Skip to main content
Log in

Target selection in eye–hand coordination: Do we reach to where we look or do we look to where we reach?

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

During a goal-directed movement of the hand to a visual target the controlling nervous system depends on information provided by the visual system. This suggests that a coupling between these two systems is crucial. In a choice condition with two or more equivalent objects present at the same time the question arises whether we (a) reach for the object we have selected to look at or (b) look to the object we have selected to grasp. Therefore, we examined the preference of human subjects selecting the left or the right target and its correlation to the action to be performed (eye-, arm- or coordinated eye–arm movement) as well as the horizontal position of the target. Two targets were presented at the same distance to the left and right of a fixation point and the stimulus onset asynchrony (SOA) was adjusted until both targets were selected equally often. This balanced SOA was then taken as a quantitative measure of selection preference. We compared these preferences at three horizontal positions for the different movement types (eye, arm, both). The preferences of the ‘arm’ and ‘coordinated eye–arm’ movement types were correlated more strongly than the preferences of the other movement types. Thus, we look to where we have already selected to grasp. These findings provide evidence that in a coordinated movement of eyes and arm the control of gaze is a means to an end, namely a tool to conduct the arm movement properly.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Andersen RA, Bracewell RM, Barash S, Gnadt JW, Fogassi L (1990) Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque. J Neurosci 10(4):1176–1196

    PubMed  CAS  Google Scholar 

  • Asanuma C, Andersen RA, Cowan WM (1985) The thalamic relations of the caudal inferior parietal lobule and the lateral prefrontal cortex in monkeys: divergent cortical projections from cell clusters in the medial pulvinar nucleus. J Comp Neurol 241(3):357–381

    Article  PubMed  CAS  Google Scholar 

  • Barbas H, Mesulam MM (1981) Organization of afferent input to subdivisions of area 8 in the rhesus monkey. J Comp Neurol 200(3):407–431

    Article  PubMed  CAS  Google Scholar 

  • Basso MA, Wurtz RH (1997) Modulation of neuronal activity by target uncertainty. Nature 389(6646):66–69

    Article  PubMed  CAS  Google Scholar 

  • Batista AP, Buneo CA, Snyder LH, Andersen RA (1999) Reach plans in eye-centered coordinates. Science 285(5425):257–260

    Article  PubMed  CAS  Google Scholar 

  • Carey DP (2000) Eye-hand coordination: eye to hand or hand to eye? Curr Biol 10(11):R416–R419

    Article  PubMed  CAS  Google Scholar 

  • Carey DP, Coleman RJ, Della Sala S (1997) Magnetic misreaching. Cortex 33(4):639–652

    PubMed  CAS  Google Scholar 

  • Cavanaugh J, Wurtz RH (2004) Subcortical modulation of attention counters change blindness. J Neurosci 24(50):11236–11243

    Article  PubMed  CAS  Google Scholar 

  • Cohen YE, Andersen RA (2000) Reaches to sounds encoded in an eye-centered reference frame. Neuron 27(3):647–652

    Article  PubMed  CAS  Google Scholar 

  • Crammond DJ, Kalaska JF (1989) Neuronal activity in primate parietal cortex area 5 varies with intended movement direction during an instructed-delay period. Exp Brain Res 76(2):458–462

    Article  PubMed  CAS  Google Scholar 

  • Findlay JM (1980) The visual stimulus for saccadic eye movements in human observers. Perception 9(1):7–21

    Article  PubMed  CAS  Google Scholar 

  • Fisk JD, Goodale MA (1985) The organization of eye and limb movements during unrestricted reaching to targets in contralateral and ipsilateral visual space. Exp Brain Res 60(1):159–178

    Article  PubMed  CAS  Google Scholar 

  • Frens MA, Erkelens CJ (1991) Coordination of hand movements and saccades: evidence for a common and a separate pathway. Exp Brain Res 85(3):682–690

    Article  PubMed  CAS  Google Scholar 

  • Fries W (1984) Cortical projections to the superior colliculus in the macaque monkey: a retrograde study using horseradish peroxidase. J Comp Neurol 230(1):55–76

    Article  PubMed  CAS  Google Scholar 

  • Fries W (1985) Inputs from motor and premotor cortex to the superior colliculus of the macaque monkey. Behav Brain Res 18(2):95–105

    Article  PubMed  CAS  Google Scholar 

  • Gescheider GA (1997) Psychophysics: the fundamentals, 3rd edn. Lawrence Erlbaum Associates, Mahwah

    Google Scholar 

  • Gielen CC, van den Heuvel PJ, van Gisbergen JA (1984) Coordination of fast eye and arm movements in a tracking task. Exp Brain Res 56(1):154–161

    Article  PubMed  CAS  Google Scholar 

  • Goodale MA, Haffenden A (1998) Frames of reference for perception and action in the human visual system. Neurosci Biobehav Rev 22(2):161–172

    Article  PubMed  CAS  Google Scholar 

  • Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15(1):20–25

    Article  PubMed  CAS  Google Scholar 

  • Goodale MA, Pelisson D, Prablanc C (1986) Large adjustments in visually guided reaching do not depend on vision of the hand or perception of target displacement. Nature 320(6064):748–750

    Article  PubMed  CAS  Google Scholar 

  • Grunewald A, Linden JF, Andersen RA (1999) Responses to auditory stimuli in macaque lateral intraparietal area. I. Effects of training. J Neurophysiol 82(1):330–342

    PubMed  CAS  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(3):455–472

    Article  PubMed  CAS  Google Scholar 

  • Horwitz GD, Newsome WT (1999) Separate signals for target selection and movement specification in the superior colliculus. Science 284(5417):1158–1161

    Article  PubMed  CAS  Google Scholar 

  • Iba M, Sawaguchi T (2003) Involvement of the dorsolateral prefrontal cortex of monkeys in visuospatial target selection. J Neurophysiol 89:587–599

    Article  PubMed  Google Scholar 

  • Lacquaniti F, Guigon E, Bianchi L, Ferraina S, Caminiti R (1995) Representing spatial information for limb movement: role of area 5 in the monkey. Cereb Cortex 5(5):391–409

    Article  PubMed  CAS  Google Scholar 

  • Lévy-Schoen A (1969) Détermination et latence de la résponse oculomotrice à deux stimulus simultanés ou successifs selon leur excentricité relative. Année Psychol 69:373–392

    Article  Google Scholar 

  • Lévy-Schoen A (1974) Le champ d’activité du regard: données expérimentales. Année Psychol 74:43–66

    Article  PubMed  Google Scholar 

  • Linden JF, Grunewald A, Andersen RA (1999) Responses to auditory stimuli in macaque lateral intraparietal area. II. Behavioral modulation. J Neurophysiol 82(1):343–358

    PubMed  CAS  Google Scholar 

  • Lunenburger L, Kutz DF, Hoffmann KP (2000) Influence of arm movements on saccades in humans. Eur J Neurosci 12(11):4107–4116

    Article  PubMed  CAS  Google Scholar 

  • Mazzoni P, Bracewell RM, Barash S, Andersen RA (1996) Spatially tuned auditory responses in area LIP of macaques performing delayed memory saccades to acoustic targets. J Neurophysiol 75(3):1233–1241

    PubMed  CAS  Google Scholar 

  • McPeek RM, Keller EL (2004) Deficits in saccade target selection after inactivation of superior colliculus. Nat Neurosci 7(7):757–763

    Article  PubMed  CAS  Google Scholar 

  • Muller JR, Philiastides MG, Newsome WT (2005) Microstimulation of the superior colliculus focuses attention without moving the eyes. Proc Natl Acad Sci USA 102(3):524–529

    Article  PubMed  CAS  Google Scholar 

  • Murata A, Gallese V, Kaseda M, Sakata H (1996) Parietal neurons related to memory-guided hand manipulation. J Neurophysiol 75(5):2180–2186

    PubMed  CAS  Google Scholar 

  • Neggers SF, Bekkering H (2000) Ocular gaze is anchored to the target of an ongoing pointing movement. J Neurophysiol 83(2):639–651

    PubMed  CAS  Google Scholar 

  • Neggers SF, Bekkering H (2002) Coordinated control of eye and hand movements in dynamic reaching. Hum Mov Sci 21(3):349–376

    Article  PubMed  CAS  Google Scholar 

  • Pashler H, Carrier M, Hoffman J (1993) Saccadic eye movements and dual-task interference. Q J Exp Psychol A 46(1):51–82

    PubMed  CAS  Google Scholar 

  • Platt ML, Glimcher PW (1998) Response fields of intraparietal neurons quantified with multiple saccadic targets. Exp Brain Res 121(1):65–75

    Article  PubMed  CAS  Google Scholar 

  • Platt ML, Glimcher PW (1999) Neural correlates of decision variables in parietal cortex. Nature 400(6741):233–238

    Article  PubMed  CAS  Google Scholar 

  • Pouget A, Deneve S, Duhamel JR (2002) A computational perspective on the neural basis of multisensory spatial representations. Nat Rev Neurosci 3(9):741–747

    Article  PubMed  CAS  Google Scholar 

  • Prablanc C, Martin O (1992) Automatic control during hand reaching at undetected two-dimensional target displacements. J Neurophysiol 67(2):455–469

    PubMed  CAS  Google Scholar 

  • Sarlegna F, Blouin J, Bresciani JP, Bourdin C, Vercher JL, Gauthier GM (2003) Target and hand position information in the online control of goal-directed arm movements. Exp Brain Res 151(4):524–535

    Article  PubMed  Google Scholar 

  • Scherberger H, Goodale MA, Andersen RA (2003) Target selection for reaching and saccades share a similar behavioral reference frame in the macaque. J Neurophysiol 89(3):1456–1466

    Article  PubMed  Google Scholar 

  • Schiller PH, Chou IH (1998) The effects of frontal eye field and dorsomedial frontal cortex lesions on visually guided eye movements. Nat Neurosci 1(3):248–253

    Article  PubMed  CAS  Google Scholar 

  • Seal J, Commenges D (1985) A quantitative analysis of stimulus- and movement-related responses in the posterior parietal cortex of the monkey. Exp Brain Res 58(1):144–153

    Article  PubMed  CAS  Google Scholar 

  • Shadlen MN, Newsome WT (1996) Motion perception: seeing and deciding. Proc Natl Acad Sci USA 93(2):628–633

    Article  PubMed  CAS  Google Scholar 

  • Snyder LH, Batista AP, Andersen RA (1997) Coding of intention in the posterior parietal cortex. Nature 386(6621):167–170

    Article  PubMed  CAS  Google Scholar 

  • Snyder LH, Batista AP, Andersen RA (1998) Change in motor plan, without a change in the spatial locus of attention, modulates activity in posterior parietal cortex. J Neurophysiol 79:2814–2819

    PubMed  CAS  Google Scholar 

  • Snyder LH, Calton JL, Dickinson AR, Lawrence BM (2002) Eye-hand coordination: saccades are faster when accompanied by a coordinated arm movement. J Neurophysiol 87(5):2279–2286

    PubMed  Google Scholar 

  • Soechting JF, Engel KC, Flanders M (2001) The Duncker illusion and eye-hand coordination. J Neurophysiol 85(2):843–854

    PubMed  CAS  Google Scholar 

  • Stricanne B, Andersen RA, Mazzoni P (1996) Eye-centered, head-centered, and intermediate coding of remembered sound locations in area LIP. J Neurophysiol 76(3):2071–2076

    PubMed  CAS  Google Scholar 

  • Stuphorn V, Bauswein E, Hoffmann KP (2000) Neurons in the primate superior colliculus coding for arm movements in gaze-related coordinates. J Neurophysiol 83(3):1283–1299

    PubMed  CAS  Google Scholar 

  • Wardak C, Olivier E, Duhamel JR (2002) Saccadic target selection deficits after lateral intraparietal area inactivation in monkeys. J Neurosci 22(22):9877–9884

    PubMed  CAS  Google Scholar 

  • Werner W (1993) Neurons in the primate superior colliculus are active before and during arm movements to visual targets. Eur J Neurosci 5(4):335–340

    Article  PubMed  CAS  Google Scholar 

  • Werner W, Dannenberg S, Hoffmann KP (1997) Arm-movement-related neurons in the primate superior colliculus and underlying reticular formation: comparison of neuronal activity with EMGs of muscles of the shoulder, arm and trunk during reaching. Exp Brain Res 115(2):191–205

    Article  PubMed  CAS  Google Scholar 

  • Wurtz RH, Goldberg ME (1971) Superior colliculus cell responses related to eye movements in awake monkeys. Science 171(966):82–84

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by a grant from the German Science Foundation (DFG) as part of the Sonderforschungsbereich 509, project B2. We would like to thank W. Junke for technical support. We also thank D. Jancke, J. Pratt and two anonymous reviewers for helpful comments on earlier versions of this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Annette Horstmann.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Horstmann, A., Hoffmann, KP. Target selection in eye–hand coordination: Do we reach to where we look or do we look to where we reach?. Exp Brain Res 167, 187–195 (2005). https://doi.org/10.1007/s00221-005-0038-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-005-0038-6

Keywords

Navigation