Skip to main content

Advertisement

Log in

Neural activity in prefrontal cortex during copying geometrical shapes

I. Single cells encode shape, sequence, and metric parameters

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

Abstract

In drawing a copy of a geometrical shape, a sequence of movements must be produced to represent the sides of the object in the proper spatial relationship. We investigated neural mechanisms of this process by training monkeys to draw (using a joystick) copies of geometrical shapes (triangles, squares, trapezoids and inverted triangles) presented on a video monitor while recording single cell activity in prefrontal cortex. The drawing trajectories monkeys produced were divided into a series of discrete segments, varying in direction and length. We performed a stepwise multiple linear regression analysis to identify those copy parameters significantly influencing cell activity. The copied shape (e.g., triangle, square) and the serial position of the segment within each trajectory were the most prevalent effects (in 46% and 43% of cells, respectively), followed by segment direction (32%) and length (16%). Effects of temporal factors (maximum segment speed and time to maximum segment speed) were less frequent. These results demonstrate that prefrontal neurons encode several spatial and sequence variables that define copy trajectories. We also found that specific groupings of significant effects tended to occur together in single neurons. Specifically, single neurons simultaneously processed the serial position of a segment within each trajectory along with the corresponding spatial (but not temporal) attributes of that segment (i.e., direction and length), as well as with the overall shape to which the segments belong. Finally, we discovered that relationships between neural activity and segment serial position were systematic in many instances, described by monotonically increasing and decreasing functions, as well as parabolic functions. These findings indicate that, within the copying task, the serial segment position is a key factor for neural activity in the periprincipalis area of the prefrontal cortex.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1A, B.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.
Fig. 9.
Fig. 10.
Fig. 11.
Fig. 12.
Fig. 13.
Fig. 14.
Fig. 15.
Fig. 16.

Similar content being viewed by others

References

  • Armitage P, Berry G (1987) Statistical methods in medical research. Blackwell Scientific, Oxford

  • Averbeck BB, Chafee MV, Crowe DA, Georgopoulos AP (2001) Single unit activity related to serial order during copying of geometric shapes. Soc Neurosci Abstr 467.2

  • Averbeck BB, Crowe DA, Chafee MV, Georgopoulos AP (2003) Neural activity in prefrontal cortex during copying geometrical shapes. II. Decoding shape segments from neural ensembles. Exp Brain Res (in press)

  • Barbas H (1988) Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey. J Comp Neurol 276:313–342

    Google Scholar 

  • Barone P, Joseph JP (1989) Prefrontal cortex and spatial sequencing in macaque monkey. Exp Brain Res 78:447–464

    CAS  PubMed  Google Scholar 

  • Benson DF, Barton MI (1970) Disturbances in constructional ability. Cortex 6:19–46

    CAS  PubMed  Google Scholar 

  • Benton AL (1968) Differential behavioral effects in frontal lobe disease. Neuropsychologia 6:53–60

    Article  Google Scholar 

  • Bernstein N (1967) The co-ordination and regulation of movements. Pergamon, Oxford

  • Boussaoud D, Wise SP (1993a) Primate frontal cortex: effects of stimulus and movement. Exp Brain Res 95:28–40

    CAS  PubMed  Google Scholar 

  • Boussaoud D, Wise SP (1993b) Primate frontal cortex: neuronal activity following attentional versus intentional cues. Exp Brain Res 95:15–27

    CAS  PubMed  Google Scholar 

  • Carpenter AF, Georgopoulos AP, Pellizzer G (1999) Motor cortical encoding of serial order in a context-recall task. Science 283:1752–1757

    CAS  PubMed  Google Scholar 

  • Clower WT, Alexander GE (1998) Movement sequence-related activity reflecting numerical order of components in supplementary and presupplementary motor areas. J Neurophysiol 80:1562–1566

    CAS  PubMed  Google Scholar 

  • di Pellegrino G, Wise SP (1993) Visuospatial versus visuomotor activity in the premotor and prefrontal cortex of a primate. J Neurosci 13:1227–1243

    PubMed  Google Scholar 

  • Draper NR, Smith H (1998) Applied regression analysis. John Wiley and Sons, New York

  • Fuchs AF, Robinson DA (1966) A method for measuring horizontal and vertical eye movement chronically in the monkey. J Appl Physiol 21:1068–1070

    CAS  PubMed  Google Scholar 

  • Funahashi S, Inoue M, Kubota K (1997) Delay-period activity in the primate prefrontal cortex encoding multiple spatial positions and their order of presentation. Behav Brain Res 84:203–223

    CAS  PubMed  Google Scholar 

  • Gainotti G (1985) Constructional apraxia. In: Frederiks JAM (ed) Handbook of clinical neurology, vol 1. Elsevier, Amsterdam, pp 491–506

  • Goldman-Rakic PS (1987) Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. In: Mountcastle VB, Plum F, Geiger SR (eds) Handbook of physiology. The nervous system. Higher functions of the brain, sect. 1, vol. V, chap. 9. American Physiological Society, Bethesda, MD, pp 373–417

  • Goldman-Rakic PS, Bates JF, Chafee MV (1992) The prefrontal cortex and internally generated motor acts. Curr Opin Neurobiol 2:830–835

    CAS  PubMed  Google Scholar 

  • Hoshi E, Shima K, Tanji J (2000) Neuronal activity in the primate prefrontal cortex in the process of motor selection based on two behavioral rules. J Neurophysiol 83:2355–2373

    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 20:535–538

    CAS  PubMed  Google Scholar 

  • Keele S (1981) Behavioral analysis of movement. In: V B (ed) Handbook of physiology, vol 2. American Physiological Society, Baltimore, MD, pp 1391–1414

  • Kermadi I, Joseph JP (1995) Activity in the caudate nucleus of monkey during spatial sequencing. J Neurophysiol 74:911–933

    PubMed  Google Scholar 

  • Kermadi I, Jurquet Y, Arzi M, Joseph JP (1993) Neural activity in the caudate nucleus of monkeys during spatial sequencing. Exp Brain Res 94:352–356

    CAS  PubMed  Google Scholar 

  • Kettner RE, Marcario JK, Port NL (1996) Control of remembered reaching sequences in monkey. II. Storage and preparation before movement in motor and premotor cortex. Exp Brain Res 112:347–358

    CAS  PubMed  Google Scholar 

  • Kleist K (1934) Gehirnpathologie. Barth, Leipzig

  • Koski L, Iacoboni M, Mazziotta JC (2002) Deconstructing apraxia: understanding disorders of intentional movement after stroke. Curr Opin Neurol 15:71–77

    Article  PubMed  Google Scholar 

  • Kubota K, Funahashi S (1982) Direction-specific activities of dorsolateral prefrontal and motor cortex pyramidal tract neurons during visual tracking. J Neurophysiol 47:362–376

    CAS  PubMed  Google Scholar 

  • Lee D, Port NL, Kruse W, Georgopoulos AP (1998) Neuronal population coding: multielectrode recordings in primate cerebral cortex. In: Eichenbaum H, Davis J (eds) Neuronal ensembles: strategies for recording and decoding. Wiley, New York

    Google Scholar 

  • Levy R, Goldman-Rakic PS (1999) Association of storage and processing functions in the dorsolateral prefrontal cortex of the nonhuman primate. J Neurosci 19:5149–5158

    Google Scholar 

  • Lu MT, Preston JB, Strick PL (1994) Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe. J Comp Neurol 341:375–392

    CAS  PubMed  Google Scholar 

  • Lu X, Matsuzawa M, Hikosaka O (2002) A neural correlate of oculomotor sequences in supplementary eye field. Neuron 34:317–325

    CAS  PubMed  Google Scholar 

  • Luria A (1966) Higher cortical functions in man. Basic Books, New York

  • Luria AR, Tsvetkova LS (1964) The programming of constructive ability in local brain injuries. Neuropsychologia 2:95–107

    Article  Google Scholar 

  • Massey JT, Lurito JT, Pellizzer G, Georgopoulos AP (1992) Three-dimensional drawings in isometric conditions: relation between geometry and kinematics. Exp Brain Res 88:685–690

    CAS  PubMed  Google Scholar 

  • Milner TE, Ijaz MM (1990) The effect of accuracy constraints on three-dimensional movement kinematics. Neuroscience 35:365–374

    CAS  PubMed  Google Scholar 

  • Morasso P (1983) Three dimensional arm trajectories. Biol Cybern 48:187–194

    CAS  PubMed  Google Scholar 

  • Mottet D, Bardy BG, Athenes S (1994) A note on data smoothing for movement analysis: the relevance of a nonlinear method. J Motor Behav 26:51–55

    Google Scholar 

  • Mountcastle VB, Reitboeck HJ, Poggio GF, Steinmetz MA (1991) Adaptation of the Reitboeck method of multiple microelectrode recording to the neocortex of the waking monkey. J Neurosci Methods 36:77–84

    CAS  PubMed  Google Scholar 

  • Mushiake H, Strick PL (1995) Pallidal neuron activity during sequential arm movements. J Neurophysiol 74:2754–2758

    PubMed  Google Scholar 

  • Mushiake H, Inase M, Tanji J (1990) Selective coding of motor sequence in the supplementary motor area of the monkey cerebral cortex. Exp Brain Res 82:208–210

    CAS  PubMed  Google Scholar 

  • Mushiake H, Inase M, Tanji J (1991) Neuronal activity in the primate premotor, supplementary, and precentral motor cortex during visually guided and internally determined sequential movements. J Neurophysiol 66:705–718

    PubMed  Google Scholar 

  • Nakamura K, Sakai K, Hikosaka O (1999) Effects of local inactivation of monkey medial frontal cortex in learning of sequential procedures. J Neurophysiol 82:1063–1068

    CAS  PubMed  Google Scholar 

  • Niki H (1974a) Prefrontal unit activity during delayed alternation in the monkey. I. Relation to direction of response. Brain Res 68:185–196

    CAS  PubMed  Google Scholar 

  • Niki H (1974b) Prefrontal unit activity during delayed alternation in the monkey. II. Relation to absolute versus relative direction of response. Brain Res 68:197–204

    CAS  PubMed  Google Scholar 

  • Pellizzer G, Massey JT, Lurito JT, Georgopoulos AP (1992) Three-dimensional drawings in isometric conditions: planar segmentation of force trajectory. Exp Brain Res 92:326–337

    CAS  PubMed  Google Scholar 

  • Petrides M (1991) Functional specialization within the dorsolateral frontal cortex for serial order memory. Proc R Soc Lond B Biol Sci 246:299–306

    CAS  PubMed  Google Scholar 

  • Poppelreuter W (1917) Die psychische Schadigungen durch Kopfschuss im Kriege, vol. 1. Voss, Leipzig

  • Rabiner LR, Gold B (1975) Theory and application of digital signal processing. Prentice-Hall, New Jersey

  • Schwartz MF, Reed ES, Montgomery M, Palmer C, Mayer NH (1991) The quantitative description of action disorganization after brain damage: a case study. Cogn Neuropsychol 8:381–414

    Google Scholar 

  • Shallice T (1982) Specific impairments of planning. Philos Trans R Soc Lond B Biol Sci 298:199–209

    CAS  PubMed  Google Scholar 

  • Shima K, Tanji J (2000) Neuronal activity in the supplementary and presupplementary motor areas for temporal organization of multiple movements. J Neurophysiol 84:2148–2160

    CAS  PubMed  Google Scholar 

  • Soechting JF, Terzuolo CA (1987a) Organization of arm movements in three-dimensional space. Wrist motion is piecewise planar. Neuroscience 23:53–61

    CAS  PubMed  Google Scholar 

  • Soechting JF, Terzuolo CA (1987b) Organization of arm movements. Motion is segmented. Neuroscience 23:39–51

    CAS  PubMed  Google Scholar 

  • Viviani P, Cenzato M (1985) Segmentation and coupling in complex movements. J Exp Psychol Hum Percept Perform 11:828–845

    Google Scholar 

  • Wright CE (1990) Generalized motor programs: reexamining claims of effector independence in writing. In: Jeannerod M (ed) Attention and performance XIII. Lawrence Erlbaum Associates, Hillsdale, NJ, pp 294–320

Download references

Acknowledgements

This work was supported by United States Public Health Service grant NS17413, the United States Department of Veterans Affairs, and the American Legion Brain Sciences Chair.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Apostolos P. Georgopoulos.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Averbeck, B.B., Chafee, M.V., Crowe, D.A. et al. Neural activity in prefrontal cortex during copying geometrical shapes. Exp Brain Res 150, 127–141 (2003). https://doi.org/10.1007/s00221-003-1416-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-003-1416-6

Keywords

Navigation