Reprint Ss SCIENCE 15 March 1991, Volume 251, pp. 1388-1360 Movement of Neural Activity on the Superior Colliculus Motor Map During Gaze Shifts Dousias P. Munoz,” Denis PELISSON,f AND DaNiEL GUITTONt Copyright © 1991 by the American Association for the Advancement of ScienceMovement of Neural Activity on the Superior Colliculus Motor Map During Gaze Shifts Doveras P. Munoz,* Denis Péuisson,t Dantex Gurrront “The superior colliculus contains neurons that cause displacements of the visual axis (gaze shifts). ‘These cells are arranged topographically in a motor map on which the vector (amplitude and direction) of the coded movement varies continuously with location. How this spatial representation becomes a temporal code (frequency and duration) in the motoncurons is unknown, During a gaze shift, a zone of neural activity moved continuously on the map from an initial location, defining the vector of the desired gaze shift, to a final “zero” position containing neurons that were active during fixation. Thus, the spatial-temporal transformation may be accomplished by control of gaze throughout the spatial trajectory of activity on the motor map. HE MAMMALIAN SUPERIOR COLIC: ulus (SC) is a laminated neural seruc- ture that transforms sensory infor ‘mation into motor commands that rapidly move the visual axis (1). Visually responsive neurons in che superficial layers are orgar nized into a retinotopic map of visual space, subtending up t0 80° of the contralateral Og and Neronpery, coal Ores. 4801 User Mone sti Coa 38 204 ‘shoal Eye Taare, Natal Tomer of Hea Bung 1, Ropm TOOL Bethesda, MD 20882 ‘trae adie. Vision ot Mount INSERM, C94, ‘FTo'whom eorrepondehes should be aadreea Fig. 1. Mowementrelted diichages of TRNS Shown in each panel ate the gaze (0), head (FD), alee (E) postion trace, neal charge for eels Q24 (Ato B) and Q37 (Eto Hs and spike density funn {number of action portals (pic) per second ap] (12. The eeurrence Pat clon porcaval is tepreened by 2 sal ‘eral ine Additonal ssl lines superimposed ‘ontop of exhers indicate extra spies witha the Sime Sums ime bin. The prcred movements for {ell Q24 were divetes horizonally and for cll {37 were directed down to he lf ae an angie of stout 45° to te horizontal. Trees re ligne on seth ont (vere! dashed line). Aros maximum spike dens a8 visual field (2). Here we investigated the deeper layers, which aze organized into a ‘motor map (1) In the cat, che animal studied here, coor: inated eyehead movements are used 10 look at targets sicuated farther dian about 10° from center (3). Microstimulation of the deeper layers, in dhe cat whose head is A 8 — os + =e coe hn ke g ‘ : oe a E F —_/_ — =~ le SEE Ze unrestrained, elicits topographically coded sguze (gaze = eye-in-space = eye-inchead + hhead-in-space) shifts in which the vectors are predicted by the location being stimulated fon the motor map (4). This motor map is retinocopically coded and isin spacial regis ter with the overlying visual map. ‘The deeper layers contain rectoreticular ‘neurons (TRNs) that control gaze shifts via projections to contralateral brainstem re ‘ions that generate eye and head movements G). TRNS have both multimodal sensory responses (6) and movementrelated dis- charges (7-9). Many TRNs burst just before 1 gaze shift, These neurons are grouped on the motor map into a large, nearly circular zone, the center of which specifies the am- plitude and direction of the intended gaze shift. Other TRNs, located in the 2¢r0- amplicude location at the rostral pole of the 'SC, are active when the cat fxates a target and are silent during orienting gaze shifts (8, 10). Therefore, the retinotopie position of the ensemble of active TRNS ditfers if mex sured atthe start and end of a gaze shift. In ‘our experiments, we determined, in the cat, the retinotopic lncation of the active enscm. ble of neurons during a gaze shift (11) We analyzed the activity of TRNs identi- fied on the basis of their antidromic re: sponse after stimulation of the contralateral predorsal bundle (7, 8). The animal was required to make predictive gaze shifts to a spatial locus devoid of a newly appeati sensory cue, a procedure that prevented phasic visual responses fiom contaminating the movement-related neuronal activity ‘The movemencelated discharges of ewo TRNe, cells Q24 and Q37, recorded in the same cat are shown in Fig. 1, Of the wo ae SCIENCE, Vor. 251cells, Q24 was located more rostally (12) “This cell discharged in relation to all predic tive gaze shifts, made in the cell's preferred direction, that were larger than about 5° amplitude. The timing of the discharge de pended on the amplitude of movement: as gaze shife amplinade increased (10°, 17%, 40°, 80° in Fig. 1, A to D, respectively) the peak discharge occurred progressively fic ther fom the start of the gaze shift. Indeed, for 80° gaze shifts (Fig. 1D), the eell was silent at movement onset ell Q37 was most active before the 50° and 70 gaze shifts (Fig. 1, Gand H), had a weak discharge before the 25% movement (Fig. 1F), and gave only a few spikes before the 10° movement (Fig. 1E) (13). For each cel, we plotted the latency to the peak ofthe burst discharge from onset (Fig. 2A) or termination (Fig. 2B) of each gaze shift as a function of the roral amplitude of the gaze displacement. Only movements that consisted of a single-step gaze shift along the cll’ preferred direction were eon- sidered (Fig. 1). As total gaze displacement increased, the latency from the end of each sg7e shift to peak discharge remained con- stant for cell Q24 (Fig. 2B). Hence the discharge of Q24 was greatest near a fixed position of gaze relative to the target. Ie follows that the latency from movement ‘onset to peak discharge for Q24 increased with the amplitude ofthe gaze displacement (Fig, 2A} because the duration of gaze shifs rormally increases with amplitude (3). By ‘comparison, Q37 reached peak discharge at constant tency before gaze shifs in the amplitude range 30° to 80° (Fig. 2A) and therefore at decreasing (tha is, increasingly negative) latencies relative to the end of gaze shifts in thac range (Fig. 2B). Q37 was virtually silent for gaze shifts smaller than Fig. 2 (A and B) Leng rom ost (A) and end {Bho gaze ho peak dacarg oe O24 (yan G57) 2 con of ee apie suze dplsccmet Each guar repre dat from one pte sil. Negave sacs prt {ab in which peak dihatgeprecled movement about 30°, The nine TRNs that we studied n detail were clustered, functionally, into ‘wo groups: ells 1 t0 5 (including Q24) ‘were recorded in the anterior SC: (ampli- tudes les than 30° on the moror map); cells {609 (including Q37) were recorded inthe more caudal SC (amplitudes greater than 50°) (Fig. 2, D and E) ‘We also compared the instantancous fi ing frequency of each cell [using the average spike density function (11, 14)] to che cor responding value of instantaneous gaze er tor (difference between final and current 22¢ positions) for diferent amplitude gaze shifts (Fig. 2, C and F). For each eel, the curves corresponding to different gaze shifts tended «0 join a common trajectory, regard less ofthe total gaze displacement. The peak discharge for different amplitudes of move- ment was similar and was attained at a specific value of instantaneous gaze error: beeween 8° and 12° for cell Q24 and be- tween 50° and 70° for cell Q37. Comparable plots of spike density as 2 function of either instantaneous eye or head err revealed no (for the eye) or weaker (forthe head) over: laps for differen amplitude movements ay, ‘The data in Figs. 1 and 2 are inconsistent with the classic notion that vecror-tuned ‘neurons inthe SC specify initial motor error (1, 16), Rather, our results indicate that a zone of TRN activity moves across the SC of the cat during the course of an orienting ‘gue shift (17) (Fig. 2G). Immediately be fore 2 gaze shift, a zone of TRN activity is ‘established inthe caudal region of one SC at location on the mocor map that codes the initial vector error (say, 60° horiaontal) that fists between the initial postion of the visual axis and the target of interest. As the ae shift proceeds, this 2one of TRIN activ- ity moves toward the rosteal pole. ts instar {ancous location on the motor map specifics the remaining gaze error. As the gaze shift terminates (hat is, gaze error is zer0), the active zone invades the rostral pole, where fixation related TRNS are located (8, 10) Discharges similar to those of cells Q37 and Q24 would be recorded by two microele 0 10 #3 0 8 6) 7 80 0 8m Tw Gaze ampttude (469) ° ~ ts ‘0 7 % % 4 8 Go 70 fo 0m om wm 010 mw & Wo Gaze amplitude (cep) 1076 101g a Fos 7 06. . a coe £02] es 0% mm ‘Gaze eror (deg) ‘onset of gaze shit ‘ner (A) and termination (B). Liner regression analysts corelation cocficent: (A) Q24, = 090: (B) Q37, = ~0.64,(D and E) Lincar regression lines for hine TRINS in which suicient data were obtained, Corclaoa cons for lines 1 109, respectively, in (Dy 86, 0.90, 088, 0.65, 0.75, ~0.25, ~0.02,0.20, and -0.08, m(E)-7-~ 001,049,093, -061,6.28, 0.66, “0.61, ~0.63, and ~0 70. (€ and F) Plots of 24's (C) and Q37% (F) morale instantaneous Hing fiequeney 8 a fonction of insantancous gaze eror for diferent anpiuide menements song the optimal —~ sirection. Each curve was obtained by () aliging three to seven gize shi of ictal magatue on the end ‘of the gue saccade and obtaining che werage trajectory, (i) caleulating the corresponding serage spike density finction (17), which we then nocmalizd using the highest of dhe pesk value obaine i allo the til that covered ee whol ampli rg a(n ang i or ape pe dy Ron 9 mo the — ‘ght, atime thar coresponds tothe minimal delay bern 3 sd bare of tity te tccorescuospina thay and a might escclertion of gaze (8). Time implicit on eich curve: ears atthe Back cele the Start of a gaze shift and progresses from right tole (chats, owed O° gaze cron). Measurement of fn, fiequency began at the onic of gaze shifts. (G) Propose actity pattems in the TRN layer ofthe Se during, the execution ofan orincing gaze shift. Neuealacuvey (Sring frequency) is represented sctematally 252 hl - freudng rom te ewe dimesona ov sie ofthe Se rtp map The a0" of Gap te fntersctton, inthe rostral poke, ofthe horizontal and vertical meridians Each sction shows the TEN layer at nao! gaze {afer tne The Back dots mpresen hypotheses ses tht would yl das iat fo that SEs ‘observed in 37 anc Q24, respectively, No seal incended caudal Postal 15 MARCH 1991 REPORTS. 1259trodes located at the left and right black dots, respectively, on the top portion of Fig. 2G. ‘An alternative interpretation ofthe data is that a circular wave of actviy propagates radially from an origin at the initial site of activation. Our data are not compatible with this notion. There wasa lackof burst activity in TRNs located farther ftom the fixation zone than the initially active zone. For ex mpl, cell Q37 did noc burst (Fig. 1B) after the star of 10" to 15° gaze shits that Began at the SC site of Q24. Our observations suggest that a ropo- ‘graphically represented motor command is "wansformed into the temporal fring pattem that motoneurons send to muscles (the 9o- ‘alled_ spatial temporal transform). when {gaze is controlled throughout the spacial trajectory of neural activity on the motor map (18). This conclusion implies that tra- dlicional models of eolicular contol of gaze shifts need to be revised, In these models, the SC provides a command specifying only the initial vector of the intended gaze shift (1): a brainstem feedback control system is hypothesized to subtract actual gaze posi- tion from this signal, thereby yielding in stantancous gaze error, which drives the movement (19). Our results show that the SC itself spatially encodes the gaze error Therefore, the SC may reside within che ave feedback loop (3, 8, 14). This hypoth- ‘sis is supported by observations that 2 sudden increase in the discharge frequency ‘of TRN phasic bursts speeds up a gaze shit without affecting its accuracy (8). Such a finding is dificult to incorporate in traci- sional models ofthe SC, but, in @ feedback control system wherein the SC provides the crror signal, the higher velocities reduce gaze error more quickly, allowing shorter ‘movement duration while maintaining accu yy. [REFERENCES AND NOTES Sac Oe ee Me Soa ats, EA 81090000) 2 Meet etic a Soeur lf of che val Feld” Neurone a si biforaley Soto epee lee Rae, $5 «Ae eee AP 4 ccna 1 Soa oes olay Mt Ce ce eee Ses Teen dt ti «cha nt 8 Geng, tn to: SSCs CE Site kB Tae ae: Rae 338 6 188) Cee re eRe a Bo Saas, 7. Eee ee inn, Bae 368,18 tine 00 8D. Manos, tess, Mei Unni, Monee C98 gD. Gaon Rev. ewe 9 Rhee A: Ganay Dru Nar 72159 (i 8 Cran snd A Boon Esp fn er 87.419 98S) 10, B'T Minor rd Gato, Sec New. Abr. 14966198. Manors DM, Weanan HF Wor 16,1084 (198 Li Iso se shed te vere ted Atconge accrues of I ery SeaTHR Gfthae me TRNe mere sorter wie ange of pe apne why Sd de proce Uaeiae, howe te ott seen, es but sonar. dacs Meta [ic'ten decribed). Cam were waned senrat ening onemens of feet rg [ler anddieetioe An pans bac of arse ith orernion wis peenal in So of he “ries dag te pres ono ‘en moved tind the barr to roma en {her The tal smal eect the ope ‘iC were amped tage responce Ta {heanimad orev to aspal avd ofan Fetch, Guinn B. ronan tap Be a, 654 (1985) such the the ara ne 0 (te opponae sco bart i compe darks, Sint rlswere eine. To cae nc ‘target also sm many poms ao Inbeograns, wich gee a estan of te pobabt Ey ofan ion postal oretg rene bee Ts, Prove th cae for sing tras we subst ‘Esta tists, 20h efor cach spe, terebycrenting a pike pry sy to, (is) Wid ais ecttiqu, he dme of ecuene of ‘puke wa ae aman br an athe te tn ele peck war peed The Tov ich eufoveed rates he Reape apie ‘Senay fone 12 More srteror portions 08 the motor emp code {ale ase she, The servos postion 9°04 ‘es abou 1S man anor fo hat of O87. Mi ‘roimalon attests of Q24 and QB? hed 1S? and A gus ne respec ch ae le Ibe vahes redeed oh ig 3 18, Thelege range of gsc shape, ver which the datiug of OS? preded mover ona ‘Gaon of cle te cal Scand i Gut the none shareteranerof the motor apy In 18 1s. theca SC. sal ro ofthe ve mop ras ide ange arpites Col O87 seated =O" [pss Earning he proper of ell Q24 0 {G55 imps hth eso chage ae fmt of gue tis Inger han Gi the ‘Seca sang of oreo 86100 ge ‘ue wouil probly ve i std wiry Theft Untorunatewe sould met 3 or Srp greater tan 70° tae ect ly (rconcd sch ge angle ep ge to BPM seman TPM, EM Opn, RAL Ware 72,649 (1988) D'P Mme Pevon, D- Guiza, unpublished ous monty, ncuron sat bart Before asad hve Ste emcees pp and kes nin toe breton nd amt ngs ove thecal “the By compartem, or FRM al 3, ‘i ter tm on spt br an ape ‘hey harp oral pnts se Oo owes “Tr anc camge of pc tion (£257 (1 4 {he ca pred on fe acing tr oF fot thse machaiins pete ta dee sce the cath had ‘Theoret comin raed wand ring ‘roving at pero the mn map of he SCnre Tor Pa ana WMG Segh [a ath. Bop 9, 127 (1947). ‘onal tags hae been conc roles {LA Bros [in Newel Cop Re Eloi and Cv Mabburg Ee (Spine: Ver, Be a Ton pe aes, Pe Ra a. Se Gian Seo Ae 16, 1084 (1990). Pea pak, Mabonadsy 1. 58 Br Re 271,341 10983), D. Gutton RM, Douglas ‘Vo: Nesopbpol 82,1080 (1904) B. Gok. son and MWe 68, 427 1987). VT [rie and D-A Raison, Jy {Lon £375, 209 (1985). Pekizon and. Prablan, ‘Bata Re. 380, 397 (19H9), Organ J Nesp $9,997 (1988) KD Teron fn P'S Babes, 66,1588 (980, Sepals Mee ach Cama of the Fonds de Rosh oo Sane Se ‘Gute ands spend ome Monta ew. Dp fests (DFA, 10 August 190, sep 7 December 1900 ‘SCIENCE, VOL. 251