Evidence for a causal inverse model in an avian cortico-basal ganglia circuit

Edited by Thomas C. Südhof, Stanford University School of Medicine, Stanford, CA, and approved March 7, 2014 (received for review September 11, 2013)
April 7, 2014
111 (16) 6063-6068

Significance

Auditory neural responses mirror motor activity in a songbird cortical area. The average temporal offset of mirrored responses is roughly equal to short sensorimotor loop delays. This correspondence between mirroring offsets and loop delays constitutes evidence for a causal inverse model. Causal inverse models can map a desired sensation into the required action.

Abstract

Learning by imitation is fundamental to both communication and social behavior and requires the conversion of complex, nonlinear sensory codes for perception into similarly complex motor codes for generating action. To understand the neural substrates underlying this conversion, we study sensorimotor transformations in songbird cortical output neurons of a basal-ganglia pathway involved in song learning. Despite the complexity of sensory and motor codes, we find a simple, temporally specific, causal correspondence between them. Sensory neural responses to song playback mirror motor-related activity recorded during singing, with a temporal offset of roughly 40 ms, in agreement with short feedback loop delays estimated using electrical and auditory stimulation. Such matching of mirroring offsets and loop delays is consistent with a recent Hebbian theory of motor learning and suggests that cortico-basal ganglia pathways could support motor control via causal inverse models that can invert the rich correspondence between motor exploration and sensory feedback.

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Acknowledgments

We thank Klaus Hepp, Alexander Hanuschkin, and Walter Senn for helpful discussions and critical reading. This work was funded by Swiss National Science Foundation Grant 31003A_127024, the European Research Council (ERC) under the European Community's Seventh Framework Programme (FP7/2007-2013/ERC Grant AdG 268911), Burroughs Wellcome Foundation, Sloan Foundation, and Defense Advanced Research Planning Agency.

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Information & Authors

Information

Published in

The cover image for PNAS Vol.111; No.16
Proceedings of the National Academy of Sciences
Vol. 111 | No. 16
April 22, 2014
PubMed: 24711417

Classifications

Submission history

Published online: April 7, 2014
Published in issue: April 22, 2014

Keywords

  1. lateral magnocellular nucleus of the anterior nidopallium
  2. Hebbian learning
  3. mirror neuron

Acknowledgments

We thank Klaus Hepp, Alexander Hanuschkin, and Walter Senn for helpful discussions and critical reading. This work was funded by Swiss National Science Foundation Grant 31003A_127024, the European Research Council (ERC) under the European Community's Seventh Framework Programme (FP7/2007-2013/ERC Grant AdG 268911), Burroughs Wellcome Foundation, Sloan Foundation, and Defense Advanced Research Planning Agency.

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Nicolas Giret
Institute of Neuroinformatics and
Neuroscience Center Zurich, University of Zurich and ETH Zurich, 8057 Zurich, Switzerland; and
Joergen Kornfeld
Institute of Neuroinformatics and
Surya Ganguli
Department of Applied Physics, Stanford University, Stanford, CA 94305-5447
Richard H. R. Hahnloser1 [email protected]
Institute of Neuroinformatics and
Neuroscience Center Zurich, University of Zurich and ETH Zurich, 8057 Zurich, Switzerland; and

Notes

1
To whom correspondence should be addressed. E-mail: [email protected].
Author contributions: N.G., J.K., S.G., and R.H.R.H. designed research; N.G. and J.K. performed research; N.G., J.K., and R.H.R.H. analyzed data; and N.G., S.G., and R.H.R.H. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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    Evidence for a causal inverse model in an avian cortico-basal ganglia circuit
    Proceedings of the National Academy of Sciences
    • Vol. 111
    • No. 16
    • pp. 5755-6115

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