Skip to main content
SpringerLink
Log in

Orienting movements in area 9 identified by long-train ICMS

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

The effect of intracortical microstimulation has been studied in several cortical areas from motor to sensory areas. The frontal pole has received particular attention, and several microstimulation studies have been conducted in the frontal eye field, supplementary eye field, and the premotor ear–eye field, but no microstimulation studies concerning area 9 are currently available in the literature. In the present study, to fill up this gap, electrical microstimulation was applied to area 9 in two macaque monkeys using long-train pulses of 500–700–800 and 1,000 ms, during two different experimental conditions: a spontaneous condition, while the animals were not actively fixating on a visual target, and during a visual fixation task. In these experiments, we identified backward ear movements, goal-directed eye movements, and the development of head forces. Kinematic parameters for ear and eye movements overlapped in the spontaneous condition, but they were different during the visual fixation task. In this condition, ear and eye kinematics have an opposite behavior: movement amplitude, duration, and maximal and mean velocities increase during a visual fixation task for the ear, while they decrease for the eye. Therefore, a top-down visual attention engagement could modify the kinematic parameters for these two effectors. Stimulation with the longest train durations, i.e., 800/1,000 ms, evokes not only the highest eye amplitude, but also a significant development of head forces. In this research article, we propose a new vision of the frontal oculomotor fields, speculating a role for area 9 in the control of goal-directed orienting behaviors and gaze shift control.

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

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

Similar content being viewed by others

References

  • Akkal D, Escola L, Bioulac B, Burbaud P (2004) Time predictability modulates pre-supplementary motor area neuronal activity. NeuroReport 15(8):1283–1286

    Article  CAS  PubMed  Google Scholar 

  • Andrew RJ (1963) Evolution of facial expression. Science 142(3595):1034–1041

    Article  CAS  PubMed  Google Scholar 

  • Azuma M, Suzuki H (1984) Properties and distribution of auditory neurons in the dorsolateral prefrontal cortex of the alert monkey. Brain Res 298(2):343–346

    Article  CAS  PubMed  Google Scholar 

  • Bon L, Lucchetti C (1994) Ear and eye representation in the frontal cortex, area 8b, of the macaque monkey: an electrophysiological study. Exp Brain Res 102(2):259–271

    Article  CAS  PubMed  Google Scholar 

  • Bon L, Lucchetti C (2006) Auditory environmental cells and visual fixation effect in area 8B of macaque monkey. Exp Brain Res 168(3):441–449

    Article  PubMed  Google Scholar 

  • Bon L, Lucchetti C, Portolan F, Pagan M (2002) Equipment note MUPRO: a multipurpose robot. Int J Neurosci 112(7):855–868. doi:10.1080/00207450290025888

    Article  PubMed  Google Scholar 

  • Bon L, Lanzilotto M, Lucchetti C (2009) PEEF: premotor ear–eye field. A new vista of area 8B. In: LoGrasso L, Morretti G (eds) Prefrontal cortex: roles, interventions and traumas. Nova Science Publisher, Portland, OR,  pp 157–175

  • Borra E, Gerbella M, Rozzi S, Luppino G (2011) Anatomical evidence for the involvement of the macaque ventrolateral prefrontal area 12r in controlling goal-directed actions. J Neurosci 31(34):12351–12363. doi:10.1523/jneurosci.1745-11.2011

    Article  CAS  PubMed  Google Scholar 

  • Borra E, Gerbella M, Rozzi S, Luppino G (2013) Projections from caudal ventrolateral prefrontal areas to brainstem preoculomotor structures and to basal ganglia and cerebellar oculomotor loops in the macaque. Cereb Cortex 24:24

    Google Scholar 

  • Bruce CJ, Goldberg ME (1985) Primate frontal eye fields. I. Single neurons discharging before saccades. J Neurophysiol 53(3):603–635

    CAS  PubMed  Google Scholar 

  • Chapman BB, Pace MA, Cushing SL, Corneil BD (2012) Recruitment of a contralateral head turning synergy by stimulation of monkey supplementary eye fields. J Neurophysiol 107(6):1694–1710. doi:10.1152/jn.00487.2011

    Article  PubMed  Google Scholar 

  • Chen LL (2006) Head movements evoked by electrical stimulation in the frontal eye field of the monkey: evidence for independent eye and head control. J Neurophysiol 95(6):3528–3542. doi:10.1152/jn.01320.2005

    Article  PubMed  Google Scholar 

  • Chen LL, Tehovnik EJ (2007) Cortical control of eye and head movements: integration of movements and percepts. Eur J Neurosci 25(5):1253–1264

    Article  PubMed  Google Scholar 

  • Chen LL, Walton MM (2005) Head movement evoked by electrical stimulation in the supplementary eye field of the rhesus monkey. J Neurophysiol 94(6):4502–4519

    Article  PubMed  Google Scholar 

  • Cheron G, Draye JP, Bengoetxea A, Dan B (1999) Kinematics invariance in multi-directional complex movements in free space: effect of changing initial direction. Clin Neurophysiol 110(4):757–764. doi:10.1016/S1388-2457(99)00012-7

    Article  CAS  PubMed  Google Scholar 

  • Cooke DF, Taylor CSR, Moore T, Graziano MSA (2003) Complex movements evoked by microstimulation of the ventral intraparietal area. Proc Natl Acad Sci 100(10):6163–6168. doi:10.1073/pnas.1031751100

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ferrier D (1876) The functions of the brain. Elder, London

    Book  Google Scholar 

  • Freedman EG, Sparks DL (1997) Eye–head coordination during head-unrestrained gaze shifts in rhesus monkeys. J Neurophysiol 77(5):2328–2348

    CAS  PubMed  Google Scholar 

  • Fujii N, Mushiake H, Tanji J (2002) Distribution of eye- and arm-movement-related neuronal activity in the SEF and in the SMA and Pre-SMA of monkeys. J Neurophysiol 87(4):2158–2166. doi:10.1152/jn.00867.2001

    PubMed  Google Scholar 

  • Funahashi S (2013) Space representation in the prefrontal cortex. Prog Neurobiol 103:131–155

    Article  PubMed  Google Scholar 

  • Funahashi S, Chafee MV, Goldman-Rakic PS (1993) Prefrontal neuronal activity in rhesus monkeys performing a delayed anti-saccade task. Nature 365(6448):753–756

    Article  CAS  PubMed  Google Scholar 

  • Fuster J (2008) The prefrontal cortex. Access online via Elsevier

  • Fuster JM, Bodner M, Kroger JK (2000) Cross-modal and cross-temporal association in neurons of frontal cortex. Nature 405(6784):347–351

    Article  CAS  PubMed  Google Scholar 

  • Gandhi NJ, Sparks DL (2001) Experimental control of eye and head positions prior to head-unrestrained gaze shifts in monkey. Vision Res 41(25):3243–3254. doi:10.1016/s0042-6989(01)00054-2

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Genovesio A, Tsujimoto S, Wise SP (2012) Encoding goals but not abstract magnitude in the primate prefrontal cortex. Neuron 74(4):656–662

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gerbella M, Belmalih A, Borra E, Rozzi S, Luppino G (2010) Cortical connections of the macaque caudal ventrolateral prefrontal areas 45A and 45B. Cereb Cortex 20(1):141–168. doi:10.1093/cercor/bhp087

    Article  PubMed  Google Scholar 

  • Graziano MSA, Taylor CSR, Moore T (2002a) Complex movements evoked by microstimulation of precentral cortex. Neuron 34(5):841–851. doi:10.1016/S0896-6273(02)00698-0

    Article  CAS  PubMed  Google Scholar 

  • Graziano MSA, Taylor CSR, Moore T, Cooke DF (2002b) The cortical control of movement revisited. Neuron 36(3):349–362. doi:10.1016/S0896-6273(02)01003-6

    Article  CAS  PubMed  Google Scholar 

  • Judge SJ, Richmond BJ, Chu FC (1980) Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res 20(6):535–538

    Article  CAS  PubMed  Google Scholar 

  • Lanzilotto M, Perciavalle V, Lucchetti C (2013a) Auditory and visual systems organization in Brodmann Area 8 for gaze-shift control: where we do not see, we can hear. Frontiers Behav Neurosci 7:198. doi:10.3389/fnbeh.2013.00198

  • Lanzilotto M, Perciavalle V, Lucchetti C (2013b) A new field in monkey’s frontal cortex: premotor ear–eye field (PEEF). Neurosci Biobehav Rev 37:1434–1444

    Google Scholar 

  • Lucchetti C, Bon L (2001) Time-modulated neuronal activity in the premotor cortex of macaque monkeys. Exp Brain Res 141(2):254–260

    Article  CAS  PubMed  Google Scholar 

  • Lucchetti C, Ulrici A, Bon L (2005) Dorsal premotor areas of nonhuman primate: functional flexibility in time domain. Eur J Appl Physiol 95(2–3):121–130

    Article  PubMed  Google Scholar 

  • Lucchetti C, Lanzilotto M, Bon L (2008) Auditory-motor and cognitive aspects in area 8B of macaque monkey’s frontal cortex: a premotor ear–eye field (PEEF). Exp Brain Res 186(1):131–141

    Article  CAS  PubMed  Google Scholar 

  • Lucchetti C, Lanzilotto M, Perciavalle V, Bon L (2012) Neuronal activity reflecting progression of trials in the pre-supplementary motor area of macaque monkey: an expression of neuronal flexibility. Neurosci Lett 506(1):33–38. doi:10.1016/j.neulet.2011.10.043

    Article  CAS  PubMed  Google Scholar 

  • Matsuzaka Y, Tanji J (1996) Changing directions of forthcoming arm movements: neuronal activity in the presupplementary and supplementary motor area of monkey cerebral cortex. J Neurophysiol 76(4):2327–2342

    CAS  PubMed  Google Scholar 

  • Mitz AR, Godschalk M (1989) Eye-movement representation in the frontal lobe of rhesus monkeys. Neurosci Lett 106(1–2):157–162. doi:10.1016/0304-3940(89)90219-X

    Article  CAS  PubMed  Google Scholar 

  • Moschovakis AK, Gregoriou GG, Ugolini G, Doldan M, Graf W, Guldin W, Hadjidimitrakis K, Savaki HE (2004) Oculomotor areas of the primate frontal lobes: a transneuronal transfer of rabies virus and [14C]-2-deoxyglucose functional imaging study. J Neurosci 24(25):5726–5740

    Article  CAS  PubMed  Google Scholar 

  • Pierrot-Deseilligny C, Milea D, Muri RM (2004) Eye movement control by the cerebral cortex. Curr Opin Neurol 17(1):17–25

    Article  PubMed  Google Scholar 

  • Plakke B, Ng CW, Poremba A (2013) Neural correlates of auditory recognition memory in primate lateral prefrontal cortex. Neuroscience 244:62–76. doi:10.1016/j.neuroscience.2013.04.002

    Article  CAS  PubMed  Google Scholar 

  • Preuss TM, Stepniewska I, Kaas JH (1996) Movement representation in the dorsal and ventral premotor areas of owl monkeys: a microstimulation study. J Comp Neurol 371(4):649–676

    Article  CAS  PubMed  Google Scholar 

  • Rauschecker JP, Romanski LM (2011) Auditory cortical organization: evidence for functional streams. In: Winer JA, Schreiner CE (eds) The auditory cortex. Springer, New York, pp 99–116. doi:10.1007/978-1-4419-0074-6_4

    Chapter  Google Scholar 

  • Remmel RS (1984) An inexpensive eye movement monitor using the scleral search coil technique. IEEE Trans Biomed Eng 31(4):388–390

    Article  CAS  PubMed  Google Scholar 

  • Romanski LM, Averbeck BB (2009) The primate cortical auditory system and neural representation of conspecific vocalizations. Annu Rev Neurosci 32(1):315–346. doi:10.1146/annurev.neuro.051508.135431

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Romanski LM, Bates JF, Goldman-Rakic PS (1999a) Auditory belt and parabelt projections to the prefrontal cortex in the Rhesus monkey. J Comp Neurol 403(2):141–157. doi:10.1002/(sici)1096-9861(19990111)403:2<141:aid-cne1>3.0.co;2-v

    Article  CAS  PubMed  Google Scholar 

  • Romanski LM, Tian B, Fritz J, Mishkin M, Goldman-Rakic PS, Rauschecker JP (1999b) Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat Neurosci 2(12):1131–1136

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sawaguchi T, Iba M (2001) Prefrontal cortical representation of visuospatial working memory in monkeys examined by local inactivation with muscimol. J Neurophysiol 86(4):2041–2053

    CAS  PubMed  Google Scholar 

  • Schall JD (ed) (1997) Visuomotor areas of the frontal lobe. Cerebral Cortex Plenum Press, New York

    Google Scholar 

  • Sparks DL, Freedman EG, Chen LL, Gandhi NJ (2001) Cortical and subcortical contributions to coordinated eye and head movements. Vision Res 41(25–26):3295–3305

    Article  CAS  PubMed  Google Scholar 

  • Stanford TR, Freedman EG, Sparks DL (1996) Site and parameters of microstimulation: evidence for independent effects on the properties of saccades evoked from the primate superior colliculus. J Neurophysiol 76(5):3360–3381

    CAS  PubMed  Google Scholar 

  • Stebbins W (1980) The evolution of hearing in the mammals. In: Popper A, Fay R (eds) Comparative studies of hearing in vertebrates. Proceedings in life sciences. Springer, New York, pp 421–436. doi:10.1007/978-1-4613-8074-0_15

    Chapter  Google Scholar 

  • Stryker MP, Schiller PH (1975) Eye and head movements evoked by electrical stimulation of monkey superior colliculus. Exp Brain Res 23(1):103–112

    Article  CAS  PubMed  Google Scholar 

  • Tehovnik EJ, Slocum WM (2004) Behavioural state affects saccades elicited electrically from neocortex. Neurosci Biobehav Rev 28(1):13–25

    Article  PubMed  Google Scholar 

  • Tehovnik EJ, Sommer MA, Chou IH, Slocum WM, Schiller PH (2000) Eye fields in the frontal lobes of primates. Brain Res Brain Res Rev 32(2–3):413–448

    Article  CAS  PubMed  Google Scholar 

  • Tehovnik EJ, Slocum WM, Carvey CE (2003) Behavioural state affects saccadic eye movements evoked by microstimulation of striate cortex. Eur J Neurosci 18(4):969–979

    Article  PubMed  Google Scholar 

  • Thier P, Andersen RA (1998) Electrical microstimulation distinguishes distinct saccade-related areas in the posterior parietal cortex. J Neurophysiol 80(4):1713–1735

    CAS  PubMed  Google Scholar 

  • Tu TA, Keating EG (2000) Electrical stimulation of the frontal eye field in a monkey produces combined eye and head movements. J Neurophysiol 84(2):1103–1106

    CAS  PubMed  Google Scholar 

  • Yeterian EH, Pandya DN (2010) Fiber pathways and cortical connections of preoccipital areas in rhesus monkeys. J Comp Neurol 518(18):3725–3751

    Article  CAS  PubMed  Google Scholar 

  • Yeterian EH, Pandya DN, Tomaiuolo F, Petrides M (2012) The cortical connectivity of the prefrontal cortex in the monkey brain. Cortex 48(1):58–81

    Article  PubMed Central  PubMed  Google Scholar 

  • Yin TC (2013) Physiological and behavioral studies of sound localization. J Acoust Soc Am 133(5):4805588

    Article  Google Scholar 

  • Yu L, Terada K, Usui N, Usui K, Baba K, Inoue Y (2010) Ear movement induced by electrical cortical stimulation. Epilepsy Behav 18(4):488–490

    Google Scholar 

Download references

Acknowledgments

This work was supported by the Department of Biomedical Sciences, University of Catania (“Progetti di Ricerca di Ateneo 2011”). We thank Professor Gianfranco Franchi for his invaluable advice; Professor Giuseppe Luppino, Dr. Stefano Rozzi, Dr. Elena Borra, and Dr. Marzio Gerbella for their help in the histological reconstruction; Dr. Chandramouli Chandrasekaran for his comments on the paper; Dr. Vasco Lolli, Mr. Vincenzo Molino, and Mr. Alfonso Guida for animal care. We also thank two anonymous reviewers for their suggestions, comments and criticisms which improved our manuscript.

Conflict of interest

The authors declare the absence of any potential conflict of interest, financial or otherwise.

Author information

Authors and Affiliations

  1. Section of Physiology and Neuroscience, Department of Biomedical Sciences, Metabolic and Neuroscience, University of Modena and Reggio Emilia, 41125, Modena, Italy

    M. Lanzilotto & C. Lucchetti

  2. Section of Polyclinic, Interdepartmental Facilities Center, University of Modena and Reggio Emilia, 41125, Modena, Italy

    M. Lanzilotto & C. Lucchetti

  3. Section of Physiology, Department of Biomedical Sciences, University of Catania, 95125, Catania, Italy

    V. Perciavalle

Authors
  1. M. Lanzilotto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. Perciavalle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Lucchetti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Lanzilotto.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lanzilotto, M., Perciavalle, V. & Lucchetti, C. Orienting movements in area 9 identified by long-train ICMS. Brain Struct Funct 220, 763–779 (2015). https://doi.org/10.1007/s00429-013-0682-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-013-0682-8

Keywords

Search

Navigation