Peripheral and central contributions to psychophysical spatial interactions

Won Res. Vol. 12,~~. 253-259.Pecgamm Pms 1972.

Printed in

&sat Britain.

PERIPHERAL AND CENTRAL CONTRIBUTIONS PSYCHOPHYSICAL SPATIAL INTERACTIONS

TO

ADRIANA FIORENTINI, ELLIOTT& BAYLY’ANDLAMBERTO MAIWI

Laboratorio di Ne~o~siologia de1CNR, Pisa, Italy (Received 28 February

1971;in revisedform 12 May 1971)

INTRODUCTION THE RAPIDLYincreasing knowledge of the spatial organization of the receptive fields of neurons in the retina, lateral geniculate body and visual cortex has recently renewed the interest in the perceptual phenomena of simultaneous or successive contrast. A number of recent psychophysical investigations were devoted to the study of visual contrast sensitivity with pairs of light stimuli of variable separation simulating the conditions of stimulation that are currently used in the electrophysiological analysis of the receptive field organization ~~THEIMER, 1965, 1967; FIOREN~NI and MAZZANTINI,1966; TrroHAs, 1968). This and other equivalent techniques have made apparent some si~larities between the spatial interactions that are observed psychophysically and those that occur in the receptive fields of the retinal ganglion cells of mammals. The similarity holds both for the spatial distribution of lateral interactions and for their temporal properties. As far as the interacting stimuli are presented to the same eye, however, it is impossible to know whether the effects observed psychophysi~lly reflect the properties of retinal or central mechanisms or of both. In the present work the psychophysical spatial interactions have been investigated by pairs of light stimuli that were presented either to one and the same eye or dichoptically to the two eyes. Two psychophysical functions have been tested, i.e. the contrast sensitivity for steadily illu~nated targets and the flicker sensitivity for targets that were periodically modulated in time at a fixed temporal frequency and a variable modulation depth. It will be shown that the psychophysical effects of spatial interactions between steady light stimuli are determined primarily by events occurring before binocular interaction. On the contrary, the effects of spatial interactions between time-modulated stimuli arise, at least in part, from events that take place at or beyond the site of convergence of the neural paths from the two eyes. APPARATUS AND METHOD The apparatusprovideda pair of light stimuli(a discand a concentricannulus)and a circularbackground of 3 dep dia. The disc and the annulus were obtained by illuminatina from behind two diffusing sheets screen2 by black cardboard with suitable apertures. The light sources were two glow tubes (Syl&nia R 113OB). The background was illuminated by a tungsten lamp that was suitably filtered to match the color of the glow tubes. The light beams from the disc, the annulus and the background were superimposedby half-reflecting cubes. The subject viewedthe stimuluspattern from a distanceof I.2 m. A dim light spot was assignedas a 1 Present address: Biomedical Engineering Dept., Technological Institute, Northwestern University, Evanston, Ill. 60201,U.S.A. 253

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ADRIANA FIO~INI,ELLIOTT~.BAYLYAND

LAMBERTOMAFFEI

fixation point at the same optical distance as the stimuli. The stimulus pattern appeared below the fixation spot, at an angular distance of 5 deg. The huninance of the disc and the annulus could be varied independently by photometric wedges and neutral density filters. Polarizing filters were also inserted on the beams from the disc and the annulus. The subject viewed the stimulus pattern either monoeularly (right eye) or with both eyes, through 4 mm artificial pupils and polarizing filters. The polarizing filters in front of the stimuli were adjusted to provide either monocular or dichoptic presentation of the stimulus pattern. For the dichoptic experiment the right eye viewed the disc and the left eye the annulus. For the monocular experiment both stimuli were viewed by the right eye, while the left eye was occluded. The background luminance was 5 x IOe3 cd/m*. The disc dia. was 0.2 deg for the monocular and O-3deg for the dichoptic experiments. Various annuli have been used, having different average diameters (from O-35 to 2-i deg). Three quantities were measured, both monocularly and dichoptically: (a) contrast threshold for the steadily illuminated disc either presented alone or in the presence of one of several annuli of different diameters, (b) amplitude-modulation-threshold for the disc modulated sinusaidally at a low temporal frequency, and presented alone or in the presence of a steadily illuminated annulus of variable diameter and (c) amplitude-modulation-threshold for the disc modulated as in (b) and presented together with an annulus of variable diameter that was also modulated either in phase or 180 deg out of phase with the disc. The procedure was as follows. (a) The threshold for each of the annuli was dete~in~ first by the method of adjustment. Then the luminance of the disc was adjusted to threshold by means of the photometric wedge in the presence of each of the various annuli, the luminance of which was adjusted to threshold, When the smaller annuli were presented, the subject was not required to distinguish between the disc and the annulus. He had only to adjust the disc luminance so that the total pattern (disc plus annulus) appeared just brighter than the background. Each threshold determination was preceded or followed by a control threshold determination for the disc presented alone. The monocular and the dichoptic experiments were carried out on separate sessions. The annuli used for this experiment had an approximately constant area of O-15 degZ, except for the two larger annuli (average dia. 15 and 2-l deg) the area of which was 02.5 degf. The width of the smallest annulus was 0.14 deg, that of the largest annulus 0.04 deg. The luminance of the annuli at threshold ranged between 3 x 10m3 and 9 x low3 cd/m*, the lowest threshold corresponding to the annulus of smallest diameter. (b) The amplitude-modulation-threshold for the disc (minimum modulation depth required to perceive flicker) was determined by the method of limits in the presence of each of several annuli that were steadily illu~nated. The annuli had approximately constant area of about O-25 dega and average dia. varying from 0.57 to 1.1 deg. The average luminance of the disc was 0.2 cd/m” and the modulation frequency was 1 cps for one subject (AF) and 2 cps for another subject (LM). The luminance of the annulus was equal to the average luminance of the disc (monocular and dichoptic experiment) or O-3 log units above the annulus threshold (monocular experiment). In the latter case the luminance of the smallest annulus (057 deg dia.) was about 6 x 10e3 cd/m2 and that of the largest annulus about lo-’ cd/m*. Each threshold determination was preceded or followed by a control threshold determination for the modulated disc presented alone. The monocular and dichoptic thresholds were determined during separate sessions. The monocular ex~riment was carried out by one subject (A.F.). (c) The amplitude modulation threshold for a given annulus was determined first, while the disc was steadily illuminated. Then the amplitude modulation threshold for the disc was measured in the presence of the steady annulus or with the annulus modulated with the same or the opposite phase at a modulation depth I.5 times the annulus threshold. The average luminance of the annulus was the same as the disc in the dichoptic experiment and 0.3 log units above the annulus contrast threshold in the monocular experiment. The latter was carried out by one subject (A.F.). The annuli were the same as in experiment (b). Two annuli only were used during each session. RESULTS

The contrast threshold for the steadily illuminated disc is plotted in Fig, 1 as a function of the average annulus radius. The mean threshold determined in the absence of the annulus is arbitrarily taken equal to unity. For the monocular condition the disc threshold is affected by the surroun~ng annulus. In agreement with previous results, the disc threshold is lower in the presence of small annuli and higher with wider annuli than for the disc alone. No such relation is found between the disc and the annulus when the two steady stimuli are presented dichoptically : the threshold for the disc seems to be independent of the radius of the steady annulus.

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FIG. 1. Log increment threshold for a steady disc centered at 5 deg from the fovea and surrounded by a steady annulus of liminal luminance, plotted against the average annulus radius. The threshold for the disc when presented alone is taken equal lo unity. Background luminance 5 x 10-j cd/m*. Disc dia: O-2 deg for the monocular and 0.3 deg for the dichoptic presentation. Data for two subjects. Standard errors of single experimental points (circles and crosses) range between 0.02 and 0.04 log units.

The modulation threshold for the disc in the presence of a steady annulus (Fig. 2) is found to be a function of the annulus radius both with monocular and dichoptic presentation of the stimuli. For the monocular presentation, the effects of the annulus are different, according to the annulus luminance. When the luminance of the annulus is lower than that of the disc, the modulation threshold for the disc is increased by annuli of small diameter and decreased by annuli of larger diameter. The changes of the modulation threshold are approximately symmetrical of the changes of contrast threshold reported in Fig. 1, in agreement with previous results obtained in the fovea and at 10 deg from the fovea.

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FIG. 2. Amplitude-modulation-threshold for a modulated disc surrounded by a steady armulus, expressed as a ratio to the threshold measured in the absence of the annulus. Luminance: background 5 x lo-’ cd/m’, disc (average luminance) 0.2 cd/m’, annulus: 0.2 cd/m* (full and open circles), O-3 log units above threshold (triangles) subject A.F. Standard errors of single experimental points range between 0.05 and 0.1.

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ADWNA FIORENTINI, ELLIOTTJ. BAYLYANDLAMBERTO MAFFEI

At higher annulus luminance, no facilitation of Bicker perception for the disc is produced by any annulus, but the smaller annuli produce a considerable increase of the modulation threshold. The same occurs when the annuli of higher luminance are presented dichoptica~y. Unfortunately, the annuli of lower luminance were not suitable for the dichoptic experiment: a dim annulus would be suppressed if presented dichoptically with a brighter disc. Thus the subsequent experiment with modulated annuli had to be performed with the annuli of higher average luminance. 20_

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FIG. 3. Amp~~d~modulation-typhoid for a modulated disc (O-2deg)s~round~ by a steady or modulated am&us, expressed as a ratio to the threshold measured in the absence of the annulus. Average huninances : disc O-2cd/m’, annulus 0.3 Iog units above threshold. Monocular viewing. Subject A.F. Standard errors of single experimental points range between @06 and 0.2.

The results obtained from the experiment with modulated annuli are presented in Fig. 3 for monocular viewing, and Fig. 4 for dichoptic viewing. It is apparent from the figures that with the smallest annulus a modulation in phase with the disc facilitates the perception of flicker, whereas a modulation with opposite phase impairs flicker perception. The opposite occurs with larger annuli. The effects are qualitatively the same whether the modulated annulus is presented to the same eye as the disc or to the other eye. The magnitude of the difference between the thresholds obtained with the annulus modulated in phase and out of phase is somewhat greater with monocular than with dichoptic viewing. This fact might be related to the different annulus luminances used in the two experiments. Under both conditions the differential effects of a change in phase of the modulated annulus are very conspicuous for annuli exceeding 1 deg dia. These larger annuli, if steadily illuminated, do not appreciably affect the modulation threshold of the disc. DISCUSSION in the monocular viewing conditions are qualitatively similar to previous findings relative to the fovea (FIORENTINI and MAFFEI,1970) and to the farther periphery (FIORENTINI and MAFFEI, 1968). Obviously the spatial distribution of the faciliThe results

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Peripheral and Central Contributions to Psychophysical Spatial

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FIG. 4. Amplitud~modulation-threshold for a modulated disc (O-3deg) surrounded by a steady or modulated annuhrs, expressed as a ratio to the threshold measured in the absence of the annulus. Average luminances of disc and ammlus: O-2cd/m’. Dichoptic viewing. Data for two subjects. Standard errors of single experimental points range between 0.04 and O-14. tatory and inhibitory effects varies with the retinal location for stimuli located more peripherally in the visual field.

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The previous and the present results in summary show that: (1) facilitatory (for small interstimulus distances) and inhibitory (for greater interstimulus distances) interactions occur between two steadily illuminated concentric areas of the visual field of one eye. No interaction is found with dichoptic steady stimuli (see also WESTHEIMER, 1967). (2) Dynamic interactions take place between concentric areas illuminated with time-modulated lights of low temporal frequency. The latter are also facilitator-y for small interstimulus distances and inhibitory for greater distances, as indicated by the opposite effects of in-phase and out-of-phase modulation of the two interacting stimuli. Dynamic spatial interactions can be reproduced by stimuli presented separately to the two eyes. It is generally assumed that most of the excitatory and inhibitory interactions which underlie the observed changes in psychophysical thresholds are located in the retina. And indeed there is a striking similarity between the spatial distribution of psychophysical interactions and the distribution of interactions that occur within the receptive fields of retinal ganglion cells of the cat (FIORENTINIand MAFFEI,1968, 1970). Recent experiments, however, have proved that a reorganization of the receptive fields takes place at the lateral geniculate body. The geniculate receptive fields, despite their similarity in shape and size to the receptive fields of retinal ganglion cells, are far from being a replica of the latter. A number of retinal fibers converge upon an individual geniculate neuron in such a way that a few retinal receptive field centers project to the geniculate receptive field center and other retinal centers project to the geniculate receptive field surround (MAFFEIand FIORENTINI, 1971). Because of this reorganization at the geniculate level the center-surround arrangement of retinal receptive fields cannot account for the perceived effects of spatial interactions. The present findings with dichoptic stimulus presentation indicate that the mechanisms responsible for the steady-state spatial interactions are located peripherally to the site of “IslON 1212-G

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ADRIANAFIORENTINI, ELLIOTTJ. BAYLYAND LAMBERTO MAFFEI

convergence of the visual paths from the two eyes. The lateral geniculate body could be the site of these mechanisms. The dynamic spatial interactions, on the contrary, have to be ascribed, at least in part, to mechanisms located at or beyond the site of neural binocular convergence. The cortical neurons are one of the possible sites for these effects, since the neural paths from the two eyes in primates show at this level a high degree of binocular convergence (HUBEL and WIESEL, 1968). In conclusion, the neural processes of elaboration

of visual information

the basis of contrast enhancement would be accomplished

which are at

at a relatively peripheral stage

as far as the steady components of light stimuli are concerned. The time-varying components could be handled at subsequent stages by processes that possibly reinforce each other.

REFERENCES FIORENTINI, A. and MAFPEI,L. (1968).Perceptual correlates of inhibitory and facilitatory spatial interactions

in the visual system. Vision Res. 8, 1195-1203. FIORENTINI, A. and MAFFEZ, L. (1970). Transfer characteristics of excitation and inhibition in the human visual system. J. Neurophysiol. 33,285292. FIORENTINI. A. and MAZZANTINI.L. (1966). Neural inhibition in the human fovea: a study of interactions between two line stimuli. Atti Fond. G:Ronchi 21,738-747. HUBEL,D. H. and WIESEL,T. N. (1968). Receptive fields and functional architecture of monkey striate cortex. J. Physiol., Lond. 195, 215-243. MAFFEI,L. and FIORENTIE~I, A. (1971).Retino-geniculateconvergenceand the analysisof contrast.J. Neurophysiol., in press. THOMAS,J. P. (1968). Linearity of spatial integrations involving inhibitory interactions. Vision Res. 8,49-60. W-R, G. (1965). Spatial interactionin the humanretina duringscotopic vision. J. PhysioL, Lund. 181,881-894. WESTHEIMER, G. (1967). Spatial interaction in human cone vision. J. Physiol., Lmd. 190, 139-154.

Abstract-Increment thresholds for a steady light disc and amplitude-modulation thresholds for a timemodulated disc centered at 5 deg from the fovea have been measured in the presence of an annulus of variable diameter concentric to the disc and viewed either by the same eye as the disc or by the other eye. Facilitatory and inhibitory interactions between steady stimuli are found to occur only for homolateral presentation of the stimuli, whereas spatial interactions between time-modulated stimuli occur also with dichoptic stimulus presentation.

R&m&On mesure pour un disque hnnineux cent& Z+5” de la fovka les seuils di@rentiels en lumi&e stable et les seuils d’amplitude de modulation pour une lumikre moduk temporellement, en ptince d’un anneau de diam&e variable concentrique au disque et vu soit par le m@me oeil que le disque, soit par l’autre oeil. Les interactions de facilitation et d’inhibition entre stimuli stables ne se produisent que pour une prkentation homol&rale des stimuli, tandis que les interactions spatiales entre stimuli moduUs temporellement se produisent aussi en pr&entation dichoptique.

Peripheral and Central Contributions to Psychophysical Spatial Interactions

Zusamme&smag-Unterschiedsschwellen wurden sowohl ftlr kontinuierlichdargebotene als such zeitlich modulierte Rreisscheiben in Gegenwart eines konzentrischen Ringes variablen Durchmessers5” periphergemessen.Dabei wurden der Ring und das Testzeichenentwederdem gleichen Auge oder den beiden verschiedenenAugen einzeln dargeboten. Wechselwirkungen zwischen den kontinuierlich dargebotenen Testzeichen ergaben sich nur bei homolateraler Darbiehmg, v&&rend bei den zeitlich modulierten Testzeichen sich such eine r&unliche Wechselwirkung ergab, werm die beiden Reize verschiedenenAugen dargeboten wurden.

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