Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Temporal structure in neuronal activity during working memory in macaque parietal cortex

Abstract

Many cortical structures have elevated firing rates during working memory, but it is not known how the activity is maintained. To investigate whether reverberating activity is important, we studied the temporal structure of local field potential (LFP) activity and spiking from area LIP in two awake macaques during a memory-saccade task. Using spectral analysis, we found spatially tuned elevated power in the gamma band (25–90 Hz) in LFP and spiking activity during the memory period. Spiking and LFP activity were also coherent in the gamma band but not at lower frequencies. Finally, we decoded LFP activity on a single-trial basis and found that LFP activity in parietal cortex discriminated between preferred and anti-preferred direction with approximately the same accuracy as the spike rate and predicted the time of a planned movement with better accuracy than the spike rate. This finding could accelerate the development of a cortical neural prosthesis.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The memory-saccade task.
Figure 2: LFP spectrograms averaged across trials during saccades to either the preferred or anti-preferred direction.
Figure 3: Tuning of spiking and LFP activity.
Figure 4: Spike spectrum.
Figure 5: Spike spectrograms.
Figure 6: Spike-triggered average potential from a single cell at a single site.
Figure 7: Coherency of spiking and LFP activity across time.
Figure 8: Single-trial decoding of a movement plan.

Similar content being viewed by others

References

  1. Fuster, J. Memory in Cerebral Cortex: An Empirical Approach to Neural Networks in the Human and Nonhuman Brain (MIT Press, Cambridge, Massachusetts, 1995).

    Google Scholar 

  2. Bruce, C.J. & Goldberg, M.E. Primate frontal eye fields: I. Single neurons discharging before saccades. J. Neurophysiol. 53, 603–635 (1985).

    Article  CAS  Google Scholar 

  3. Gnadt, J.W. & Andersen, R.A. Memory related motor planning activity in posterior parietal cortex of macaque. Exp. Brain Res. 70, 216–220 (1988).

    CAS  PubMed  Google Scholar 

  4. Koch, K.W. & Fuster, J.M. Unit activity in monkey parietal cortex related to haptic perception and temporary memory. Exp. Brain Res. 76, 292–306 (1989).

    Article  CAS  Google Scholar 

  5. Miller, E.K., Erickson, C.A. & Desimone, R. Neural mechanisms of visual working memory in prefrontal cortex of the macaque. J. Neurosci. 16, 5154–5167 (1996).

    Article  CAS  Google Scholar 

  6. Andersen, R.A. Encoding of intention and spatial location in the posterior parietal cortex. Cereb. Cortex 5, 457–469 (1995).

    Article  CAS  Google Scholar 

  7. Funahashi, S., Bruce, C.J. & Goldman-Rakic, P.S. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J. Neurophysiol. 61, 331–349 (1989).

    Article  CAS  Google Scholar 

  8. Mazzoni, P., Bracewell, R.M., Barash, S. & Andersen, R.A. Motor intention activity in the macaque's lateral intraparietal area. I. Dissociation of motor plan from sensory memory. J. Neurophysiol. 76, 1439–1456 (1996).

    Article  CAS  Google Scholar 

  9. Snyder, L.H., Batista, A.P. & Andersen, R.A. Coding of intention in the posterior parietal cortex. Nature 386, 167–170 (1997).

    Article  CAS  Google Scholar 

  10. Goldman-Rakic, P.S. Cellular basis of working memory. Neuron 14, 477–485 (1995).

    Article  CAS  Google Scholar 

  11. Seung, H.S. How the brain keeps the eyes still. Proc. Natl. Acad. Sci. USA 93, 13339–13344 (1996).

    Article  CAS  Google Scholar 

  12. Wang, X.-J. Synaptic basis of cortical persistent activity: the importance of NMDA receptors to working memory. J. Neurosci. 19, 9587–9603 (1999).

    Article  CAS  Google Scholar 

  13. Hebb, D. Organization of Behavior (Wiley, New York, 1949).

    Google Scholar 

  14. Amit, D.J. The hebbian paradigm reintegrated: local reverberations as internal representation. Behav. Brain Sci. 18, 617–626 (1995).

    Article  Google Scholar 

  15. Eckhorn, R., Frien, A., Bauer, R., Woelbern, T. & Kehr, H. High-frequency (60–90 Hz) oscillations in primary visual cortex of awake monkey. Neuroreport 4, 243–246 (1993).

    Article  CAS  Google Scholar 

  16. Gray, C.M. & Singer, W. Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc. Natl. Acad. Sci. USA 86, 1698–1702 (1989).

    Article  CAS  Google Scholar 

  17. Gray, C.M., Konig, P., Engel, A.K. & Singer, W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338, 334–337 (1989).

    Article  CAS  Google Scholar 

  18. Kreiter, A.K. & Singer, W. Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey. J. Neurosci. 16, 2381–2396 (1996).

    Article  CAS  Google Scholar 

  19. Fries, P., Reynolds, J.H., Rorie, A.E. & Desimone, R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291, 1560–1563 (2001).

    Article  CAS  Google Scholar 

  20. Steinmetz, P.N. et al. Attention modulates synchronized neuronal firing in primate somatosensory cortex. Nature 404, 187–190 (2000).

    Article  CAS  Google Scholar 

  21. Rougeul, A., Bouyer, J.J., Dedet, L. & Debray, O. Fast somato-parietal rhythms during combined focal attention and immobility in baboon and squirrel monkey. Electro. Clin. Neurophysiol. 46, 310–319 (1979).

    Article  CAS  Google Scholar 

  22. Bressler, S.L., Coppola, R. & Nakamura, R. Episodic multiregional cortical coherence at multiple frequencies during visual task-performance. Nature 366, 153–156 (1993).

    Article  CAS  Google Scholar 

  23. Murthy, V.N. & Fetz, E.E. Oscillatory activity in sensorimotor cortex of awake monkeys: synchronization of local field potentials and relation to behavior. J. Neurophysiol. 76, 3949–3967 (1996).

    Article  CAS  Google Scholar 

  24. Roelfsema, P.R., Engel, A.K., Konig, P. & Singer, W. Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385, 157–161 (1997).

    Article  CAS  Google Scholar 

  25. Donoghue, J.P., Sanes, J.N., Hatsopoulos, N.G. & Gaal, G. Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. J. Neurophysiol. 79, 159–173 (1998).

    Article  CAS  Google Scholar 

  26. Lebedev, M.A. & Wise, S.P. Oscillations in the premotor cortex: single-unit activity from awake, behaving monkeys. Exp. Brain Res. 130, 195–215 (2000).

    Article  CAS  Google Scholar 

  27. Nakamura, K., Mikami, A. & Kubota, K. Oscillatory neuronal-activity related to visual short-term memory in monkey temporal pole. Neuroreport 3, 117–120 (1992).

    Article  CAS  Google Scholar 

  28. Tallon-Baudry, C., Bertrand, O., Peronnet, F. & Pernier, J. Induced gamma-band activity during the delay of a visual short-term memory task in humans. J. Neurosci. 18, 4244–4254 (1998).

    Article  CAS  Google Scholar 

  29. Chaffee, M.V. & Goldman-Rakic, P.S. Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip during a spatial working memory task. J. Neurophysiol. 79, 2919–2940 (1998).

    Article  Google Scholar 

  30. Mitzdorf, U. Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol. Rev. 65, 37–100 (1985).

    Article  CAS  Google Scholar 

  31. Engel, A.K., Konig, P., Gray, C.M. & Singer, W. Stimulus-dependent neuronal oscillations in cat visual-cortex - intercolumnar interaction as determined by cross-correlation analysis. Eur. J. Neurosci. 2, 588–606 (1990).

    Article  Google Scholar 

  32. Singer, W. & Gray, C.M. Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18, 555–586 (1995).

    Article  CAS  Google Scholar 

  33. Pezaris, J.S., Sahani, M. & Andersen, R.A. Response-locked changes in auto- and cross-covariations in parietal cortex. Neurocomputing 2627, 471–476 (1999).

    Article  Google Scholar 

  34. Jarvis, M.R. & Mitra, P.P. Sampling properties of the spectrum and coherency of sequences of action potentials. Neural Comput. 13, 717–749 (2001).

    Article  CAS  Google Scholar 

  35. Thomson, D.J. Spectrum estimation and harmonic analysis. Proc. IEEE 70, 1055–1996 (1982).

    Article  Google Scholar 

  36. Percival, D.B. & Walden, A.T. Spectral Analysis for Physical Applications (Cambridge University Press, Cambridge, 1993).

    Book  Google Scholar 

  37. Mitra, P.P. & Pesaran, B. Analysis of dynamic brain imaging data. Biophys. J. 76, 691–708 (1999).

    Article  CAS  Google Scholar 

  38. Blatt, G., Andersen, R.A. & Stoner, G. Visual receptive field organization and cortico-cortical connections of area LIP in the macaque. J. Comp. Neurol. 299, 421–445 (1990).

    Article  CAS  Google Scholar 

  39. Wessberg, J. et al. Real-time prediction of hand trajectory by ensembles of cortical neurons in primates. Nature 408, 361–365 (2000).

    Article  CAS  Google Scholar 

  40. Colby, C.L. & Goldberg, M.E. Space and attention in parietal cortex. Annu. Rev. Neurosci. 22, 319–349 (1999).

    Article  CAS  Google Scholar 

  41. Wehr, M. & Laurent, G. Odour encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384, 162–166 (1996).

    Article  CAS  Google Scholar 

  42. Pezaris, J.S., Sahani, M. & Andersen, R.A. in Computational Neuroscience: Trends in Research (ed. Bower, J. M.) 937–942 (Plenum, New York, 1996).

    Google Scholar 

  43. Sahani, M., Pezaris, J.S. & Andersen, R.A. in Advances in Neural Information Processing Systems 10 (eds. Jordan, M. I., Kearns, M. J. & Solla, S. A.) 222–228 (MIT Press, Cambridge, Massachusetts, 1998).

    Google Scholar 

  44. Brillinger, D.R. Time Series (Holt, Rinehart and Winston, New York, 1974).

    Google Scholar 

  45. Efron, B. & Tibshirani, R.J. An Introduction to the Bootstrap (Chapman and Hall, London, 1993).

    Book  Google Scholar 

  46. Thomson, D.J. & Chave, A.D. Advances in Spectrum Analysis and Array Processing (Prentice Hall, Englewood Cliffs, New Jersey, 1991).

    Google Scholar 

  47. Ripley, B.D. Pattern Recognition and Neural Networks (Cambridge University Press, Cambridge, 1996).

    Book  Google Scholar 

Download references

Acknowledgements

This work was supported by the DARPA grant MDA972-00-1-0029, NIH grants EY05522-21 and MH62528-01, ONR grant N00014-94-0412, the Keck Foundation, the McKnight Foundation, the Sloan-Swartz Foundation, the Center for Neuromorphic Systems Engineering at Caltech and the Workshop for the Analysis of Neural Data (http://www.vis.caltech.edu/~WAND).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard A. Andersen.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pesaran, B., Pezaris, J., Sahani, M. et al. Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat Neurosci 5, 805–811 (2002). https://doi.org/10.1038/nn890

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn890

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing