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Published in: Experimental Brain Research 2/2005

01-11-2005 | Research Article

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

Authors: Annette Horstmann, Klaus-Peter Hoffmann

Published in: Experimental Brain Research | Issue 2/2005

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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.
Literature
go back to reference 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):1176–1196PubMed 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):1176–1196PubMed
go back to reference 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):357–381CrossRefPubMed 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):357–381CrossRefPubMed
go back to reference Barbas H, Mesulam MM (1981) Organization of afferent input to subdivisions of area 8 in the rhesus monkey. J Comp Neurol 200(3):407–431CrossRefPubMed Barbas H, Mesulam MM (1981) Organization of afferent input to subdivisions of area 8 in the rhesus monkey. J Comp Neurol 200(3):407–431CrossRefPubMed
go back to reference Basso MA, Wurtz RH (1997) Modulation of neuronal activity by target uncertainty. Nature 389(6646):66–69CrossRefPubMed Basso MA, Wurtz RH (1997) Modulation of neuronal activity by target uncertainty. Nature 389(6646):66–69CrossRefPubMed
go back to reference Batista AP, Buneo CA, Snyder LH, Andersen RA (1999) Reach plans in eye-centered coordinates. Science 285(5425):257–260CrossRefPubMed Batista AP, Buneo CA, Snyder LH, Andersen RA (1999) Reach plans in eye-centered coordinates. Science 285(5425):257–260CrossRefPubMed
go back to reference Carey DP, Coleman RJ, Della Sala S (1997) Magnetic misreaching. Cortex 33(4):639–652PubMed Carey DP, Coleman RJ, Della Sala S (1997) Magnetic misreaching. Cortex 33(4):639–652PubMed
go back to reference Cavanaugh J, Wurtz RH (2004) Subcortical modulation of attention counters change blindness. J Neurosci 24(50):11236–11243CrossRefPubMed Cavanaugh J, Wurtz RH (2004) Subcortical modulation of attention counters change blindness. J Neurosci 24(50):11236–11243CrossRefPubMed
go back to reference Cohen YE, Andersen RA (2000) Reaches to sounds encoded in an eye-centered reference frame. Neuron 27(3):647–652CrossRefPubMed Cohen YE, Andersen RA (2000) Reaches to sounds encoded in an eye-centered reference frame. Neuron 27(3):647–652CrossRefPubMed
go back to reference 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):458–462CrossRefPubMed 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):458–462CrossRefPubMed
go back to reference Findlay JM (1980) The visual stimulus for saccadic eye movements in human observers. Perception 9(1):7–21PubMedCrossRef Findlay JM (1980) The visual stimulus for saccadic eye movements in human observers. Perception 9(1):7–21PubMedCrossRef
go back to reference 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):159–178CrossRefPubMed 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):159–178CrossRefPubMed
go back to reference Frens MA, Erkelens CJ (1991) Coordination of hand movements and saccades: evidence for a common and a separate pathway. Exp Brain Res 85(3):682–690PubMedCrossRef Frens MA, Erkelens CJ (1991) Coordination of hand movements and saccades: evidence for a common and a separate pathway. Exp Brain Res 85(3):682–690PubMedCrossRef
go back to reference Fries W (1984) Cortical projections to the superior colliculus in the macaque monkey: a retrograde study using horseradish peroxidase. J Comp Neurol 230(1):55–76CrossRefPubMed Fries W (1984) Cortical projections to the superior colliculus in the macaque monkey: a retrograde study using horseradish peroxidase. J Comp Neurol 230(1):55–76CrossRefPubMed
go back to reference Fries W (1985) Inputs from motor and premotor cortex to the superior colliculus of the macaque monkey. Behav Brain Res 18(2):95–105CrossRefPubMed Fries W (1985) Inputs from motor and premotor cortex to the superior colliculus of the macaque monkey. Behav Brain Res 18(2):95–105CrossRefPubMed
go back to reference Gescheider GA (1997) Psychophysics: the fundamentals, 3rd edn. Lawrence Erlbaum Associates, Mahwah Gescheider GA (1997) Psychophysics: the fundamentals, 3rd edn. Lawrence Erlbaum Associates, Mahwah
go back to reference 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):154–161CrossRefPubMed 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):154–161CrossRefPubMed
go back to reference Goodale MA, Haffenden A (1998) Frames of reference for perception and action in the human visual system. Neurosci Biobehav Rev 22(2):161–172CrossRefPubMed Goodale MA, Haffenden A (1998) Frames of reference for perception and action in the human visual system. Neurosci Biobehav Rev 22(2):161–172CrossRefPubMed
go back to reference Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15(1):20–25CrossRefPubMed Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15(1):20–25CrossRefPubMed
go back to reference 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):748–750CrossRefPubMed 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):748–750CrossRefPubMed
go back to reference Grunewald A, Linden JF, Andersen RA (1999) Responses to auditory stimuli in macaque lateral intraparietal area. I. Effects of training. J Neurophysiol 82(1):330–342PubMed Grunewald A, Linden JF, Andersen RA (1999) Responses to auditory stimuli in macaque lateral intraparietal area. I. Effects of training. J Neurophysiol 82(1):330–342PubMed
go back to reference 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):455–472CrossRefPubMed 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):455–472CrossRefPubMed
go back to reference Horwitz GD, Newsome WT (1999) Separate signals for target selection and movement specification in the superior colliculus. Science 284(5417):1158–1161PubMedCrossRef Horwitz GD, Newsome WT (1999) Separate signals for target selection and movement specification in the superior colliculus. Science 284(5417):1158–1161PubMedCrossRef
go back to reference Iba M, Sawaguchi T (2003) Involvement of the dorsolateral prefrontal cortex of monkeys in visuospatial target selection. J Neurophysiol 89:587–599PubMedCrossRef Iba M, Sawaguchi T (2003) Involvement of the dorsolateral prefrontal cortex of monkeys in visuospatial target selection. J Neurophysiol 89:587–599PubMedCrossRef
go back to reference 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):391–409PubMedCrossRef 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):391–409PubMedCrossRef
go back to reference Lévy-Schoen A (1969) Détermination et latence de la résponse oculomotrice à deux stimulus simultanés ou successifs selon leur excentricité relative. Année Psychol 69:373–392CrossRef Lévy-Schoen A (1969) Détermination et latence de la résponse oculomotrice à deux stimulus simultanés ou successifs selon leur excentricité relative. Année Psychol 69:373–392CrossRef
go back to reference Lévy-Schoen A (1974) Le champ d’activité du regard: données expérimentales. Année Psychol 74:43–66PubMedCrossRef Lévy-Schoen A (1974) Le champ d’activité du regard: données expérimentales. Année Psychol 74:43–66PubMedCrossRef
go back to reference Linden JF, Grunewald A, Andersen RA (1999) Responses to auditory stimuli in macaque lateral intraparietal area. II. Behavioral modulation. J Neurophysiol 82(1):343–358PubMed Linden JF, Grunewald A, Andersen RA (1999) Responses to auditory stimuli in macaque lateral intraparietal area. II. Behavioral modulation. J Neurophysiol 82(1):343–358PubMed
go back to reference Lunenburger L, Kutz DF, Hoffmann KP (2000) Influence of arm movements on saccades in humans. Eur J Neurosci 12(11):4107–4116PubMedCrossRef Lunenburger L, Kutz DF, Hoffmann KP (2000) Influence of arm movements on saccades in humans. Eur J Neurosci 12(11):4107–4116PubMedCrossRef
go back to reference 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):1233–1241PubMed 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):1233–1241PubMed
go back to reference McPeek RM, Keller EL (2004) Deficits in saccade target selection after inactivation of superior colliculus. Nat Neurosci 7(7):757–763CrossRefPubMed McPeek RM, Keller EL (2004) Deficits in saccade target selection after inactivation of superior colliculus. Nat Neurosci 7(7):757–763CrossRefPubMed
go back to reference 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):524–529CrossRefPubMed 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):524–529CrossRefPubMed
go back to reference Murata A, Gallese V, Kaseda M, Sakata H (1996) Parietal neurons related to memory-guided hand manipulation. J Neurophysiol 75(5):2180–2186PubMed Murata A, Gallese V, Kaseda M, Sakata H (1996) Parietal neurons related to memory-guided hand manipulation. J Neurophysiol 75(5):2180–2186PubMed
go back to reference Neggers SF, Bekkering H (2000) Ocular gaze is anchored to the target of an ongoing pointing movement. J Neurophysiol 83(2):639–651PubMed Neggers SF, Bekkering H (2000) Ocular gaze is anchored to the target of an ongoing pointing movement. J Neurophysiol 83(2):639–651PubMed
go back to reference Neggers SF, Bekkering H (2002) Coordinated control of eye and hand movements in dynamic reaching. Hum Mov Sci 21(3):349–376CrossRefPubMed Neggers SF, Bekkering H (2002) Coordinated control of eye and hand movements in dynamic reaching. Hum Mov Sci 21(3):349–376CrossRefPubMed
go back to reference Pashler H, Carrier M, Hoffman J (1993) Saccadic eye movements and dual-task interference. Q J Exp Psychol A 46(1):51–82PubMed Pashler H, Carrier M, Hoffman J (1993) Saccadic eye movements and dual-task interference. Q J Exp Psychol A 46(1):51–82PubMed
go back to reference Platt ML, Glimcher PW (1998) Response fields of intraparietal neurons quantified with multiple saccadic targets. Exp Brain Res 121(1):65–75CrossRefPubMed Platt ML, Glimcher PW (1998) Response fields of intraparietal neurons quantified with multiple saccadic targets. Exp Brain Res 121(1):65–75CrossRefPubMed
go back to reference Platt ML, Glimcher PW (1999) Neural correlates of decision variables in parietal cortex. Nature 400(6741):233–238CrossRefPubMed Platt ML, Glimcher PW (1999) Neural correlates of decision variables in parietal cortex. Nature 400(6741):233–238CrossRefPubMed
go back to reference Pouget A, Deneve S, Duhamel JR (2002) A computational perspective on the neural basis of multisensory spatial representations. Nat Rev Neurosci 3(9):741–747CrossRefPubMed Pouget A, Deneve S, Duhamel JR (2002) A computational perspective on the neural basis of multisensory spatial representations. Nat Rev Neurosci 3(9):741–747CrossRefPubMed
go back to reference Prablanc C, Martin O (1992) Automatic control during hand reaching at undetected two-dimensional target displacements. J Neurophysiol 67(2):455–469PubMed Prablanc C, Martin O (1992) Automatic control during hand reaching at undetected two-dimensional target displacements. J Neurophysiol 67(2):455–469PubMed
go back to reference 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):524–535CrossRefPubMed 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):524–535CrossRefPubMed
go back to reference 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):1456–1466PubMedCrossRef 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):1456–1466PubMedCrossRef
go back to reference 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):248–253CrossRefPubMed 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):248–253CrossRefPubMed
go back to reference 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):144–153CrossRefPubMed 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):144–153CrossRefPubMed
go back to reference Shadlen MN, Newsome WT (1996) Motion perception: seeing and deciding. Proc Natl Acad Sci USA 93(2):628–633CrossRefPubMed Shadlen MN, Newsome WT (1996) Motion perception: seeing and deciding. Proc Natl Acad Sci USA 93(2):628–633CrossRefPubMed
go back to reference Snyder LH, Batista AP, Andersen RA (1997) Coding of intention in the posterior parietal cortex. Nature 386(6621):167–170CrossRefPubMed Snyder LH, Batista AP, Andersen RA (1997) Coding of intention in the posterior parietal cortex. Nature 386(6621):167–170CrossRefPubMed
go back to reference 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 79:2814–2819PubMed 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 79:2814–2819PubMed
go back to reference 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):2279–2286PubMed 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):2279–2286PubMed
go back to reference Soechting JF, Engel KC, Flanders M (2001) The Duncker illusion and eye-hand coordination. J Neurophysiol 85(2):843–854PubMed Soechting JF, Engel KC, Flanders M (2001) The Duncker illusion and eye-hand coordination. J Neurophysiol 85(2):843–854PubMed
go back to reference 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):2071–2076PubMed 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):2071–2076PubMed
go back to reference 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):1283–1299PubMed 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):1283–1299PubMed
go back to reference Wardak C, Olivier E, Duhamel JR (2002) Saccadic target selection deficits after lateral intraparietal area inactivation in monkeys. J Neurosci 22(22):9877–9884PubMed Wardak C, Olivier E, Duhamel JR (2002) Saccadic target selection deficits after lateral intraparietal area inactivation in monkeys. J Neurosci 22(22):9877–9884PubMed
go back to reference Werner W (1993) Neurons in the primate superior colliculus are active before and during arm movements to visual targets. Eur J Neurosci 5(4):335–340PubMedCrossRef Werner W (1993) Neurons in the primate superior colliculus are active before and during arm movements to visual targets. Eur J Neurosci 5(4):335–340PubMedCrossRef
go back to reference 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):191–205PubMedCrossRef 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):191–205PubMedCrossRef
go back to reference Wurtz RH, Goldberg ME (1971) Superior colliculus cell responses related to eye movements in awake monkeys. Science 171(966):82–84PubMedCrossRef Wurtz RH, Goldberg ME (1971) Superior colliculus cell responses related to eye movements in awake monkeys. Science 171(966):82–84PubMedCrossRef
Metadata
Title
Target selection in eye–hand coordination: Do we reach to where we look or do we look to where we reach?
Authors
Annette Horstmann
Klaus-Peter Hoffmann
Publication date
01-11-2005
Publisher
Springer-Verlag
Published in
Experimental Brain Research / Issue 2/2005
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-005-0038-6

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