Skip to main content
SpringerLink
Log in

Orienting of attention and eye movements

  • Original Paper
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

According to the premotor theory of attention, the mechanisms responsible for spatial attention and the mechanisms involved in programming ocular saccades are basically the same. The aim of the present experiments was to test this claim. In experiment 1 subjects were presented with a visual display consisting of a fixation point and four boxes arranged horizontally and located above the fixation cross. Two of the boxes were in the left visual hemifield, two in the right. A fifth box was located on the vertical meridian below the fixation cross. Digit cues indicated in which of the upper boxes the imperative stimulus was most likely to appear. Subjects were instructed to direct attention to the cued box and to perform a saccadic eye movement to the lower box on presentation of the imperative stimulus. The trajectory of the saccades deviated contralateral to the hemifield in which the imperative stimulus was presented. This deviation was larger when the hemifield where the imperative stimulus was presented was the cued one. In experiment 2, the visual display consisted of five boxes forming a cross. The central box served as a fixation point. The cue was a small line, linked to the central box, pointing to different directions and indicating where the visual imperative stimulus would appear. In 50% of trials, the imperative stimulus was a visual stimulus presented either in one of the lateral boxes or in the central one. In the remaining 50% of trials, the imperative stimulus was a non-lateralised sound. Half the subjects were instructed to make a saccade to the upper box at the presentation of the visual imperative stimulus and to the lower box at the presentation of the acoustic stimulus. Half the subjects received the opposite instructions. The results confirmed that the saccades deviate contralateral to the hemifield of stimulus presentation in the case of visual imperative stimuli. Most importantly, they showed that the saccades deviate contralateral to the cued hemifield, also in the case of acoustic imperative stimuli. Experiment 3 was similar to experiment 2. It confirmed the results of that experiment and showed that slow ocular drifts, which are observed in the time interval between cue and imperative stimulus presentation, cannot explain the ocular deviations. Taken together, the experiments demonstrate that spatial attention allocation leads to an activation of oculomotor circuits, in spite of eye immobility.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Andersen RA (1987) The role of the inferior parietal lobule in spatial perception and visual-motor integration. In: Plum F, Mountcastle VB, Geiger SR (eds) Higher functions of the brain. (Handbook of physiology, vol 5, The nervous system) American Physiological Society, Bethesda, MD

    Google Scholar 

  • Aslin RN, Shea SL (1987) The amplitude and angle of saccades to double-step target displacements. Vision Res 27:1925–1942

    CAS  PubMed  Google Scholar 

  • Bach M, Bouis D, Fischer B (1983) An accurate and linear infrared oculometer. J Neurosci Methods 9:9–14

    Google Scholar 

  • Becker W (1989) Metrics. In: Wurtz RH, Goldberg ME (eds) Reviews of oculomotor research, vol 3. Neurobiology of saccadic eye movements. Elsevier, Amsterdam, pp 13–67

    Google Scholar 

  • Becker W, Jurgens R (1979) An analysis of the saccadic system by means of double step stimuli. Vision Res 19:967–983

    Article  CAS  PubMed  Google Scholar 

  • Bruce CJ (1990) Integration of sensory and motor signals in primate frontal eye fields. In: Edelman GM, Gall WE, Cowan WM (eds) From signal to sense: local and global order in perceptual maps, Wiley-Liss, New York, pp 261–314

    Google Scholar 

  • Dassonville P, Schlag J, Schlag-Rey M (1992) The frontal eye field provides their goal of saccadic eye movement. Exp Brain Res 89:300–310

    Google Scholar 

  • Doma H, Hallett PE (1988) Dependence of saccadic eye-movements on stimulus luminance, and an effect of task. Vision Res 28:915–924

    Google Scholar 

  • Downing CJ, Pinker S (1985) The spatial structure of visual attention. In: Posner MI, Marin OSM (eds) Attention and performance XI. Erlbaum, Hillsdale, NJ

    Google Scholar 

  • Duhamel J, Colby CL, Goldberg ME (1992) The updating of the representation of visual space in parietal cortex by intended eye movements. Science 255:90–92

    Google Scholar 

  • Eriksen CW, Hoffman JE (1973) The extent of processing of noise elements during selective coding from visual displays. Percept Psychophysics 14:155–160

    Google Scholar 

  • Eriksen CW, Hoffman JE (1974) Selective attention: noise suppression or signal enhancement? Bull Psychonom Soc 4:587–589

    Google Scholar 

  • Findlay JM (1982) Global visual processing for saccadic eye movements. Vision Res 22:1033–1045

    Google Scholar 

  • Fischer B, Weber H (1992) Characteristics of “anti” saccades in man. Exp Brain Res 89:415–424

    Google Scholar 

  • Fuster JM (1981) Prefrontal cortex in motor control. In: Brooks VB (ed) The nervous system. (Handbook of physiology, sect 1), American Physiological Society, Bethesda, MD, 1149–1178

    Google Scholar 

  • Guitton D, Buchtel HA, Douglas RM (1985) Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades. Exp Brain Res 58:455–472

    Google Scholar 

  • Hallett PE (1978) Primary and secondary saccades to goals defined by instructions. Vision Res 18:1279–1296

    Article  PubMed  Google Scholar 

  • Hallett PE, Adams BD (1980) The predictability of saccadic latency in a novel voluntary oculomotor task. Vision Res 20:329–339

    Article  CAS  PubMed  Google Scholar 

  • Hawkins HL, Hillyard SA, Luck SJ, Mouloua M, Downing CJ, Woodward DP (1990) Visual attention modulates signal detectability. J Exp Psychol Hum Percept Perform 16:802–811

    Google Scholar 

  • Hikosaka O, Sakamoto M, Usui S (1989a) Functional properties of monkey caudate neurons. I. Activities related to saccadic eye movements. J Neurophysiol 61:780–798

    Google Scholar 

  • Hikosaka O, Sakamoto M, Usui S (1989b) Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. J Neurophysiol 61:814–832

    Google Scholar 

  • Hikosaka O, Wurtz RH (1983a) Visual and oculomotor functions of monkey substantia nigra pars reticulata. I. Relation of visual and auditory responses to saccades. J Neurophysiol 49:1230–1253

    Google Scholar 

  • Hikosaka O, Wurtz RH (1983b) Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. J Neurophysiol 49:1285–1301

    Google Scholar 

  • Hikosaka O, Wurtz RH (1989) The basal ganglia. In: Wurtz RH, Goldberg ME (eds) Neurobiology of saccadic eye movements. (Reviews of oculomotor research, vol 3) Elsevier, Amsterdam, pp 257–281

    Google Scholar 

  • Hughes HC, Zimba LD (1985) Spatial maps of directed visual attention. J Exp Psychol Hum Percept Perform 11:409–430

    Google Scholar 

  • Hughes HC, Zimba LD (1987) Natural boundaries for the spatial spread of directed visual attention. Neuropsychologia 25:5–18

    Google Scholar 

  • Klein RM (1980) Does oculomotor readiness mediate cognitive control of visual attention? In: Nickerson RS (ed) Attention and Performance VIII. Erlbaum, Hillsdale, NJ, pp 259–276

    Google Scholar 

  • Klein RM, Kingstone A, Pontefract A (1992) Orienting of visual attention. In: Rayner K (ed) Eye movements and visual cognition: scene perception and reading. Springer, New York, pp 46–65

    Google Scholar 

  • Kowler E, Steinman RM (1979a) The effect of expectations on slow oculomotor control. I. Periodic target steps. Vision Res 19:619–632

    Google Scholar 

  • Kowler E, Steinman RM (1979b) The effect of expectations on slow oculomotor control. II. Single target displacements. Vision Res 19:633–646

    Google Scholar 

  • Milner B (1982) Some cognitive effects of frontal lobe lesions in man. Philos Trans Soc London (Biol) 298:211–226

    Google Scholar 

  • Muller HJ, Findlay JM (1987) Sensitivity and criterion effects in the spatial cuing of visual attention. Percept Psychophys 42:383–399

    Google Scholar 

  • Muller HJ, Humphreys GW (1991) Luminance-increment detection: capacity limited or not? J Exp Psychol Hum Percept Perform 17:107–124

    Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9:97–113

    Article  CAS  PubMed  Google Scholar 

  • Posner MI (1980) Orienting of attention. Q J Exp Psychol 32:3–25

    CAS  PubMed  Google Scholar 

  • Posner MI, Petersen SE (1990) The attentional system of the human brain. Ann Rev Neurosci 13:25–42

    Google Scholar 

  • Posner MI, Snyder CRR, Davidson BJ (1980) Attention and the detection of signals. J Exp Psychol Gen 109:160–174

    Article  CAS  Google Scholar 

  • Rafal RD, Calabresi PA, Brennan CW, Sciolto TK (1989) Saccade preparation inhibits reorienting to recently attended locations. J Exp Psychol Hum Percept Perform 15:673–685

    Article  CAS  PubMed  Google Scholar 

  • Reuter-Lorenz PA, Fendrich R (1992) Oculomotor readiness and covert orienting: differences between central and peripheral precues. Percept Psychophysics 52:336–344

    Google Scholar 

  • Rizzolatti G (1983) Mechanisms of selective attention in mammals. In: Ewert JP, Capranica RR, Ingle DJ (eds) Advances in vertebrate neuroethology. Plenum Press, London, pp 261–297

    Google Scholar 

  • Rizzolatti G, Camarda R (1987) Neural circuits for spatial attention and unilateral neglect. In: Jeannerod M (ed) Neurophysiological and neuropsychological aspects of spatial neglect. North Holland, Amsterdam, pp 289–313

    Google Scholar 

  • Rizzolatti G, Gallese V (1988) Mechanisms and theories of spatial neglect. In: Boiler F, Grafman J (eds) Handbook of neuropsychology, vol 1. Elsevier, Amsterdam, pp 223–246

    Google Scholar 

  • Rizzolatti G, Riggio L, Dascola I, Umilta C (1987) Reorienting attention across the horizontal and vertical meridians: evidence in favor of a premotor theory of attention. Neuropsychologia 25:31–40

    Google Scholar 

  • Rizzolatti G, Riggio L, Sheliga BM (1994) Space and selective attention. In: Umiltà C, Moscovitch M (eds) Attention and performance XV. Erlbaum, Hillsdale, NJ

    Google Scholar 

  • Robinson DA (1972) Eye movements evoked by collicular stimulation in the alert monkey. Vision Res 12:1795–1808

    Article  CAS  PubMed  Google Scholar 

  • Schiller PH, Sandell JH (1983) Interactions between visually and electrically elicited saccades before and after superior colliculus and frontal eye field ablations in the rhesus monkey. Exp Brain Res 49:381–392

    Google Scholar 

  • Schiller PH, True SD, Conway JL (1979) Paired stimulation of the frontal eye fields and the superior colliculus of the rhesus monkey. Brain Res 179:162–164

    Google Scholar 

  • Schlag J, Schlag-Rey M (1987) Does microstimulation evoke fixed-vector saccades by generating their vector or by specifying their goal? Exp Brain Res 68:442–444

    Google Scholar 

  • Schlag-Rey M, Schlag J, Dassonville P (1992) How the frontal eye field can impose a saccade goal on superior colliculus neurons. J Neurophysiol 67:1003–1005

    Google Scholar 

  • Segraves MA, Goldberg ME (1987) Functional properties of corticotectal neurons in the monkey's frontal eye field. J Neurophysiol 58:1387–1419

    Google Scholar 

  • Smit AC, van Gisbergen JA, Cools AR (1987) A parametric analysis of human saccades in different experimental paradigms. Vision Res 27:1745–1762

    Google Scholar 

  • Sparks DL, Mays LE, Porter JD (1987) Eye movements induced by pontine stimulation: interaction with visually triggered saccades. J Neurophysiol 58:300–318

    Google Scholar 

  • Tassinari G, Aglioti S, Chelazzi L, Marzi CA, Berlucchi G (1987) Distribution in the visual field of the costs of voluntarily allocated attention and of the inhibitory after-effects of covert orienting. Neuropsychologia 25:55–71

    Article  CAS  PubMed  Google Scholar 

  • Umiltà C, Riggio L, Dascola I, Rizzolatti G (1991) Differential effects of central and peripheral cues on the reorienting of spatial attention. Eur J Cogn Psychol 3:247–267

    Google Scholar 

  • Werban-Smith MG, Findlay JM (1991) Express-saccades: is there a separate population in humans? Exp Brain Res 87:218–222

    Google Scholar 

  • Wurtz RH, Mohler CW (1976) Organization of monkey superior colliculus: enhanced visual response of superficial layer cells. J Neurophysiol 39:745–765

    Google Scholar 

Download references

Author information

Author notes

  1. B. M. Sheliga

    Present address: Department of Higher Nervous Activity, Biological Faculty, Lomonosov State University, 119899, Moscow, Russia

Authors and Affiliations

  1. Istituto di Fisiologia Umana, Università di Parma, Via Gramsci 14, I-43100, Parma, Italy

    B. M. Sheliga, L. Riggio & G. Rizzolatti

Authors
  1. B. M. Sheliga
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. Riggio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. Rizzolatti
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sheliga, B.M., Riggio, L. & Rizzolatti, G. Orienting of attention and eye movements. Exp Brain Res 98, 507–522 (1994). https://doi.org/10.1007/BF00233988

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00233988

Key words

Search

Navigation