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Corticostriatal neurons in auditory cortex drive decisions during auditory discrimination

Nature volume 497, pages 482–485 (2013)Cite this article

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Abstract

The neural pathways by which information about the acoustic world reaches the auditory cortex are well characterized, but how auditory representations are transformed into motor commands is not known. Here we use a perceptual decision-making task in rats to study this transformation. We demonstrate the role of corticostriatal projection neurons in auditory decisions by manipulating the activity of these neurons in rats performing an auditory frequency-discrimination task. Targeted channelrhodopsin-2 (ChR2)1,2-mediated stimulation of corticostriatal neurons during the task biased decisions in the direction predicted by the frequency tuning of the stimulated neurons, whereas archaerhodopsin-3 (Arch)3-mediated inactivation biased decisions in the opposite direction. Striatal projections are widespread in cortex and may provide a general mechanism for the control of motor decisions by sensory cortex.

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Figure 1: Cloud-of-tones task.
Figure 2: ChR2 stimulation of corticostriatal neurons biases subjects’ choices.
Figure 3: Arch-mediated inactivation of corticostriatal neurons anti-biases subjects’ choices.
Figure 4: Estimation of numbers of neurons affected by Arch inactivation.

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References

  1. Nagel, G. et al. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl Acad. Sci. USA 100, 13940–13945 (2003)

    Article  ADS  CAS  Google Scholar 

  2. Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G. & Deisseroth, K. Millisecond-timescale, genetically targeted optical control of neural activity. Nature Neurosci. 8, 1263–1268 (2005)

    Article  CAS  Google Scholar 

  3. Chow, B. Y. et al. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463, 98–102 (2010)

    Article  ADS  CAS  Google Scholar 

  4. Ding, L. & Gold, J. I. Caudate encodes multiple computations for perceptual decisions. J. Neurosci. 30, 15747–15759 (2010)

    Article  CAS  Google Scholar 

  5. Kimchi, E. Y. & Laubach, M. Dynamic encoding of action selection by the medial striatum. J. Neurosci. 29, 3148–3159 (2009)

    Article  CAS  Google Scholar 

  6. Reynolds, J. N., Hyland, B. I. & Wickens, J. R. A cellular mechanism of reward-related learning. Nature 413, 67–70 (2001)

    Article  ADS  CAS  Google Scholar 

  7. Pasupathy, A. & Miller, E. K. Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature 433, 873–876 (2005)

    Article  ADS  CAS  Google Scholar 

  8. Beckstead, R. M., Domesick, V. B. & Nauta, W. J. Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res. 175, 191–217 (1979)

    Article  CAS  Google Scholar 

  9. Hopkins, D. A. & Niessen, L. W. Substantia nigra projections to the reticular formation, superior colliculus and central gray in the rat, cat and monkey. Neurosci. Lett. 2, 253–259 (1976)

    Article  CAS  Google Scholar 

  10. Felsen, G. & Mainen, Z. F. Neural substrates of sensory-guided locomotor decisions in the rat superior colliculus. Neuron 60, 137–148 (2008)

    Article  CAS  Google Scholar 

  11. Kreitzer, A. C. & Malenka, R. C. Striatal plasticity and basal ganglia circuit function. Neuron 60, 543–554 (2008)

    Article  CAS  Google Scholar 

  12. Allen Brain Institute. Allen Mouse Connectivity Atlas http:// connectivity.brain-map.org. (2012)

  13. McGeorge, A. J. & Faull, R. L. The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29, 503–537 (1989)

    Article  CAS  Google Scholar 

  14. Bordi, F. & LeDoux, J. Sensory tuning beyond the sensory system: an initial analysis of auditory response properties of neurons in the lateral amygdaloid nucleus and overlying areas of the striatum. J. Neurosci. 12, 2493–2503 (1992)

    Article  CAS  Google Scholar 

  15. Bordi, F., LeDoux, J., Clugnet, M. C. & Pavlides, C. Single-unit activity in the lateral nucleus of the amygdala and overlying areas of the striatum in freely behaving rats: rates, discharge patterns, and responses to acoustic stimuli. Behav. Neurosci. 107, 757–769 (1993)

    Article  Google Scholar 

  16. Salzman, C. D., Britten, K. H. & Newsome, W. T. Cortical microstimulation influences perceptual judgements of motion direction. Nature 346, 174–177 (1990)

    Article  ADS  CAS  Google Scholar 

  17. Sally, S. L. & Kelly, J. B. Organization of auditory cortex in the albino rat: sound frequency. J. Neurophysiol. 59, 1627–1638 (1988)

    Article  CAS  Google Scholar 

  18. Uchida, N. & Mainen, Z. F. Speed and accuracy of olfactory discrimination in the rat. Nature Neurosci. 6, 1224–1229 (2003)

    Article  CAS  Google Scholar 

  19. Lilley, C. E. et al. Multiple immediate-early gene-deficient herpes simplex virus vectors allowing efficient gene delivery to neurons in culture and widespread gene delivery to the central nervous system in vivo. J. Virol. 75, 4343–4356 (2001)

    Article  CAS  Google Scholar 

  20. Lima, S. Q., Hromádka, T., Znamenskiy, P. & Zador, A. M. PINP: a new method of tagging neuronal populations for identification during in vivo electrophysiological recording. PLoS ONE 4, e6099 (2009)

    Article  ADS  Google Scholar 

  21. Ciocchi, S. et al. Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 468, 277–282 (2010)

    Article  ADS  CAS  Google Scholar 

  22. Reiner, A., Jiao, Y., Del Mar, N., Laverghetta, A. V. & Lei, W. L. Differential morphology of pyramidal tract-type and intratelencephalically projecting-type corticostriatal neurons and their intrastriatal terminals in rats. J. Comp. Neurol. 457, 420–440 (2003)

    Article  Google Scholar 

  23. Reale, R. A. & Imig, T. J. Auditory cortical field projections to the basal ganglia of the cat. Neuroscience 8, 67–86 (1983)

    Article  CAS  Google Scholar 

  24. Huber, D. et al. Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice. Nature 451, 61–64 (2008)

    Article  ADS  CAS  Google Scholar 

  25. Houweling, A. R. & Brecht, M. Behavioural report of single neuron stimulation in somatosensory cortex. Nature 451, 65–68 (2008)

    Article  ADS  CAS  Google Scholar 

  26. Britten, K. H., Shadlen, M. N., Newsome, W. T. & Movshon, J. A. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J. Neurosci. 12, 4745–4765 (1992)

    Article  CAS  Google Scholar 

  27. Jiang, H., Stein, B. E. & McHaffie, J. G. Physiological evidence for a trans-basal ganglia pathway linking extrastriate visual cortex and the superior colliculus. J. Physiol. (Lond.) 589, 5785–5799 (2011)

    Article  CAS  Google Scholar 

  28. Kelly, J. B. & Masterton, B. Auditory sensitivity of the albino rat. J. Comp. Physiol. Psychol. 91, 930–936 (1977)

    Article  CAS  Google Scholar 

  29. Palmer, J., Huk, A. & Shadlen, M. The effect of stimulus strength on the speed and accuracy of a perceptual decision. J. Vis. 5, 376–404 (2005)

    Article  Google Scholar 

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Acknowledgements

We thank B. Burbach for technical assistance, A. Reid for generating the AAV-FLEX-Arch–GFP construct and members of the Kepecs laboratory (CSHL) for the tetrode and fibre drive design. We thank K. Britten for comments and suggestions on the manuscript. AAV-CAGGS-ChR2-Venus plasmid was provided by K. Svoboda. AAV-CAGGS-FLEX-ChR2-tdTomato virus was a gift from A. Kepecs. AAV-CAG-Arch–GFP plasmid was provided by E. Boyden. AAV-EF1a-FLEX-ChR2-YFP was provided by K. Deisseroth. HSV–iCre-2A-Venus and HSV–mCherry-IRES–iCre constructs were provided by A. Luthi and packaged by BioVex. This work was supported by grants from the Swartz Foundation and the National Institutes of Health (grant numbers 25041001 and 55120101).

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Authors and Affiliations

  1. Watson School of Biological Sciences, Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, New York 11724, USA,

    Petr Znamenskiy

  2. Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, 11724, New York, USA

    Petr Znamenskiy & Anthony M. Zador

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  1. Petr Znamenskiy
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Contributions

P.Z. and A.M.Z. designed the experiments, P.Z. carried out the experiments, and P.Z. and A.M.Z. analysed the data and wrote the manuscript.

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Correspondence to Anthony M. Zador.

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The authors declare no competing financial interests.

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Znamenskiy, P., Zador, A. Corticostriatal neurons in auditory cortex drive decisions during auditory discrimination. Nature 497, 482–485 (2013). https://doi.org/10.1038/nature12077

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