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:

Generalized associative representations in parietal cortex

Nature Neuroscience volume 14, pages 1075–1079 (2011)Cite this article

Subjects

Abstract

Making associations between sensory stimuli is a critical aspect of behavior. We previously found that neurons in the lateral intraparietal area (LIP) of Macaca mulatta reflect learned associations between directions of moving visual stimuli. Individual LIP neurons might encode associations only for specific stimuli, such as motion directions; alternatively, they may encode more general associations whenever animals must decide between discrete alternatives. To test this, we asked whether LIP neurons encode learned associations between pairs of arbitrarily chosen static shapes and, in a separate task, whether the same neurons also encode associations between motion directions. Our experimental design dissociated the visual associations from the movements used to report those associations. We found robust encoding of the learned pair associations between shapes, and shape-pair–selective neurons tended to be selective for direction associations. These findings suggest that representing generic categorical outcomes may be a fundamental role of parietal neurons.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Behavioral task.
Figure 2: Example responses of LIP neurons.
Figure 3: Shape-pair selectivity across the population of LIP neurons.
Figure 4: Delayed direction-categorization task.
Figure 5: Selectivity for shape pairs and direction categories.

Similar content being viewed by others

References

  1. Miller, E.K., Freedman, D.J. & Wallis, J.D. The prefrontal cortex: categories, concepts and cognition. Phil. Trans. R. Soc. Lond. B 357, 1123–1136 (2002).

    Article  Google Scholar 

  2. Osada, T. et al. Towards understanding of the cortical network underlying associative memory. Phil. Trans. R. Soc. Lond. B 363, 2187–2199 (2008).

    Article  Google Scholar 

  3. Freedman, D.J. & Assad, J.A. Experience-dependent representation of visual categories in parietal cortex. Nature 443, 85–88 (2006).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  5. Lewis, J.W. & Van Essen, D.C. Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J. Comp. Neurol. 428, 112–137 (2000).

    Article  CAS  PubMed  Google Scholar 

  6. Shadlen, M.N. & Newsome, W.T. Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. J. Neurophysiol. 86, 1916–1936 (2001).

    Article  CAS  PubMed  Google Scholar 

  7. Roitman, J.D. & Shadlen, M.N. Response of neurons in the lateral intraparietal area during a combined visual discrimination reaction time task. J. Neurosci. 22, 9475–9489 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Churchland, A.K., Kiani, R. & Shadlen, M.N. Decision-making with multiple alternatives. Nat. Neurosci. 11, 693–702 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Gold, J.I. & Shadlen, M.N. The neural basis of decision making. Annu. Rev. Neurosci. 30, 535–574 (2007).

    Article  CAS  PubMed  Google Scholar 

  10. Sereno, A.B. & Maunsell, J.H. Shape selectivity in primate lateral intraparietal cortex. Nature 395, 500–503 (1998).

    Article  CAS  PubMed  Google Scholar 

  11. Janssen, P. et al. Coding of shape and position in macaque lateral intraparietal area. J. Neurosci. 28, 6679–6690 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Toth, L.J. & Assad, J.A. Dynamic coding of behaviourally relevant stimuli in parietal cortex. Nature 415, 165–168 (2002).

    Article  CAS  PubMed  Google Scholar 

  13. Platt, M.L. & Glimcher, P.W. Neural correlates of decision variables in parietal cortex. Nature 400, 233–238 (1999).

    Article  CAS  PubMed  Google Scholar 

  14. Maunsell, J.H. Neuronal representations of cognitive state: reward or attention? Trends Cogn. Sci. 8, 261–265 (2004).

    Article  PubMed  Google Scholar 

  15. Herrington, T.M. et al. The effect of microsaccades on the correlation between neural activity and behavior in middle temporal, ventral intraparietal, and lateral intraparietal areas. J. Neurosci. 29, 5793–5805 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. 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 

  17. Freedman, D.J. & Assad, J.A. Distinct encoding of spatial and nonspatial visual information in parietal cortex. J. Neurosci. 29, 5671–5680 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Sakai, K. & Miyashita, Y. Neural organization for the long-term memory of paired associates. Nature 354, 152–155 (1991).

    Article  CAS  PubMed  Google Scholar 

  19. Messinger, A. et al. Neuronal representations of stimulus associations develop in the temporal lobe during learning. Proc. Natl. Acad. Sci. USA 98, 12239–12244 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Naya, Y. et al. Delay-period activities in two subdivisions of monkey inferotemporal cortex during pair association memory task. Eur. J. Neurosci. 18, 2915–2918 (2003).

    Article  PubMed  Google Scholar 

  21. Rainer, G., Rao, S.C. & Miller, E.K. Prospective coding for objects in primate prefrontal cortex. J. Neurosci. 19, 5493–5505 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Schlack, A. & Albright, T.D. Remembering visual motion: neural correlates of associative plasticity and motion recall in cortical area MT. Neuron 53, 881–890 (2007).

    Article  CAS  PubMed  Google Scholar 

  23. Born, R.T. & Bradley, D.C. Structure and function of visual area MT. Annu. Rev. Neurosci. 28, 157–189 (2005).

    Article  CAS  PubMed  Google Scholar 

  24. Mishkin, M., Ungerleider, L.G. & Macko, K.A. Object vision and spatial vision: two cortical pathways. Trends Neurosci. 6, 414–417 (1983).

    Article  Google Scholar 

  25. Ferrera, V.P. & Grinband, J. Walk the line: parietal neurons respect category boundaries. Nat. Neurosci. 9, 1207–1208 (2006).

    Article  CAS  PubMed  Google Scholar 

  26. Nieder, A., Diester, I. & Tudusciuc, O. Temporal and spatial enumeration processes in the primate parietal cortex. Science 313, 1431–1435 (2006).

    Article  CAS  PubMed  Google Scholar 

  27. Tudusciuc, O. & Nieder, A. Neuronal population coding of continuous and discrete quantity in the primate posterior parietal cortex. Proc. Natl. Acad. Sci. USA 104, 14513–14518 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Tudusciuc, O. & Nieder, A. Contributions of primate prefrontal and posterior parietal cortices to length and numerosity representation. J. Neurophysiol. 101, 2984–2994 (2009).

    Article  PubMed  Google Scholar 

  29. Vallentin, D. & Nieder, A. Representations of visual proportions in the primate posterior parietal and prefrontal cortices. Eur. J. Neurosci. 32, 1380–1387 (2010).

    Article  PubMed  Google Scholar 

  30. Freedman, D.J. & Assad, J.A. A proposed common neural mechanism for categorization and perceptual decisions. Nat. Neurosci. 14, 143–146 (2011).

    Article  CAS  PubMed  Google Scholar 

  31. Shadlen, M.N., Roozbeh, K., Hanks, T.D. & Churchland, A.K. Neurobiology of decision making: an intentional framework. in Better Than Conscious? Decision Making, the Human Mind, and Implications for Institutions (eds. Engel, C. & Singer, W.) 71–102 (MIT Press, Cambridge, Massachusetts, 2008).

  32. Bennur, S. & Gold, J.I. Distinct representations of a perceptual decision and the associated oculomotor plan in the monkey lateral intraparietal area. J. Neurosci. 31, 913–921 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Goldberg, M.E. et al. Saccades, salience and attention: the role of the lateral intraparietal area in visual behavior. Prog. Brain Res. 155, 157–175 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Andersen, R.A. & Buneo, C.A. Intentional maps in posterior parietal cortex. Annu. Rev. Neurosci. 25, 189–220 (2002).

    Article  CAS  PubMed  Google Scholar 

  35. Fanini, A. & Assad, J.A. Direction selectivity of neurons in the macaque lateral intraparietal area. J. Neurophysiol. 101, 289–305 (2009).

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank J. Maunsell, M. Livingstone, R. Born, R. Wilson, D. Zaksas, D. Ruff, G. Kreiman, J. Ware and the Harvard Catalyst Program for comments and discussions, and K. Irwin, J. LeBlanc, T. Lafratta and C. Ponce for technical assistance. This work was supported by National Eye Institute grant EY-12106 (J.A.A.), Vision Core grant EY-12196, a National Institute of Mental Health Predoctoral National Research Service Award (F31 MH085439, J.K.F.), The Edward R. and Anne G. Lefler Center for the Study of Neurodegenerative Disorders Predoctoral Fellowship (J.K.F.) and a Charles H. Hood Postdoctoral Fellowship (D.J.F.).

Author information

Authors and Affiliations

  1. Department of Neurobiology, Harvard Medical School, Boston, Massachusetts, USA

    Jamie K Fitzgerald, David J Freedman & John A Assad

  2. Department of Neurobiology, The University of Chicago, Chicago, Illinois, USA

    David J Freedman

  3. Center for Neuroscience and Cognitive Systems@UniTn, Istituto Italiano di Tecnologia, Rovereto, Italy

    John A Assad

Authors
  1. Jamie K Fitzgerald
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David J Freedman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John A Assad
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.K.F., D.J.F. and J.A.A. designed the experiments. J.K.F. collected and analyzed the data and wrote the manuscript. D.J.F. and J.A.A. assisted in data analysis and manuscript preparation.

Corresponding author

Correspondence to John A Assad.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Results, Supplementary Tables 1–5 and Supplementary Figure 1 (PDF 290 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fitzgerald, J., Freedman, D. & Assad, J. Generalized associative representations in parietal cortex. Nat Neurosci 14, 1075–1079 (2011). https://doi.org/10.1038/nn.2878

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2878

This article is cited by

Search

Advanced 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