys. Cowie nd Roinson (1994) presented evidene hinting tht stimultion of ertin sites within the deep lyers of the SC my produe hed movements without n ompnying gze shift. Reently, Corneil nd Munoz (Soiety for Neurosiene Astrt, 763.7, 1999) reported tht stimultion of the SC with prmeters su-threshold to those required to produe gze shifts n eliit hed movements without hnging the gze position. While hed-movements evoked y stimultion of the SC support the seprte hnnel model, they re not inonsistent with the gze displement hypothesis. For exmple, the stimultion-indued output ould e gze ommnd tht ws gted y OPNs in the eye pthwy, ut not gted in the hed pthwy. To differentite etween the gze displement nd seprte hnnel hypotheses, one might suggest orrelting the neurl tivity with the metris of gze, eye nd hed omponents. However, this pproh my not e definitive for two resons. (1) Gze, eye nd hed mplitudes nd diretions do not vry independently nd typilly re highly orrelted. (2) Bsed on sles of mesurements rgument (see Sprks nd Gndhi (2002)), orreltion nlysis my not e n pproprite sttistil test for neurons orgnized in ple ode. Thus, onditions under whih the three movement metris n e dissoited, one held onstnt while the other two vry, re neessry to determine the representtion of gze in SC neurons (Freedmn nd Sprks 1997). One ehviorl dissoition (Figure 1A) emphsizes tht for lrge gze shifts, the eye mplitude sturtes t ~35 deg, even s the hed nd gze omponents vry. The shded regions in pnel B show for three representtive gze shifts (-; vertil lines pnel A nd rows in pnel B) how the enoding mehnism dittes the popultion of tive SC neurons. The gze-displement hypothesis (gze olumn, pnel B) requires tht, for gze shifts of inresingly lrger mplitudes, the tive ensemle of neurons shifts to more udl lotions. Thus, in reording from neuron with n optiml vetor lrger thn the three representtive gze shifts (lk dot, pnel B), n inrese in firing rte would e ssoited with lrger gze mplitude (gze olumn, pnel C). An inrese in firing rte is lso orrelted with n inrese in hed mplitude (hed olumn, pnel C) euse it ovries with gze mplitude. In ontrst, eye mplitude would remin reltively onstnt despite hnges in the firing rte. Aording to the seprte hnnel hypothesis, the sme popultion of neurons enoding eye displement would remin tive for ll three gze shifts, holding the shded region onstnt

10 Gndhi & Sprks Pge 10 Chnging views of the role of the superior olliulus in the ontrol of gze (eye olumn, pnel B). Hene, neuron in the udl SC would dishrge t the sme firing rte ross lrge rnge of gze nd hed mplitude, s long s the eye movement remins reltively onstnt (eye olumn, pnel C). Neurons enoding hed displement, on the other hnd, will ehve very muh like SC neurons issuing gze-displement ommnds euse hed nd gze mplitude ovry for lrge gze shifts (ompre hed nd gze olumns in pnels B nd C). Note tht while this ehviorl dissoition llows n evlution of the eye enoding sheme, it does not distinguish etween gze nd hed displements. Thus, n nlysis of only this suset of movements my not e suffiient to distinguish etween the gze-displement nd seprte-hnnel hypotheses. In the seond dissoition ondition, SC tivity is nlyzed for the suset of movements for whih the hed metris re held onstnt while eye nd gze mplitude nd diretion vry (pnel D). In this se, the popultion of neurons enoding gze or eye displements will shift for different gze shifts, ut the tive ensemle of neurons enoding hed displement will remin onstnt (pnel E). Aordingly, the firing rte of neuron enoding hed displement will not vry despite vritions in gze nd eye diretions (hed olumn, pnel F). Firing rtes of neurons enoding gze or eye displements, on the other hnd, will e relted to gze nd eye diretions, respetively, ut not to hed diretion (gze nd eye olumns, pnel F). Thus, onsidertion of only this suset of movements llows test of the heddisplement model ut it does not dissoite etween the gze nd eye displement models. In the finl dissoition ondition, gze mplitude is held onstnt while eye nd hed ontriutions vry inversely s funtion of IEP h (pnel G). In this sitution, the sme popultion of neurons enoding gze displement is tivted for the three representtive movements (gze olumn, pnel H). The neurl tivity remins onstnt for the sme gze mplitude, despite vrious omintions of eye nd hed omponents (gze olumn, pnel I). As the IEP h is devited in the diretion of the ensuing gze shift, the eye mplitude dereses nd the hed mplitude inreses. Thus, for onstnt gze mplitude, the popultion of neurons enoding eye displement nd hed displement shift their enter of tivity in opposite diretions s funtion of IEP h (eye nd hed olumns, pnel H). Consequently, the firing rte of representtive neuron enoding either eye or hed displement, while not relted to gze mplitude, would e inversely relted to eye nd hed mplitudes (eye nd hed olumns, pnel I). Freedmn nd Sprks (1997) performed these nlyses on 36 SC neurons reorded during hedunrestrined gze shifts direted to visul trgets. All neurons enoded gze displement; the reltionship with gze, eye nd hed mplitudes to firing rte oeyed the preditions of the gze displement hypothesis (gze olumn, pnels C, F nd I). Thus, these uthors onluded tht SC neurons enode desired gze displement, nd tht the single gze ommnd is seprted into eye nd hed pthwys downstrem of the SC. While the experimentl design of Freedmn nd Sprks (1997) is the most thorough nd quntittive to dte, their onlusion depends ritilly on the ssumption tht the vestiulo-oulr reflex (VOR) is intive during gze shifts. If the VOR is signifintly tive, their interprettion my e ontminted y the neurl unertinty prolem (Sprks 1999; Sprks nd Gndhi 2002). For instne, the neurons onsidered to enode desired gze displement my tully issue desire eye movement ommnd only. Other neurl pthwys my generte n ompnying hed movement nd, euse the VOR gin is ner unity, sumit n oulr ounter-rottion signl of the mount tht equls the hed mplitude. Thus, the extroulr motoneurons inorporte the exittory drive from the sdi system nd the inhiitory vestiulr signl, resulting in dissoition etween the desired (enoded y SC neurons) nd exeuted eye movement (see Sprks nd Gndhi (2002) for detils). The results of Freedmn nd ollegues (Freedmn nd Sprks 1997; Freedmn et l. 1996) n e ounted for y yet other hypotheses of the role of SC in the ontrol of gze shifts. For exmple, the SC my ontin seprte popultions of eye nd hed ells, ut ll neurons enode desired gze displement. Ativtion of either type of neuron sends signls to innervte musles in the pproprite pthwy. Downstrem of SC, the eye nd hed pthwys n intert (vi mehnisms suh rossoupling, vestiulo-oulr reflex, efferene opy, proprioeption), produing dissoition etween the desired movement ommnd nd exeuted movement mplitude (Sprks 1999). Thus, thorough understnding of olliulr prtiiption in the ontrol of gze shifts is likely to remin elusive until intertions etween the eye nd hed pthwys re eluidted. Smooth pursuit Over the pst dede the funtion of neurons in the rostrl SC hs ome under onsiderle srutiny. Aording to the trditionl views, the ells in the rostrl SC dishrge prior to smll sdes. A reent proposl tht neurons in the rostrl SC ply role in fixtion ws disussed in previous setion (Inorportion of feedk signls in the SC: Sptil

11 Gndhi & Sprks Pge 11 Chnging views of the role of the superior olliulus in the ontrol of gze ontrol sheme). In the next three setions, we onsider the possiility tht neurons in the rostrl SC prtiipte in the ontrol of eye movements other thn sdes (smooth pursuit, vergene nd ommodtion). Behviorl experiments hve demonstrted tht smll position errors (<3 deg) indued y stepping moving trget produe hnges in the speed of ongoing pursuit (Morris nd Liserger 1987; Segrves nd Golderg 1994; Kruzlis nd Miles 1996). Whether neurons in the rostrl SC generte generl position error ommnd tht n e used to produe or modify smooth eye movements ws the fous of series of experiments y Kruzlis nd ollegues (Kruzlis et l. 2000; Bsso et l. 2000). They reorded the tivity of neurons in the rostrl SC during smooth pursuit eye movements nd oserved inreses in dishrge during ontrversive pursuit movements, prtiulrly when differenes in trget nd eye speed reted smll position errors. Dereses in tivity were oserved during ipsiversive pursuit. Aordingly, one interprettion of the results is tht neurons in the rostrl SC issue ommnds used y the pursuit system. However, the sme neurons lso exhiited urst of tivity efore smll ontrversive sdes. Thus, n lterntive explntion is tht the enhned tivity oserved during pursuit eye movements ould represent the preprtion of th-up sdes smll sdes mde to the moving trget tht were not exeuted. To ddress this possiility, the tivity of ells on trils in whih th-up sdes were generted within 300 mse of the trget motion ("erly sdes") ws ompred with the tivity of the sme neuron during trils without erly sdes (Kruzlis et l., 2000). If the neurl tivity on the trils without the erly sdes reflets sde preprtion signl, higher levels of tivity should e present during the trils with erly sdes euse rpid eye movement ws tully produed. For most neurons, dishrge rte during the erly pursuit phse ws not signifintly different for the trils with nd without the erly sdes. Thus, the uthors onluded tht the enhned tivity ws ssoited with smooth pursuit, not sdes. Artifiil tivtion (mirostimultion) nd intivtion experiments were lso onduted in n ttempt to estlish more diret role of the rostrl SC in produing oulr smooth-pursuit (Bsso et l. 2000). Mirostimultion during fixtion filed to eliit ny smooth eye movements, t urrents ove or elow the threshold for evoking sdi eye movements. This is in ontrst to the smooth eye movements produed y stimultion of smll portion of the rute fundus nd neighoring posterior nk lying diretly posterior to the prinipl sulus in the frontl eye field re (MAvoy et l. 1991; Gottlie et l. 1993). Other studies, however, hve reported tht prolonged durtion, high frequeny nd lrge intensity stimultion of the SC evokes stirse of sdes, often interspersed with smooth eye movements during the intersdi intervls (Breznen et l. 1996; Missl et l. 1996; Moshovkis et l. 1998), lthough there is no onsensus whether these drift-like movements re tully smooth pursuit. The filure to initite pursuit movements with olliulr mirostimultion nnot e interpreted s evidene tht the olliulus is not involved in pursuit eye movement. Behviorl experiments hve shown tht position errors introdued y jumping moving trget only ffet ongoing pursuit movements (Morris nd Liserger 1987; Segrves nd Golderg 1994; Kruzlis nd Miles 1996). Furthermore, position steps in the diretion of motion modestly filitte pursuit while steps in the opposite diretion gretly suppress it. Thus, stimultion-indued position error signl, whih is the hypothesized output of the SC, should lter the kinemtis of pursuit even if it does not initite it. Ipsiversive pursuit should e suppressed y mirostimultion, wheres ontrversive pursuit should e filitted. Bsso et l. (2000) found tht long durtion ( mse) mirostimultion of the rostrl SC pplied ner the onset of moving trget produed lrge suppressive effets on ipsiversive smooth-pursuit; these effets were signifint nd onsistent with the preditions. The effet of mirostimultion during ontrversive smooth-pursuit ws miniml nd inonsistent. In omplementry experiment, the tivity of neurons in the rostrl SC ws redued y pplition of musimol, GABA gonist, nd pursuit performne ws ssessed s nimls trked moving trget. A step-rmp tsk ws used to ssess, independently, the effets of the diretion of the pursuit nd the lotion of the trget in the visul field. Bsso nd ollegues (Bsso et l. 2000) oserved musimol-indued redution in pursuit veloity for ontrversive pursuit initition nd n inrese in pursuit veloity during ipsiversive pursuit. However, defiits were more dependent upon whih prt of the visul field pursuit trgets were presented thn the diretion of the pursuit movement. For exmple, with right injetion, pursuit veloities were redued when the trget ws moving leftwrd in the left visul field, ut not signifintly redued when the trget ws moving leftwrd in the right visul field. Also, for the exmple of right injetion, inresed pursuit veloity ws oserved if trgets were moving rightwrd in the right visul field. Colletively, these results were interpreted s support for the hypothesis tht neurons in the rostrl SC issue generl position error ommnd tht is used y oth pursuit nd sdi susystems (Kruzlis et