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Acceleration of visually cued conditioned fear through the auditory pathway

Nature Neuroscience volume 7, pages 968–973 (2004)Cite this article

Abstract

Defensive responses elicited by sensory experiences are critical for survival. Mice acquire a conditioned fear response rapidly to an auditory cue but slowly to a visual cue, a difference in learned behavior that is likely to be mediated by direct projections to the lateral amygdala from the auditory thalamus but mainly indirect ones from the visual thalamus. Here, we show that acquisition of visually cued conditioned fear is accelerated in 'rewired' mice that have retinal projections routed to the auditory thalamus. Visual stimuli induce expression of the immediate early gene Fos (also known as c-fos) in the auditory thalamus and the lateral amygdala in rewired mice, similar to the way auditory stimuli do in control mice. Thus, the rewired auditory pathway conveys visual information and mediates rapid activity-dependent plasticity in central structures that influence learned behavior.

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Figure 1: Simplified fear conditioning pathways in normal and rewired mice.
Figure 2: Cued testing behavior in normal and rewired mice.
Figure 3: Cued freezing across sessions.
Figure 4: c-fos expression after one session of fear conditioning (a–e).

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Acknowledgements

We thank A. Majewska and A. Lyckman for their assistance with the c-fos experiments. This work was supported by grants from the US National Institutes of Health (F32 EY13900 to J.R.N., R01 NS32925 and P50 MH58880 to S.T., and R01 EY14134 and R01 EY15068 to M.S.).

Author information

Authors and Affiliations

  1. The Picower Center for Learning & Memory, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA

    Jessica R Newton, Charlene Ellsworth, Tsuyoshi Miyakawa, Susumu Tonegawa & Mriganka Sur

  2. Department of Brain & Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA

    Jessica R Newton, Charlene Ellsworth, Susumu Tonegawa & Mriganka Sur

  3. RIKEN-MIT Neuroscience Research Center, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA

    Tsuyoshi Miyakawa & Susumu Tonegawa

  4. Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA

    Tsuyoshi Miyakawa & Susumu Tonegawa

  5. Department of Biology, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA

    Tsuyoshi Miyakawa & Susumu Tonegawa

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  1. Jessica R Newton
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Corresponding author

Correspondence to Mriganka Sur.

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Supplementary information

Supplementary Fig. 1

Lesion site. Coronal sections are shown at the same level of the inferior colliculus for (a) a sham lesion and (b) a rewired mouse. Dark label in dorsal part of A shows retinal projections to the far posterior superior colliculus following bilateral intraocular injection of cholera toxin subunit B. Scale bar, 1 mm. D, dorsal, M, medial, IC = inferior colliculus. (JPG 18 kb)

Supplementary Fig. 2

Retinothalamic projections. Coronal sections are shown at the same level of the thalamus for (a) a sham lesion, (b) a rewired and (c) a SC lesion mouse. Retinal projections were labeled by intraocular injection of cholera toxin subunit B. Scale bar, 0.1 mm. D, dorsal, M, medial, LP = lateral posterior nucleus, MGN = medial geniculate nucleus. (JPG 42 kb)

Supplementary Table 1

Summary of the number of mice in each group. (PDF 9 kb)

Supplementary Note (PDF 19 kb)

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Newton, J., Ellsworth, C., Miyakawa, T. et al. Acceleration of visually cued conditioned fear through the auditory pathway. Nat Neurosci 7, 968–973 (2004). https://doi.org/10.1038/nn1306

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