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Research Articles, Behavioral/Cognitive

Selective Interruption of Auditory Interhemispheric Cross Talk Impairs Discrimination Learning of Frequency-Modulated Tone Direction But Not Gap Detection and Discrimination

Katja Saldeitis, Marcus Jeschke, Annika Michalek, Julia U. Henschke, Wolfram Wetzel, Frank W. Ohl and Eike Budinger
Journal of Neuroscience 9 March 2022, 42 (10) 2025-2038; DOI: https://doi.org/10.1523/JNEUROSCI.0216-21.2022
Katja Saldeitis
1Department Systems Physiology of Learning, Leibniz Institute for Neurobiology, Magdeburg D-39118, Germany
2Institute for Auditory Neuroscience, University Medical Center Goettingen, Göttingen D-37075, Germany
3Cognitive Hearing in Primates Group, Auditory Neuroscience and Optogenetics Laboratory, German Primate Center, Göttingen D-37077, Germany
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Marcus Jeschke
1Department Systems Physiology of Learning, Leibniz Institute for Neurobiology, Magdeburg D-39118, Germany
2Institute for Auditory Neuroscience, University Medical Center Goettingen, Göttingen D-37075, Germany
3Cognitive Hearing in Primates Group, Auditory Neuroscience and Optogenetics Laboratory, German Primate Center, Göttingen D-37077, Germany
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Annika Michalek
4Combinatorial NeuroImaging Core Facility, Leibniz Institute for Neurobiology, Magdeburg D-39118, Germany
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Julia U. Henschke
5Institute of Cognitive Neurology and Dementia Research, Otto von Guericke University, Magdeburg D-39120, Germany
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Wolfram Wetzel
1Department Systems Physiology of Learning, Leibniz Institute for Neurobiology, Magdeburg D-39118, Germany
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Frank W. Ohl
1Department Systems Physiology of Learning, Leibniz Institute for Neurobiology, Magdeburg D-39118, Germany
6Institute of Biology, Otto-von-Guericke University Magdeburg, Magdeburg D-39120, Germany
7Center for Behavioral Brain Sciences, Magdeburg D-39120, Germany
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Eike Budinger
4Combinatorial NeuroImaging Core Facility, Leibniz Institute for Neurobiology, Magdeburg D-39118, Germany
7Center for Behavioral Brain Sciences, Magdeburg D-39120, Germany
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Abstract

Functional hemispheric lateralization is a basic principle of brain organization. In the auditory domain, the right auditory cortex (AC) determines the pitch direction of continuous auditory stimuli whereas the left AC discriminates gaps in these stimuli. The involved functional interactions between the two sides, mediated by commissural connections, are poorly understood. Here, we selectively disrupted the interhemispheric cross talk from the left to the right primary AC and vice versa using chromophore-targeted laser-induced apoptosis of the respective projection neurons, which make up 6–17% of all AC neurons in Layers III, V, and VI. Following photolysis, male gerbils were trained in a first experimental set to discriminate between rising and falling frequency-modulated (FM) tone sweeps. The acquisition of the task was significantly delayed in lesioned animals of either lesion direction. However, the final discrimination performance and hit rate was lowest for animals with left-side lesioned commissural neurons, demonstrating that also information from the left AC is relevant for FM direction learning. Photolysis after successful learning did not affect the retrieval of the learned task, indicating that the disruption during learning was not because of a general functional impairment. In a second experimental set, the gerbil's ability to detect and discriminate small silent gaps of varying length within FM sweeps was tested. This ability was also preserved after interhemispheric disruption. Taken together, interhemispheric communication between the left and right AC is important for the acquisition of FM tone direction learning but not for its retrieval and for gap detection and gap duration discrimination.

SIGNIFICANCE STATEMENT Hemispheric lateralization of neuronal functions such as speech and music processing in humans are common throughout the brain; however, the involved interhemispheric interactions are ill-defined. Here, we show that the selective photolytic disruption of auditory cortical commissural connections in rodents impairs the acquisition but not retrieval of a frequency-modulated tone direction discrimination task. The final discrimination performance and hit rate was lowest for animals with lesioned left-to-right-side projections; thus, although right auditory cortex is dominant, left auditory cortex is also relevant for learning this task. The detection and discrimination of small gaps within the tone sweeps remain intact, suggesting a pathway for the processing of these temporal structures, which could be independent from the lesioned interhemispheric cross talk.

  • auditory cortex
  • chromophore-targeted photolysis
  • corpus callosum
  • hemispheric specialization
  • Mongolian gerbil
  • rodent

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The Journal of Neuroscience: 42 (10)
Journal of Neuroscience
Vol. 42, Issue 10
9 Mar 2022
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Selective Interruption of Auditory Interhemispheric Cross Talk Impairs Discrimination Learning of Frequency-Modulated Tone Direction But Not Gap Detection and Discrimination
Katja Saldeitis, Marcus Jeschke, Annika Michalek, Julia U. Henschke, Wolfram Wetzel, Frank W. Ohl, Eike Budinger
Journal of Neuroscience 9 March 2022, 42 (10) 2025-2038; DOI: 10.1523/JNEUROSCI.0216-21.2022

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Selective Interruption of Auditory Interhemispheric Cross Talk Impairs Discrimination Learning of Frequency-Modulated Tone Direction But Not Gap Detection and Discrimination
Katja Saldeitis, Marcus Jeschke, Annika Michalek, Julia U. Henschke, Wolfram Wetzel, Frank W. Ohl, Eike Budinger
Journal of Neuroscience 9 March 2022, 42 (10) 2025-2038; DOI: 10.1523/JNEUROSCI.0216-21.2022
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Keywords

  • auditory cortex
  • chromophore-targeted photolysis
  • corpus callosum
  • hemispheric specialization
  • Mongolian gerbil
  • rodent

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