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
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Fuster, J. Memory in Cerebral Cortex: An Empirical Approach to Neural Networks in the Human and Nonhuman Brain (MIT Press, Cambridge, Massachusetts, 1995).
Bruce, C.J. & Goldberg, M.E. Primate frontal eye fields: I. Single neurons discharging before saccades. J. Neurophysiol. 53, 603–635 (1985).
Gnadt, J.W. & Andersen, R.A. Memory related motor planning activity in posterior parietal cortex of macaque. Exp. Brain Res. 70, 216–220 (1988).
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).
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).
Andersen, R.A. Encoding of intention and spatial location in the posterior parietal cortex. Cereb. Cortex 5, 457–469 (1995).
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).
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).
Snyder, L.H., Batista, A.P. & Andersen, R.A. Coding of intention in the posterior parietal cortex. Nature 386, 167–170 (1997).
Goldman-Rakic, P.S. Cellular basis of working memory. Neuron 14, 477–485 (1995).
Seung, H.S. How the brain keeps the eyes still. Proc. Natl. Acad. Sci. USA 93, 13339–13344 (1996).
Wang, X.-J. Synaptic basis of cortical persistent activity: the importance of NMDA receptors to working memory. J. Neurosci. 19, 9587–9603 (1999).
Hebb, D. Organization of Behavior (Wiley, New York, 1949).
Amit, D.J. The hebbian paradigm reintegrated: local reverberations as internal representation. Behav. Brain Sci. 18, 617–626 (1995).
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).
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).
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).
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).
Fries, P., Reynolds, J.H., Rorie, A.E. & Desimone, R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291, 1560–1563 (2001).
Steinmetz, P.N. et al. Attention modulates synchronized neuronal firing in primate somatosensory cortex. Nature 404, 187–190 (2000).
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).
Bressler, S.L., Coppola, R. & Nakamura, R. Episodic multiregional cortical coherence at multiple frequencies during visual task-performance. Nature 366, 153–156 (1993).
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).
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).
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).
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).
Nakamura, K., Mikami, A. & Kubota, K. Oscillatory neuronal-activity related to visual short-term memory in monkey temporal pole. Neuroreport 3, 117–120 (1992).
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).
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).
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).
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).
Singer, W. & Gray, C.M. Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18, 555–586 (1995).
Pezaris, J.S., Sahani, M. & Andersen, R.A. Response-locked changes in auto- and cross-covariations in parietal cortex. Neurocomputing 26–27, 471–476 (1999).
Jarvis, M.R. & Mitra, P.P. Sampling properties of the spectrum and coherency of sequences of action potentials. Neural Comput. 13, 717–749 (2001).
Thomson, D.J. Spectrum estimation and harmonic analysis. Proc. IEEE 70, 1055–1996 (1982).
Percival, D.B. & Walden, A.T. Spectral Analysis for Physical Applications (Cambridge University Press, Cambridge, 1993).
Mitra, P.P. & Pesaran, B. Analysis of dynamic brain imaging data. Biophys. J. 76, 691–708 (1999).
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).
Wessberg, J. et al. Real-time prediction of hand trajectory by ensembles of cortical neurons in primates. Nature 408, 361–365 (2000).
Colby, C.L. & Goldberg, M.E. Space and attention in parietal cortex. Annu. Rev. Neurosci. 22, 319–349 (1999).
Wehr, M. & Laurent, G. Odour encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384, 162–166 (1996).
Pezaris, J.S., Sahani, M. & Andersen, R.A. in Computational Neuroscience: Trends in Research (ed. Bower, J. M.) 937–942 (Plenum, New York, 1996).
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).
Brillinger, D.R. Time Series (Holt, Rinehart and Winston, New York, 1974).
Efron, B. & Tibshirani, R.J. An Introduction to the Bootstrap (Chapman and Hall, London, 1993).
Thomson, D.J. & Chave, A.D. Advances in Spectrum Analysis and Array Processing (Prentice Hall, Englewood Cliffs, New Jersey, 1991).
Ripley, B.D. Pattern Recognition and Neural Networks (Cambridge University Press, Cambridge, 1996).
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
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nn890
This article is cited by
-
Control of working memory by phase–amplitude coupling of human hippocampal neurons
Nature (2024)
-
Resting Frontal Gamma Power is Associated with Both Expressive Language and Non-verbal Cognitive Abilities in Young Autistic Children
Journal of Autism and Developmental Disorders (2024)
-
Respiration organizes gamma synchrony in the prefronto-thalamic network
Scientific Reports (2023)
-
Neuronal selectivity for stimulus information determines prefrontal LFP gamma power regardless of task execution
Communications Biology (2023)
-
Adaptive coding across visual features during free-viewing and fixation conditions
Nature Communications (2023)