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Saccadic suppression and the dual mechanism theory of direction constancy
0042.6989 82 020335-02503.00 0 Pcrpamon Prey Lid
LET’I’ER TO THE EDITORS
SACCADIC SUPPRESSION AND THE DUAL MECHANISM THEORY OF DIRECTION CONSTANCY
(Rrceired
22 June 1981:
in r~~is~d,f~r~ 11 August 1981)
In a recent issue of this journal, Nagle ef al. (1980) described a study of visual suppression during voluntary saccades and during the saccadic movements of voluntary nystagmus. Specifically, they reported that suppression of a full-field flash was similar in the two cases (about a 0.5 log unit increase in threshold), Stability of the visual world was absent. however, during the nystagmic saccades while it was present. of course, during the ordinary ones. The dissociation between stability and suppression in voluntary nystagmus is an important and thoughtprovoking result. Contrary to the impression that might be obtained from the second paragraph of Nagle et &.‘s report, however, it does not constitute a test of the dual mechanism theory of the stable visual world that my colleagues and I have proposed (Matin. 1974, pp. 912-914). To make this clear, I will provide a brief summary of the theory and show how it bears on the dissociation phenomenon. In the dual mechanism approach to direction constancy. the first (and primary) factor is a saccade-contingent compensatory shift in the directional local signs (or perceived directions) associated with points on the retinal surface. So, for example. the perceived direction associated with stimulation of the central fovea prior to a 3’ saccade would be associated with stjmuIation of a retinal point 3’ in the periphery after the saccade if such a mechanism operated in ideal fashion. It would therefore prevent the apparent displacement of a stationary object that stimulated these two disparate points. first before, and then after, the eye movement. Experimental study of this compensatory shift showed that it occurs when saccades are made in complete darkness; it is therefore not due to retinaliy initiated (retinal) signals. The neutral term “extraretinal signal” was coined as a label for this factor in order to avoid an unnecessary commitment to either the inflow or outflow explanations of the source of the signal and to suggest the desirability of a
* In the hope of preventing possible terminological confusion. I ask the reader to note explicitly that the term “retinal signal” in this paper refers fo processes that are Miufrd by saccadic retinal stimulation. This usage does not imply an inhibitory mechanism that operates entirely at the retinal level. 33s
change from the historically popular emphasis on experiments designed to address the in~ow-out~ow controversy to an emphasis on experiments concerned with the badly neglected study of the compensatory shift per se, specifically its temporal properties (note 3 in Matin et al.. 1969a). Various experimental studies of the time-course of the compensatory shift in local signs have shown that it does not follow the time course of the ocular movement with fidelity (see Shebilske, 1977 for a recent review with extensive references to the literature). Nonetheless. the world appears stable under ordinary conditions of viewing. To account for this fact, we suggested that the saccade-contingent extraretinal process compensates for the final displacement of the eye, while a secondary mechanism, saccadic suppression, contributes to stability by preventing the perception of stimulation received in the transient period shortly before. during, and after the saccade. the time period during which gross imperfections exist in the compen~tory process. (Contrary to occasional statements in the literature, this theory clearly does not attribute the stable world to suppression per sr. Such a single factor account would be logically untenable. as has been noted in two earlier papers (Matin, 1974. p. 913; Matin. 1976. p. 113). Perhaps the matter will be put to rest if I here state more emphatically that a single factor suppression theory of direction constancy would be just plain silly: unless the compensatory extraretinal mechanism were also operating, the world would still appear displaced after the suppression ends.) When the dual mechanism theory was first proposed (Matin ef al., 1969b). I suggested a complete functional dissociation between the two processes that produce the stable visual world, although both are saccade-contingent : the compensatory shift in local signs was attributed to extraretinal signals and the suppression to retinally derived factors such as blurring and masking, which are necessary effects of saccadic retinal stimulation (the characteristic, very complex shifting of the retinal image that results from a saccadic movement).* The notion that suppression is entirely due to retinal factors was discarded when further evidence showed it to be untenable. Particularly persuasive information about the existence of
; i(,
Lcttcr
to the EdItor\
st,me cxtrarctlnal suppression factor (in addition to rhe predominantly retinal ones) was provided in an elegant stud) b) Riggs ~‘t trl. I1973). who showed suppress~on of phosphcnes when saccudes were made in cffcctivelq complete darkness condition\ that rcmovc an) possible contammation by retinal lnilurncc~. While the evidence from Riggs (‘t rrl. and others about an extrarctinal suppression factor was conclusILL. their tindings certainly did not permit an equation 01 this factor \\lth the particular extraretinal signal (hat products the compensator\, shift in r-ctinal local signs; thei,- experimental procedures simply had no hearing on the latter question. Nor has such an equation been treated as a foregone conclusion in any of my writings. Indeed. in at least one cast. I noted specifically that the possibility of such a linkage continues to remain an open question (Matin. 1976. p. 117). It seems probable that the confusion this note is intended to clarify arises from misconceptions with regard to the latter point. If the dual mechanism theory had equated saccadic suppression as a whole+ with the part of suppression that is not retinally derived. and if it had. in addition. equated the latter with the compensatory extraretinal signal. the evldcnce in Nagle r’r ct/.‘s report would be in conflict with it. Because neither of these cquatlons were ever made. however. their data arc lrrclevant to the theor). The) stand as a very important contrlhution in their own right. howcl,er. Assuming that cyc movements in voluntary nystagmus arc saccadic: and that Nagle cv 01. \\ ere successful in remo\ ing all retinal suppression
t In an earlier analysis of the Ilterature. suppression was treated as (III>’decrease in visual sensltivitj during a saccadr or in its immediate temporal tlcmtty (Matin. 1974) Thts terminology differed from the ImplIed (although not usually explicitly stated) usage of most previous ureters. v, ho tended to reserve the term for what is herein called cxtrarctinal suppressIon. The broader defimtion. which clearly identifies extraretlnal suppresston as a subset of a larger set of saccade-related “crabure” mechanism5 cont~nu?\ to stem prcferahlc. I’nfortunatel!. however. the carlter paper did not address the defimtlonal questton explicitly. with the result that the word “suppresslon” 1s ~OH sometlmcs used in the broad sense that I advocate and tometImes in the narrow one.
factors. their data provide the first (and to this date. the only) evidence that the extraretinal factor III supprcssion is not the compensator! signal (also extraretinal) that is responsible for the shifts in dlrcctronal local signs. .4(,~,1~,~~/rdyc,mer1r.s This work was supported bq rcbearch grant EYO2951 from the National Eye Institute. Natlonnt Institutes of Health. U.S.A.
El-HI
1. fblAIl\
REFERENCES
Matin E. (1974) Saccadlc suppression: a review and an analysis. Psycho/. Rev. 81, 899.-917. Matin E. (1976) Saccadic suppression and the stable world. In EJC ,Morcmmrs und Psychological Procrssr.~ (Edited by Monty R. and Senders J.). Ertbaum, New Jersey. Matin L.. Matin E. and Pearce D. (1969a) Visual perception of direction when voluntary saccades occur. I. Relation of visual direction of a fixation target exttngulshed before a saccade to a Rash presented during the saccade. Pcrwpt. Psychoph~s. 5. 65~ 80. Matin E.. Matin L.. Poia J. and Kowat K. (1969b) The intermittent light illusion and constancy of visual direction during voluntary saccades. Paper presented at the meetings of the Psychonomic Society. Nagle M.. Bridgeman B. and Stark L. (1980) Voluntary nystagmus. saccadic suppression. and stabilization of the vlsuat world. l’ision Rrs. 20, 717~-721. Riggs L.. Merton P. and Morton H. (1974) SuppressIon of visual phosphenes during saccadic eye movements. I’ision Rrs. 14, 997. 1011. Shebitske W. (1977)Visuomotor coordmation m visual dlrection and position constancies. In Stabi/it!. md C’r~v-
ytmc)’
in I/i.sw/
Perceprion:
,Muchani.snts
cmd Proc~tzvw
Wiley. New York. Shutts W.. Stark L.. Hovt W. and Ochs A. (1977) Normal (Edited
by Epstein
saccadic f/70/. 95. Stark L.. Kenyon saccadic:
W.):
structure of voluntary nystagmus. .-1r~-il\ Oplll399- 1404. Shutts W.. Ciufredda K.. Hoyt W.. Hsu R . R. and Ochs A. (1977) Voluntary nystagmus is evidence from motor and sensory mechamsms. Proc,eel/itfy\ of tile I (j 77Joinf 4ulonl~rfic’ Ctrnrrr~l Cofr/~vL’!,C(‘. pp. l-$1& 1414.
LET’I’ER TO THE EDITORS
SACCADIC SUPPRESSION AND THE DUAL MECHANISM THEORY OF DIRECTION CONSTANCY
(Rrceired
22 June 1981:
in r~~is~d,f~r~ 11 August 1981)
In a recent issue of this journal, Nagle ef al. (1980) described a study of visual suppression during voluntary saccades and during the saccadic movements of voluntary nystagmus. Specifically, they reported that suppression of a full-field flash was similar in the two cases (about a 0.5 log unit increase in threshold), Stability of the visual world was absent. however, during the nystagmic saccades while it was present. of course, during the ordinary ones. The dissociation between stability and suppression in voluntary nystagmus is an important and thoughtprovoking result. Contrary to the impression that might be obtained from the second paragraph of Nagle et &.‘s report, however, it does not constitute a test of the dual mechanism theory of the stable visual world that my colleagues and I have proposed (Matin. 1974, pp. 912-914). To make this clear, I will provide a brief summary of the theory and show how it bears on the dissociation phenomenon. In the dual mechanism approach to direction constancy. the first (and primary) factor is a saccade-contingent compensatory shift in the directional local signs (or perceived directions) associated with points on the retinal surface. So, for example. the perceived direction associated with stimulation of the central fovea prior to a 3’ saccade would be associated with stjmuIation of a retinal point 3’ in the periphery after the saccade if such a mechanism operated in ideal fashion. It would therefore prevent the apparent displacement of a stationary object that stimulated these two disparate points. first before, and then after, the eye movement. Experimental study of this compensatory shift showed that it occurs when saccades are made in complete darkness; it is therefore not due to retinaliy initiated (retinal) signals. The neutral term “extraretinal signal” was coined as a label for this factor in order to avoid an unnecessary commitment to either the inflow or outflow explanations of the source of the signal and to suggest the desirability of a
* In the hope of preventing possible terminological confusion. I ask the reader to note explicitly that the term “retinal signal” in this paper refers fo processes that are Miufrd by saccadic retinal stimulation. This usage does not imply an inhibitory mechanism that operates entirely at the retinal level. 33s
change from the historically popular emphasis on experiments designed to address the in~ow-out~ow controversy to an emphasis on experiments concerned with the badly neglected study of the compensatory shift per se, specifically its temporal properties (note 3 in Matin et al.. 1969a). Various experimental studies of the time-course of the compensatory shift in local signs have shown that it does not follow the time course of the ocular movement with fidelity (see Shebilske, 1977 for a recent review with extensive references to the literature). Nonetheless. the world appears stable under ordinary conditions of viewing. To account for this fact, we suggested that the saccade-contingent extraretinal process compensates for the final displacement of the eye, while a secondary mechanism, saccadic suppression, contributes to stability by preventing the perception of stimulation received in the transient period shortly before. during, and after the saccade. the time period during which gross imperfections exist in the compen~tory process. (Contrary to occasional statements in the literature, this theory clearly does not attribute the stable world to suppression per sr. Such a single factor account would be logically untenable. as has been noted in two earlier papers (Matin, 1974. p. 913; Matin. 1976. p. 113). Perhaps the matter will be put to rest if I here state more emphatically that a single factor suppression theory of direction constancy would be just plain silly: unless the compensatory extraretinal mechanism were also operating, the world would still appear displaced after the suppression ends.) When the dual mechanism theory was first proposed (Matin ef al., 1969b). I suggested a complete functional dissociation between the two processes that produce the stable visual world, although both are saccade-contingent : the compensatory shift in local signs was attributed to extraretinal signals and the suppression to retinally derived factors such as blurring and masking, which are necessary effects of saccadic retinal stimulation (the characteristic, very complex shifting of the retinal image that results from a saccadic movement).* The notion that suppression is entirely due to retinal factors was discarded when further evidence showed it to be untenable. Particularly persuasive information about the existence of
; i(,
Lcttcr
to the EdItor\
st,me cxtrarctlnal suppression factor (in addition to rhe predominantly retinal ones) was provided in an elegant stud) b) Riggs ~‘t trl. I1973). who showed suppress~on of phosphcnes when saccudes were made in cffcctivelq complete darkness condition\ that rcmovc an) possible contammation by retinal lnilurncc~. While the evidence from Riggs (‘t rrl. and others about an extrarctinal suppression factor was conclusILL. their tindings certainly did not permit an equation 01 this factor \\lth the particular extraretinal signal (hat products the compensator\, shift in r-ctinal local signs; thei,- experimental procedures simply had no hearing on the latter question. Nor has such an equation been treated as a foregone conclusion in any of my writings. Indeed. in at least one cast. I noted specifically that the possibility of such a linkage continues to remain an open question (Matin. 1976. p. 117). It seems probable that the confusion this note is intended to clarify arises from misconceptions with regard to the latter point. If the dual mechanism theory had equated saccadic suppression as a whole+ with the part of suppression that is not retinally derived. and if it had. in addition. equated the latter with the compensatory extraretinal signal. the evldcnce in Nagle r’r ct/.‘s report would be in conflict with it. Because neither of these cquatlons were ever made. however. their data arc lrrclevant to the theor). The) stand as a very important contrlhution in their own right. howcl,er. Assuming that cyc movements in voluntary nystagmus arc saccadic: and that Nagle cv 01. \\ ere successful in remo\ ing all retinal suppression
t In an earlier analysis of the Ilterature. suppression was treated as (III>’decrease in visual sensltivitj during a saccadr or in its immediate temporal tlcmtty (Matin. 1974) Thts terminology differed from the ImplIed (although not usually explicitly stated) usage of most previous ureters. v, ho tended to reserve the term for what is herein called cxtrarctinal suppressIon. The broader defimtion. which clearly identifies extraretlnal suppresston as a subset of a larger set of saccade-related “crabure” mechanism5 cont~nu?\ to stem prcferahlc. I’nfortunatel!. however. the carlter paper did not address the defimtlonal questton explicitly. with the result that the word “suppresslon” 1s ~OH sometlmcs used in the broad sense that I advocate and tometImes in the narrow one.
factors. their data provide the first (and to this date. the only) evidence that the extraretinal factor III supprcssion is not the compensator! signal (also extraretinal) that is responsible for the shifts in dlrcctronal local signs. .4(,~,1~,~~/rdyc,mer1r.s This work was supported bq rcbearch grant EYO2951 from the National Eye Institute. Natlonnt Institutes of Health. U.S.A.
El-HI
1. fblAIl\
REFERENCES
Matin E. (1974) Saccadlc suppression: a review and an analysis. Psycho/. Rev. 81, 899.-917. Matin E. (1976) Saccadic suppression and the stable world. In EJC ,Morcmmrs und Psychological Procrssr.~ (Edited by Monty R. and Senders J.). Ertbaum, New Jersey. Matin L.. Matin E. and Pearce D. (1969a) Visual perception of direction when voluntary saccades occur. I. Relation of visual direction of a fixation target exttngulshed before a saccade to a Rash presented during the saccade. Pcrwpt. Psychoph~s. 5. 65~ 80. Matin E.. Matin L.. Poia J. and Kowat K. (1969b) The intermittent light illusion and constancy of visual direction during voluntary saccades. Paper presented at the meetings of the Psychonomic Society. Nagle M.. Bridgeman B. and Stark L. (1980) Voluntary nystagmus. saccadic suppression. and stabilization of the vlsuat world. l’ision Rrs. 20, 717~-721. Riggs L.. Merton P. and Morton H. (1974) SuppressIon of visual phosphenes during saccadic eye movements. I’ision Rrs. 14, 997. 1011. Shebitske W. (1977)Visuomotor coordmation m visual dlrection and position constancies. In Stabi/it!. md C’r~v-
ytmc)’
in I/i.sw/
Perceprion:
,Muchani.snts
cmd Proc~tzvw
Wiley. New York. Shutts W.. Stark L.. Hovt W. and Ochs A. (1977) Normal (Edited
by Epstein
saccadic f/70/. 95. Stark L.. Kenyon saccadic:
W.):
structure of voluntary nystagmus. .-1r~-il\ Oplll399- 1404. Shutts W.. Ciufredda K.. Hoyt W.. Hsu R . R. and Ochs A. (1977) Voluntary nystagmus is evidence from motor and sensory mechamsms. Proc,eel/itfy\ of tile I (j 77Joinf 4ulonl~rfic’ Ctrnrrr~l Cofr/~vL’!,C(‘. pp. l-$1& 1414.