Skip to main content
Top
Published in: Brain Structure and Function 4/2017

01-05-2017 | Original Article

Temporal stability of reference frames in monkey area V6A during a reaching task in 3D space

Authors: Kostas Hadjidimitrakis, Federica Bertozzi, Rossella Breveglieri, Claudio Galletti, Patrizia Fattori

Published in: Brain Structure and Function | Issue 4/2017

Login to get access

Abstract

Neurons in the posterior parietal cortex of macaques show spatial tuning during several phases of an instructed delay reaching task, but their reference frames have been studied mostly during fixed periods without addressing how they evolve across task phases. In parietal area V6A, we reported recently that during the late delay and hand movement periods, most neurons represent target location either in body-centered frame of reference, or in mixed body/hand-centered coordinates, with no evidence of hand-centered representations. Here, we characterized the spatial representations of V6A neurons in earlier task epochs, i.e., immediately after target fixation and in the subsequent main part of the delay and examined whether the reference frames of individual neurons are stable across the task. We report no evidence of hand-centered coding also in the earlier phases of the task. Shortly, after target fixation and throughout the main part of the delay period, V6A neurons used either body-centered or mixed body/hand-centered reference frames. Most of the cells showed consistent reference frames across epochs. Interestingly, a population trend of shifting from mixed body/hand-centered frames to ‘pure’ body-centered coordinates was found as the task progressed. These findings suggest that, similar to other parietal areas, in V6A, the reference frames show a limited degree of temporal evolution. The stronger presence of mixed coding at the early task stages could reflect the early involvement of V6A in eye-hand coordination, whereas the increase in spatiotopic representations towards movement execution could be related to its role in online movement control.
Literature
go back to reference Andersen RA, Buneo CA (2002) Intentional maps in posterior parietal cortex. Annu Rev Neurosci 25:189–220CrossRefPubMed Andersen RA, Buneo CA (2002) Intentional maps in posterior parietal cortex. Annu Rev Neurosci 25:189–220CrossRefPubMed
go back to reference Archambault PS, Ferrari-Toniolo S, Battaglia-Mayer A (2011) Online control of hand trajectory and evolution of motor intention in the parietofrontal system. J Neurosci 31:742–752CrossRefPubMed Archambault PS, Ferrari-Toniolo S, Battaglia-Mayer A (2011) Online control of hand trajectory and evolution of motor intention in the parietofrontal system. J Neurosci 31:742–752CrossRefPubMed
go back to reference Bakola S, Passarelli L, Gamberini M, Fattori P, Galletti C (2013) Cortical connectivity suggests a role in limb coordination for macaque area PE of the superior parietal cortex. J Neurosci 33:6648–6658CrossRefPubMed Bakola S, Passarelli L, Gamberini M, Fattori P, Galletti C (2013) Cortical connectivity suggests a role in limb coordination for macaque area PE of the superior parietal cortex. J Neurosci 33:6648–6658CrossRefPubMed
go back to reference Batista AP, Buneo CA, Snyder LH, Andersen RA (1999) Reach plans in eye-centered coordinates. Science 285:257–260CrossRefPubMed Batista AP, Buneo CA, Snyder LH, Andersen RA (1999) Reach plans in eye-centered coordinates. Science 285:257–260CrossRefPubMed
go back to reference Batista AP, Santhanam G, Yu BM, Ryu SI, Afshar A, Shenoy KV (2007) Reference frames for reach planning in macaque dorsal premotor cortex. J Neurophysiol 98:966–983CrossRefPubMed Batista AP, Santhanam G, Yu BM, Ryu SI, Afshar A, Shenoy KV (2007) Reference frames for reach planning in macaque dorsal premotor cortex. J Neurophysiol 98:966–983CrossRefPubMed
go back to reference Bernier PM, Grafton ST (2010) Human posterior parietal cortex flexibly determines reference frames for reaching based on sensory context. Neuron 68:776–788CrossRefPubMed Bernier PM, Grafton ST (2010) Human posterior parietal cortex flexibly determines reference frames for reaching based on sensory context. Neuron 68:776–788CrossRefPubMed
go back to reference Bosco A, Breveglieri R, Reser D, Galletti C, Fattori P (2015) Multiple representation of reaching space in the medial posterior parietal area V6A. Cereb Cortex 25:1654–1667CrossRefPubMed Bosco A, Breveglieri R, Reser D, Galletti C, Fattori P (2015) Multiple representation of reaching space in the medial posterior parietal area V6A. Cereb Cortex 25:1654–1667CrossRefPubMed
go back to reference Bosco A, Breveglieri R, Hadjidimitrakis K, Galletti C, Fattori P (2016) Reference frames for reaching when decoupling eye and target position in depth and direction. Sci Rep 6:21646CrossRefPubMedPubMedCentral Bosco A, Breveglieri R, Hadjidimitrakis K, Galletti C, Fattori P (2016) Reference frames for reaching when decoupling eye and target position in depth and direction. Sci Rep 6:21646CrossRefPubMedPubMedCentral
go back to reference Buneo CA, Andersen RA (2012) Integration of target and hand position signals in the posterior parietal cortex: effects of workspace and hand vision. J Neurophysiol 108:187–199CrossRefPubMedPubMedCentral Buneo CA, Andersen RA (2012) Integration of target and hand position signals in the posterior parietal cortex: effects of workspace and hand vision. J Neurophysiol 108:187–199CrossRefPubMedPubMedCentral
go back to reference Buneo CA, Jarvis MR, Batista AP, Andersen RA (2002) Direct visuomotor transformations for reaching. Nature 416:632–636CrossRefPubMed Buneo CA, Jarvis MR, Batista AP, Andersen RA (2002) Direct visuomotor transformations for reaching. Nature 416:632–636CrossRefPubMed
go back to reference Buneo C, Batista A, Jarvis M, Andersen R (2008) Time-invariant reference frames for parietal reach activity. Exp Brain Res 188:77–89CrossRefPubMed Buneo C, Batista A, Jarvis M, Andersen R (2008) Time-invariant reference frames for parietal reach activity. Exp Brain Res 188:77–89CrossRefPubMed
go back to reference Chang SWC, Snyder LH (2010) Idiosyncratic and systematic aspects of spatial representations in the macaque parietal cortex. Proc Natl Acad Sci 107:7951–7956CrossRefPubMedPubMedCentral Chang SWC, Snyder LH (2010) Idiosyncratic and systematic aspects of spatial representations in the macaque parietal cortex. Proc Natl Acad Sci 107:7951–7956CrossRefPubMedPubMedCentral
go back to reference Fattori P, Kutz DF, Breveglieri R, Marzocchi N, Galletti C (2005) Spatial tuning of reaching activity in the medial parieto-occipital cortex (area V6A) of macaque monkey. Eur J Neurosci 22:956–972CrossRefPubMed Fattori P, Kutz DF, Breveglieri R, Marzocchi N, Galletti C (2005) Spatial tuning of reaching activity in the medial parieto-occipital cortex (area V6A) of macaque monkey. Eur J Neurosci 22:956–972CrossRefPubMed
go back to reference Flanders M, Helms Tillery SI, Soechting JF (1992) Early stages in a sensorimotor transformation. Behav Brain Sci 15:309–362CrossRef Flanders M, Helms Tillery SI, Soechting JF (1992) Early stages in a sensorimotor transformation. Behav Brain Sci 15:309–362CrossRef
go back to reference Galletti C, Battaglini PP, Fattori P (1995) Eye position influence on the parieto-occipital area PO (V6) of the macaque monkey. Eur J Neurosci 7:2486–2501CrossRefPubMed Galletti C, Battaglini PP, Fattori P (1995) Eye position influence on the parieto-occipital area PO (V6) of the macaque monkey. Eur J Neurosci 7:2486–2501CrossRefPubMed
go back to reference Galletti C, Fattori P, Battaglini PP, Shipp S, Zeki S (1996) Functional demarcation of a border between areas V6 and V6A in the superior parietal gyrus of the macaque monkey. Eur J Neurosci 8:30–52CrossRefPubMed Galletti C, Fattori P, Battaglini PP, Shipp S, Zeki S (1996) Functional demarcation of a border between areas V6 and V6A in the superior parietal gyrus of the macaque monkey. Eur J Neurosci 8:30–52CrossRefPubMed
go back to reference Galletti C, Fattori P, Kutz DF, Gamberini M (1999) Brain location and visual topography of cortical area V6A in the macaque monkey. Eur J Neurosci 11:575–582CrossRefPubMed Galletti C, Fattori P, Kutz DF, Gamberini M (1999) Brain location and visual topography of cortical area V6A in the macaque monkey. Eur J Neurosci 11:575–582CrossRefPubMed
go back to reference Galletti C, Kutz D, Gamberini M, Breveglieri R, Fattori P (2003) Role of the medial parieto-occipital cortex in the control of reaching and grasping movements. Exp Brain Res 153:158–170CrossRefPubMed Galletti C, Kutz D, Gamberini M, Breveglieri R, Fattori P (2003) Role of the medial parieto-occipital cortex in the control of reaching and grasping movements. Exp Brain Res 153:158–170CrossRefPubMed
go back to reference Gamberini M, Passarelli L, Fattori P, Zucchelli M, Bakola S, Luppino G, Galletti C (2009) Cortical connections of the visuomotor parietooccipital area V6Ad of the macaque monkey. J Comp Neurol 513:622–642CrossRefPubMed Gamberini M, Passarelli L, Fattori P, Zucchelli M, Bakola S, Luppino G, Galletti C (2009) Cortical connections of the visuomotor parietooccipital area V6Ad of the macaque monkey. J Comp Neurol 513:622–642CrossRefPubMed
go back to reference Gamberini M, Galletti C, Bosco A, Breveglieri R, Fattori P (2011) Is the medial posterior parietal area V6A a single functional area? J Neurosci 31:5145–5157CrossRefPubMed Gamberini M, Galletti C, Bosco A, Breveglieri R, Fattori P (2011) Is the medial posterior parietal area V6A a single functional area? J Neurosci 31:5145–5157CrossRefPubMed
go back to reference Hadjidimitrakis K, Bertozzi F, Breveglieri R, Bosco A, Dal Bo’ G, Galletti C, Fattori P (2011) Visually guided arm movements in 3D space: spatial tuning in fixation, preparation and reaching activity in monkey medial posterior parietal cortex. In: Neuroscience Sf (ed) Annual meeting of the Society for Neuroscience, Washington DC Hadjidimitrakis K, Bertozzi F, Breveglieri R, Bosco A, Dal Bo’ G, Galletti C, Fattori P (2011) Visually guided arm movements in 3D space: spatial tuning in fixation, preparation and reaching activity in monkey medial posterior parietal cortex. In: Neuroscience Sf (ed) Annual meeting of the Society for Neuroscience, Washington DC
go back to reference Hadjidimitrakis K, Breveglieri R, Bosco A, Fattori P (2012) Three-dimensional eye position signals shape both peripersonal space and arm movement activity in the medial posterior parietal cortex. Front Integr Neurosci 6:37CrossRefPubMedPubMedCentral Hadjidimitrakis K, Breveglieri R, Bosco A, Fattori P (2012) Three-dimensional eye position signals shape both peripersonal space and arm movement activity in the medial posterior parietal cortex. Front Integr Neurosci 6:37CrossRefPubMedPubMedCentral
go back to reference Hadjidimitrakis K, Bertozzi F, Breveglieri R, Fattori P, Galletti C (2014a) Body-centered, mixed, but not hand-centered coding of visual targets in the medial posterior parietal cortex during reaches in 3D space. Cereb Cortex 24:3209–3220CrossRefPubMed Hadjidimitrakis K, Bertozzi F, Breveglieri R, Fattori P, Galletti C (2014a) Body-centered, mixed, but not hand-centered coding of visual targets in the medial posterior parietal cortex during reaches in 3D space. Cereb Cortex 24:3209–3220CrossRefPubMed
go back to reference Hadjidimitrakis K, Bertozzi F, Breveglieri R, Bosco A, Galletti C, Fattori P (2014b) Common neural substrate for processing depth and direction signals for reaching in the monkey medial posterior parietal cortex. Cereb Cortex 24:1645–1657CrossRefPubMed Hadjidimitrakis K, Bertozzi F, Breveglieri R, Bosco A, Galletti C, Fattori P (2014b) Common neural substrate for processing depth and direction signals for reaching in the monkey medial posterior parietal cortex. Cereb Cortex 24:1645–1657CrossRefPubMed
go back to reference Hayhoe MM, Shrivastava A, Mruczek R, Pelz JB (2003) Visual memory and motor planning in a natural task. J Vis 3:49–63CrossRefPubMed Hayhoe MM, Shrivastava A, Mruczek R, Pelz JB (2003) Visual memory and motor planning in a natural task. J Vis 3:49–63CrossRefPubMed
go back to reference Johansson RS, Westling G, Backstrom A, Flanagan JR (2001) Eye-hand coordination in object manipulation. J Neurosci 21:6917–6932PubMed Johansson RS, Westling G, Backstrom A, Flanagan JR (2001) Eye-hand coordination in object manipulation. J Neurosci 21:6917–6932PubMed
go back to reference Kutz DF, Fattori P, Gamberini M, Breveglieri R, Galletti C (2003) Early- and late-responding cells to saccadic eye movements in the cortical area V6A of macaque monkey. Exp Brain Res 149:83–95CrossRefPubMed Kutz DF, Fattori P, Gamberini M, Breveglieri R, Galletti C (2003) Early- and late-responding cells to saccadic eye movements in the cortical area V6A of macaque monkey. Exp Brain Res 149:83–95CrossRefPubMed
go back to reference Kutz DF, Marzocchi N, Fattori P, Cavalcanti S, Galletti C (2005) Real-time supervisor system based on trinary logic to control experiments with behaving animals and humans. J Neurophysiol 93:3674–3686CrossRefPubMed Kutz DF, Marzocchi N, Fattori P, Cavalcanti S, Galletti C (2005) Real-time supervisor system based on trinary logic to control experiments with behaving animals and humans. J Neurophysiol 93:3674–3686CrossRefPubMed
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 5:391–409CrossRefPubMed 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 5:391–409CrossRefPubMed
go back to reference Leone FT, Monaco S, Henriques DY, Toni I, Medendorp WP (2015) Flexible reference frames for grasp planning in human parietofrontal cortex. eNeuro 2 Leone FT, Monaco S, Henriques DY, Toni I, Medendorp WP (2015) Flexible reference frames for grasp planning in human parietofrontal cortex. eNeuro 2
go back to reference Luppino G, Ben Hamed S, Gamberini M, Matelli M, Galletti C (2005) Occipital (V6) and parietal (V6A) areas in the anterior wall of the parieto-occipital sulcus of the macaque: a cytoarchitectonic study. Eur J Neurosci 21:3056–3076CrossRefPubMed Luppino G, Ben Hamed S, Gamberini M, Matelli M, Galletti C (2005) Occipital (V6) and parietal (V6A) areas in the anterior wall of the parieto-occipital sulcus of the macaque: a cytoarchitectonic study. Eur J Neurosci 21:3056–3076CrossRefPubMed
go back to reference Marzocchi N, Breveglieri R, Galletti C, Fattori P (2008) Reaching activity in parietal area V6A of macaque: eye influence on arm activity or retinocentric coding of reaching movements? Eur J Neurosci 27:775–789CrossRefPubMedPubMedCentral Marzocchi N, Breveglieri R, Galletti C, Fattori P (2008) Reaching activity in parietal area V6A of macaque: eye influence on arm activity or retinocentric coding of reaching movements? Eur J Neurosci 27:775–789CrossRefPubMedPubMedCentral
go back to reference McGuire LM, Sabes PN (2011) Heterogeneous representations in the superior parietal lobule are common across reaches to visual and proprioceptive targets. J Neurosci 31:6661–6673CrossRefPubMedPubMedCentral McGuire LM, Sabes PN (2011) Heterogeneous representations in the superior parietal lobule are common across reaches to visual and proprioceptive targets. J Neurosci 31:6661–6673CrossRefPubMedPubMedCentral
go back to reference Mullette-Gillman ODA, Cohen YE, Groh JM (2009) Motor-related signals in the intraparietal cortex encode locations in a hybrid, rather than eye-centered reference frame. Cereb Cortex 19:1761–1775CrossRefPubMed Mullette-Gillman ODA, Cohen YE, Groh JM (2009) Motor-related signals in the intraparietal cortex encode locations in a hybrid, rather than eye-centered reference frame. Cereb Cortex 19:1761–1775CrossRefPubMed
go back to reference Pesaran B, Nelson MJ, Andersen RA (2006) Dorsal premotor neurons encode the relative position of the hand, eye, and goal during reach planning. Neuron 51:125–134CrossRefPubMedPubMedCentral Pesaran B, Nelson MJ, Andersen RA (2006) Dorsal premotor neurons encode the relative position of the hand, eye, and goal during reach planning. Neuron 51:125–134CrossRefPubMedPubMedCentral
go back to reference Piserchia V, Breveglieri R, Hadjidimitrakis K, Bertozzi F, Galletti C, Fattori P (2016) Mixed body/hand reference frame for reaching in 3D space in macaque parietal area PEc. Cereb Cortex. doi.10.1093/cercor/bhw039 Piserchia V, Breveglieri R, Hadjidimitrakis K, Bertozzi F, Galletti C, Fattori P (2016) Mixed body/hand reference frame for reaching in 3D space in macaque parietal area PEc. Cereb Cortex. doi.10.​1093/​cercor/​bhw039
go back to reference Pouget A, Snyder LH (2000) Computational approaches to sensorimotor transformations. Nat Neurosci 3(Suppl):1192–1198CrossRefPubMed Pouget A, Snyder LH (2000) Computational approaches to sensorimotor transformations. Nat Neurosci 3(Suppl):1192–1198CrossRefPubMed
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 3:741–747CrossRefPubMed Pouget A, Deneve S, Duhamel JR (2002) A computational perspective on the neural basis of multisensory spatial representations. Nat Rev Neurosci 3:741–747CrossRefPubMed
go back to reference Zipser D, Andersen RA (1988) A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature 331:679–684CrossRefPubMed Zipser D, Andersen RA (1988) A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature 331:679–684CrossRefPubMed
Metadata
Title
Temporal stability of reference frames in monkey area V6A during a reaching task in 3D space
Authors
Kostas Hadjidimitrakis
Federica Bertozzi
Rossella Breveglieri
Claudio Galletti
Patrizia Fattori
Publication date
01-05-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 4/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-016-1319-5

Other articles of this Issue 4/2017

Brain Structure and Function 4/2017 Go to the issue