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Electrical Stimulation of Lateral Habenula during Learning: Frequency-Dependent Effects on Acquisition but Not Retrieval of a Two-Way Active Avoidance Response

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  • Anton Ilango
  • Jason Shumake
  • Wolfram Wetzel
  • Henning Scheich
  • Frank W Ohl

Abstract

The lateral habenula (LHb) is an epithalamic structure involved in signaling reward omission and aversive stimuli, and it inhibits dopaminergic neurons during motivated behavior. Less is known about LHb involvement in the acquisition and retrieval of avoidance learning. Our previous studies indicated that brief electrical stimulation of the LHb, time-locked to the avoidance of aversive footshock (presumably during the positive affective “relief” state that occurs when an aversive outcome is averted), inhibited the acquisition of avoidance learning. In the present study, we used the same paradigm to investigate different frequencies of LHb stimulation. The effect of 20 Hz vs. 50 Hz vs. 100 Hz stimulation was investigated during two phases, either during acquisition or retrieval in Mongolian gerbils. The results indicated that 50 Hz, but not 20 Hz, was sufficient to produce a long-term impairment in avoidance learning, and was somewhat more effective than 100 Hz in this regard. None of the stimulation parameters led to any effects on retrieval of avoidance learning, nor did they affect general motor activity. This suggests that, at frequencies in excess of the observed tonic firing rates of LHb neurons (>1–20 Hz), LHb stimulation may serve to interrupt the consolidation of new avoidance memories. However, these stimulation parameters are not capable of modifying avoidance memories that have already undergone extensive consolidation.

Suggested Citation

  • Anton Ilango & Jason Shumake & Wolfram Wetzel & Henning Scheich & Frank W Ohl, 2013. "Electrical Stimulation of Lateral Habenula during Learning: Frequency-Dependent Effects on Acquisition but Not Retrieval of a Two-Way Active Avoidance Response," PLOS ONE, Public Library of Science, vol. 8(6), pages 1-8, June.
  • Handle: RePEc:plo:pone00:0065684
    DOI: 10.1371/journal.pone.0065684
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    References listed on IDEAS

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    1. F. W. Ohl & H. Scheich & W. J. Freeman, 2001. "Change in pattern of ongoing cortical activity with auditory category learning," Nature, Nature, vol. 412(6848), pages 733-736, August.
    2. Masayuki Matsumoto & Okihide Hikosaka, 2007. "Lateral habenula as a source of negative reward signals in dopamine neurons," Nature, Nature, vol. 447(7148), pages 1111-1115, June.
    3. Bo Li & Joaquin Piriz & Martine Mirrione & ChiHye Chung & Christophe D. Proulx & Daniela Schulz & Fritz Henn & Roberto Malinow, 2011. "Synaptic potentiation onto habenula neurons in the learned helplessness model of depression," Nature, Nature, vol. 470(7335), pages 535-539, February.
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