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:

A shared inhibitory circuit for both exogenous and endogenous control of stimulus selection

Nature Neuroscience volume 16, pages 473–478 (2013)Cite this article

Subjects

Abstract

The mechanisms by which the brain suppresses distracting stimuli to control the locus of attention are unknown. We found that focal, reversible inactivation of a single inhibitory circuit in the barn owl midbrain tegmentum, the nucleus isthmi pars magnocellularis (Imc), abolished both stimulus-driven (exogenous) and internally driven (endogenous) competitive interactions in the optic tectum (superior colliculus in mammals), which are vital to the selection of a target among distractors in behaving animals. Imc neurons transformed spatially precise multisensory and endogenous input into powerful inhibitory output that suppressed competing representations across the entire tectal space map. We identified a small, but highly potent, circuit that is employed by both exogenous and endogenous signals to exert competitive suppression in the midbrain selection network. Our findings reveal, to the best of our knowledge, for the first time, a neural mechanism for the construction of a priority map that is critical for the selection of the most important stimulus for gaze and attention.

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: Anatomy of the Imc and optic tectum.
Figure 2: Exogenous competitive inhibition in the OTid abolished by Imc blockade.
Figure 3: The Imc mediates space-specific, sensory modality–independent and switch-like exogenous competitive inhibition in the OTid.
Figure 4: The Imc mediates competitor strength–dependent exogenous inhibition in the OTid.
Figure 5: Endogenous competitive inhibition in the OTid abolished by Imc blockade.
Figure 6: The Imc mediates space-specific, sensory modality–independent endogenous competitive inhibition in the OTid.

Similar content being viewed by others

References

  1. Fecteau, J.H. & Munoz, D.P. Salience, relevance, and firing: a priority map for target selection. Trends Cogn. Sci. 10, 382–390 (2006).

    Article  Google Scholar 

  2. Awh, E., Belopolsky, A.V. & Theeuwes, J. Top-down versus bottom-up attentional control: a failed theoretical dichotomy. Trends Cogn. Sci. 16, 437–443 (2012).

    Article  Google Scholar 

  3. Reynolds, J.H. & Chelazzi, L. Attentional modulation of visual processing. Annu. Rev. Neurosci. 27, 611–647 (2004).

    Article  CAS  Google Scholar 

  4. Bisley, J.W. The neural basis of visual attention. J. Physiol. (Lond.) 589, 49–57 (2011).

    Article  CAS  Google Scholar 

  5. Gazzaley, A., Cooney, J.W., Rissman, J. & D′Esposito, M. Top-down suppression deficit underlies working memory impairment in normal aging. Nat. Neurosci. 8, 1298–1300 (2005).

    Article  CAS  Google Scholar 

  6. McMains, S. & Kastner, S. Interactions of top-down and bottom-up mechanisms in human visual cortex. J. Neurosci. 31, 587–597 (2011).

    Article  CAS  Google Scholar 

  7. Knudsen, E.I. Control form below: the contribution of a midbrain network to spatial attention. Eur. J. Neurosci. 33, 1961–1972 (2011).

    Article  Google Scholar 

  8. Zanto, T.P. & Gazzaley, A. Neural suppression of irrelevant information underlies optimal working memory performance. J. Neurosci. 29, 3059–3066 (2009).

    Article  CAS  Google Scholar 

  9. Lovejoy, L.P. & Krauzlis, R.J. Inactivation of primate superior colliculus impairs covert selection of signals for perceptual judgments. Nat. Neurosci. 13, 261–266 (2010).

    Article  CAS  Google Scholar 

  10. McPeek, R.M. & Keller, E.L. Deficits in saccade target selection after inactivation of superior colliculus. Nat. Neurosci. 7, 757–763 (2004).

    Article  CAS  Google Scholar 

  11. Mysore, S.P., Asadollahi, A. & Knudsen, E.I. Global inhibition and stimulus competition in the owl optic tectum. J. Neurosci. 30, 1727–1738 (2010).

    Article  CAS  Google Scholar 

  12. Winkowski, D.E. & Knudsen, E.I. Top-down gain control of the auditory space map by gaze control circuitry in the barn owl. Nature 439, 336–339 (2006).

    Article  CAS  Google Scholar 

  13. Mysore, S.P., Asadollahi, A. & Knudsen, E.I. Signaling of the strongest stimulus in the owl optic tectum. J. Neurosci. 31, 5186–5196 (2011).

    Article  CAS  Google Scholar 

  14. Basso, M.A. & Wurtz, R.H. Modulation of neuronal activity by target uncertainty. Nature 389, 66–69 (1997).

    Article  CAS  Google Scholar 

  15. Mysore, S.P. & Knudsen, E.I. Flexible categorization of relative stimulus strength by the optic tectum. J. Neurosci. 31, 7745–7752 (2011).

    Article  CAS  Google Scholar 

  16. Mysore, S.P. & Knudsen, E.I. The role of a midbrain network in competitive stimulus selection. Curr. Opin. Neurobiol. 21, 653–660 (2011).

    Article  CAS  Google Scholar 

  17. Carrasco, M. Covert attention increases contrast sensitivity: psychophysical, neurophysiological and neuroimaging studies. Prog. Brain Res. 154, 33–70 (2006).

    Article  Google Scholar 

  18. Wang, Y., Major, D.E. & Karten, H.J. Morphology and connections of nucleus isthmi pars magnocellularis in chicks (Gallus gallus). J. Comp. Neurol. 469, 275–297 (2004).

    Article  Google Scholar 

  19. Marín, G. et al. A cholinergic gating mechanism controlled by competitive interactions in the optic tectum of the pigeon. J. Neurosci. 27, 8112–8121 (2007).

    Article  Google Scholar 

  20. Knudsen, E.I., Cohen, Y.E. & Masino, T. Characterization of a forebrain gaze field in the archistriatum of the barn owl: microstimulation and anatomical connections. J. Neurosci. 15, 5139–5151 (1995).

    Article  CAS  Google Scholar 

  21. Stanton, G.B., Goldberg, M.E. & Bruce, C.J. Frontal eye field efferents in the macaque monkey. II. Topography of terminal fields in midbrain and pons. J. Comp. Neurol. 271, 493–506 (1988).

    Article  CAS  Google Scholar 

  22. Knudsen, E.I. & Knudsen, P.F. Disruption of auditory spatial working memory by inactivation of the forebrain archistriatum in barn owls. Nature 383, 428–431 (1996).

    Article  CAS  Google Scholar 

  23. Dias, E.C. & Segraves, M.A. Muscimol-induced inactivation of monkey frontal eye field: effects on visually and memory-guided saccades. J. Neurophysiol. 81, 2191–2214 (1999).

    Article  CAS  Google Scholar 

  24. Bruce, C.J., Goldberg, M.E., Bushnell, M.C. & Stanton, G.B. Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. J. Neurophysiol. 54, 714–734 (1985).

    Article  CAS  Google Scholar 

  25. Moore, T. & Armstrong, K.M. Selective gating of visual signals by microstimulation of frontal cortex. Nature 421, 370–373 (2003).

    Article  CAS  Google Scholar 

  26. Moore, T. & Fallah, M. Control of eye movements and spatial attention. Proc. Natl. Acad. Sci. USA 98, 1273–1276 (2001).

    Article  CAS  Google Scholar 

  27. Sundberg, K.A., Mitchell, J.F. & Reynolds, J.H. Spatial attention modulates center-surround interactions in macaque visual area v4. Neuron 61, 952–963 (2009).

    Article  CAS  Google Scholar 

  28. Kastner, S., Pinsk, M.A., De Weerd, P., Desimone, R. & Ungerleider, L.G. Increased activity in human visual cortex during directed attention in the absence of visual stimulation. Neuron 22, 751–761 (1999).

    Article  CAS  Google Scholar 

  29. Falkner, A.L., Krishna, B.S. & Goldberg, M.E. Surround suppression sharpens the priority map in the lateral intraparietal area. J. Neurosci. 30, 12787–12797 (2010).

    Article  CAS  Google Scholar 

  30. Bair, W., Cavanaugh, J.R. & Movshon, J.A. Time course and time-distance relationships for surround suppression in macaque V1 neurons. J. Neurosci. 23, 7690–7701 (2003).

    Article  CAS  Google Scholar 

  31. Schall, J.D., Hanes, D.P., Thompson, K.G. & King, D.J. Saccade target selection in frontal eye field of macaque. I. Visual and premovement activation. J. Neurosci. 15, 6905–6918 (1995).

    Article  CAS  Google Scholar 

  32. Desimone, R., Moran, J., Schein, S.J. & Mishkin, M. A role for the corpus callosum in visual area V4 of the macaque. Vis. Neurosci. 10, 159–171 (1993).

    Article  CAS  Google Scholar 

  33. Desimone, R. & Duncan, J. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18, 193–222 (1995).

    Article  CAS  Google Scholar 

  34. Knudsen, E.I. Fundamental components of attention. Annu. Rev. Neurosci. 30, 57–78 (2007).

    Article  CAS  Google Scholar 

  35. Nummela, S.U. & Krauzlis, R.J. Inactivation of primate superior colliculus biases target choice for smooth pursuit, saccades and button press responses. J. Neurophysiol. 104, 1538–1548 (2010).

    Article  Google Scholar 

  36. Zénon, A. & Krauzlis, R.J. Attention deficits without cortical neuronal deficits. Nature 489, 434–437 (2012).

    Article  Google Scholar 

  37. Marín, G., Mpodozis, J., Sentis, E., Ossandon, T. & Letelier, J.C. Oscillatory bursts in the optic tectum of birds represent re-entrant signals from the nucleus isthmi pars parvocellularis. J. Neurosci. 25, 7081–7089 (2005).

    Article  Google Scholar 

  38. Lee, D.K., Itti, L., Koch, C. & Braun, J. Attention activates winner-take-all competition among visual filters. Nat. Neurosci. 2, 375–381 (1999).

    Article  CAS  Google Scholar 

  39. Reynolds, J.H. & Heeger, D.J. The normalization model of attention. Neuron 61, 168–185 (2009).

    Article  CAS  Google Scholar 

  40. Lee, J. & Maunsell, J.H. A normalization model of attentional modulation of single unit responses. PLoS ONE 4, e4651 (2009).

    Article  Google Scholar 

  41. Cavanaugh, J.R., Bair, W. & Movshon, J.A. Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. J. Neurophysiol. 88, 2530–2546 (2002).

    Article  Google Scholar 

  42. Kastner, S. & Ungerleider, L.G. Mechanisms of visual attention in the human cortex. Annu. Rev. Neurosci. 23, 315–341 (2000).

    Article  CAS  Google Scholar 

  43. Carrasco, M. Visual attention: the past 25 years. Vision Res. 51, 1484–1525 (2011).

    Article  Google Scholar 

  44. Gazzaley, A., Cooney, J.W., McEvoy, K., Knight, R.T. & D′Esposito, M. Top-down enhancement and suppression of the magnitude and speed of neural activity. J. Cogn. Neurosci. 17, 507–517 (2005).

    Article  Google Scholar 

  45. Winkowski, D.E. & Knudsen, E.I. Distinct mechanisms for top-down control of neural gain and sensitivity in the owl optic tectum. Neuron 60, 698–708 (2008).

    Article  CAS  Google Scholar 

  46. Mysore, S.P. & Knudsen, E.I. Reciprocal inhibition of inhibition: a circuit motif for flexible categorization in stimulus selection. Neuron 73, 193–205 (2012).

    Article  CAS  Google Scholar 

  47. Witten, I.B., Knudsen, P.F. & Knudsen, E.I. A dominance hierarchy of auditory spatial cues in barn owls. PLoS ONE 5, e10396 (2010).

    Article  Google Scholar 

  48. Winkowski, D.E. & Knudsen, E.I. Top-down control of multimodal sensitivity in the barn owl optic tectum. J. Neurosci. 27, 13279–13291 (2007).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank P. Knudsen for the immunohistochemistry. We are grateful to A. Asadollahi, A. Bryant, A. Goddard, J. Schwarz and N. Steinmetz for critically reading the manuscript. This work was supported by funding from the US National Institutes of Health (9R01 EY019179, E.I.K.).

Author information

Authors and Affiliations

  1. Department of Neurobiology, Stanford University, Stanford, California, USA

    Shreesh P Mysore & Eric I Knudsen

Authors
  1. Shreesh P Mysore
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eric I Knudsen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S.P.M. and E.I.K. designed the study and wrote the paper. S.P.M. performed the experiments and the analyses.

Corresponding author

Correspondence to Shreesh P Mysore.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–4 (PDF 2185 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mysore, S., Knudsen, E. A shared inhibitory circuit for both exogenous and endogenous control of stimulus selection. Nat Neurosci 16, 473–478 (2013). https://doi.org/10.1038/nn.3352

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.3352

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