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

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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.

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References

  • Andersen RA, Buneo CA (2002) Intentional maps in posterior parietal cortex. Annu Rev Neurosci 25:189–220

    Article  CAS  PubMed  Google Scholar 

  • 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 31:742–752

    Article  CAS  PubMed  Google Scholar 

  • 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 33:6648–6658

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 98:966–983

    Article  PubMed  Google Scholar 

  • Bernier PM, Grafton ST (2010) Human posterior parietal cortex flexibly determines reference frames for reaching based on sensory context. Neuron 68:776–788

    Article  CAS  PubMed  Google Scholar 

  • Blohm G (2012) Simulating the cortical 3D visuomotor transformation of reach depth. PLoS One 7:e41241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 25:1654–1667

    Article  CAS  PubMed  Google Scholar 

  • 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 6:21646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bremner L, Andersen R (2012) Coding of the reach vector in parietal area 5D. Neuron 75:342–351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bremner LR, Andersen RA (2014) Temporal analysis of reference frames in parietal cortex area 5d during reach planning. J Neurosci 34:5273–5284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 108:187–199

    Article  PubMed  PubMed Central  Google Scholar 

  • Buneo CA, Jarvis MR, Batista AP, Andersen RA (2002) Direct visuomotor transformations for reaching. Nature 416:632–636

    Article  CAS  PubMed  Google Scholar 

  • Buneo C, Batista A, Jarvis M, Andersen R (2008) Time-invariant reference frames for parietal reach activity. Exp Brain Res 188:77–89

    Article  PubMed  Google Scholar 

  • Chang SWC, Snyder LH (2010) Idiosyncratic and systematic aspects of spatial representations in the macaque parietal cortex. Proc Natl Acad Sci 107:7951–7956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang SWC, Dickinson AR, Snyder LH (2008) Limb-specific representation for reaching in the posterior parietal cortex. J Neurosci 28:6128–6140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang SW, Papadimitriou C, Snyder LH (2009) Using a compound gain field to compute a reach plan. Neuron 64:744–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 22:956–972

    Article  PubMed  Google Scholar 

  • Fattori P, Breveglieri R, Bosco A, Gamberini M, Galletti C (2015) Vision for prehension in the medial parietal cortex. Cereb Cortex. doi:10.1093/cercor/bhv302

    PubMed  Google Scholar 

  • Flanders M, Helms Tillery SI, Soechting JF (1992) Early stages in a sensorimotor transformation. Behav Brain Sci 15:309–362

    Article  Google Scholar 

  • Galletti C, Battaglini PP, Fattori P (1995) Eye position influence on the parieto-occipital area PO (V6) of the macaque monkey. Eur J Neurosci 7:2486–2501

    Article  CAS  PubMed  Google Scholar 

  • 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 8:30–52

    Article  CAS  PubMed  Google Scholar 

  • 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 11:575–582

    Article  CAS  PubMed  Google Scholar 

  • 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 153:158–170

    Article  PubMed  Google Scholar 

  • 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 513:622–642

    Article  PubMed  Google Scholar 

  • Gamberini M, Galletti C, Bosco A, Breveglieri R, Fattori P (2011) Is the medial posterior parietal area V6A a single functional area? J Neurosci 31:5145–5157

    Article  CAS  PubMed  Google Scholar 

  • 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, 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 6:37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 24:3209–3220

    Article  CAS  PubMed  Google Scholar 

  • 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 24:1645–1657

    Article  CAS  PubMed  Google Scholar 

  • Hayhoe MM, Shrivastava A, Mruczek R, Pelz JB (2003) Visual memory and motor planning in a natural task. J Vis 3:49–63

    Article  PubMed  Google Scholar 

  • Johansson RS, Westling G, Backstrom A, Flanagan JR (2001) Eye-hand coordination in object manipulation. J Neurosci 21:6917–6932

    CAS  PubMed  Google Scholar 

  • 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 149:83–95

    Article  CAS  PubMed  Google Scholar 

  • 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 93:3674–3686

    Article  CAS  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 5:391–409

    Article  CAS  PubMed  Google Scholar 

  • Leone FT, Monaco S, Henriques DY, Toni I, Medendorp WP (2015) Flexible reference frames for grasp planning in human parietofrontal cortex. eNeuro 2

  • 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 21:3056–3076

    Article  PubMed  Google Scholar 

  • 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 27:775–789

    Article  PubMed  PubMed Central  Google Scholar 

  • McGuire LM, Sabes PN (2011) Heterogeneous representations in the superior parietal lobule are common across reaches to visual and proprioceptive targets. J Neurosci 31:6661–6673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 19:1761–1775

    Article  PubMed  Google Scholar 

  • Pesaran B, Nelson MJ, Andersen RA (2006) Dorsal premotor neurons encode the relative position of the hand, eye, and goal during reach planning. Neuron 51:125–134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Pouget A, Snyder LH (2000) Computational approaches to sensorimotor transformations. Nat Neurosci 3(Suppl):1192–1198

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zipser D, Andersen RA (1988) A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature 331:679–684

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. A. Bosco and G. Dal Bo’ for help in the recordings, Michela Gamberini and Lauretta Passarelli for the anatomical reconstructions, and Prof. Marcello Rosa for helpful comments on an earlier version of the manuscript. This work was supported by EU FP7-IST-217077-EYESHOTS, by Ministero dell’Università e della Ricerca Italy, FIRB2013 prot. RBFR132BKP), by Fondazione del Monte di Bologna e Ravenna (Italy), and National Health and Medical Research Council Grant APP1020839 and APP1082144 (Australia).

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Correspondence to Kostas Hadjidimitrakis or Patrizia Fattori.

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Hadjidimitrakis, K., Bertozzi, F., Breveglieri, R. et al. Temporal stability of reference frames in monkey area V6A during a reaching task in 3D space. Brain Struct Funct 222, 1959–1970 (2017). https://doi.org/10.1007/s00429-016-1319-5

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