Play and tickling responses map to the lateral columns of the rat periaqueductal gray

Natalie Gloveli; Jean Simonnet; Wei Tang; Miguel Concha-Miranda; Eduard Maier; Anton Dvorzhak; Dietmar Schmitz; Michael Brecht

doi:10.1016/j.neuron.2023.06.018

Play and tickling responses map to the lateral columns of the rat periaqueductal gray

Neuron. 2023 Oct 4;111(19):3041-3052.e7. doi: 10.1016/j.neuron.2023.06.018. Epub 2023 Jul 28.

Authors

Natalie Gloveli¹, Jean Simonnet², Wei Tang², Miguel Concha-Miranda², Eduard Maier³, Anton Dvorzhak⁴, Dietmar Schmitz⁵, Michael Brecht⁶

Affiliations

¹ Bernstein Center for Computational Neuroscience Berlin, Humboldt-Universität zu Berlin, Philippstr. 13, Haus 6, 10115 Berlin, Germany; Charité-Universitätsmedizin Berlin, Einstein Center for Neurosciences, Berlin, 10117 Berlin, Germany.
² Bernstein Center for Computational Neuroscience Berlin, Humboldt-Universität zu Berlin, Philippstr. 13, Haus 6, 10115 Berlin, Germany.
³ Bernstein Center for Computational Neuroscience Berlin, Humboldt-Universität zu Berlin, Philippstr. 13, Haus 6, 10115 Berlin, Germany; Department of Neuropeptide Research in Psychiatry, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, Germany.
⁴ Charité-Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin Institute of Health, Neuroscience Research Center, 10117 Berlin, Germany.
⁵ Bernstein Center for Computational Neuroscience Berlin, Humboldt-Universität zu Berlin, Philippstr. 13, Haus 6, 10115 Berlin, Germany; NeuroCure Cluster of Excellence, Humboldt-Universität zu Berlin, Berlin, Germany; Charité-Universitätsmedizin Berlin, Einstein Center for Neurosciences, Berlin, 10117 Berlin, Germany; Charité-Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin Institute of Health, Neuroscience Research Center, 10117 Berlin, Germany; German Center for Neurodegenerative Diseases (DZNE), 10117 Berlin, Germany.
⁶ Bernstein Center for Computational Neuroscience Berlin, Humboldt-Universität zu Berlin, Philippstr. 13, Haus 6, 10115 Berlin, Germany; NeuroCure Cluster of Excellence, Humboldt-Universität zu Berlin, Berlin, Germany; Charité-Universitätsmedizin Berlin, Einstein Center for Neurosciences, Berlin, 10117 Berlin, Germany. Electronic address: michael.brecht@bccn-berlin.de.

Abstract

The persistence of play after decortication points to a subcortical mechanism of play control. We found that global blockade of the rat periaqueductal gray with either muscimol or lidocaine interfered with ticklishness and play. We recorded vocalizations and neural activity from the periaqueductal gray of young, playful rats during interspecific touch, play, and tickling. Rats vocalized weakly to touch and more strongly to play and tickling. Periaqueductal gray units showed diverse but strong modulation to tickling and play. Hierarchical clustering based on neuronal responses to play and tickling revealed functional clusters mapping to different periaqueductal gray columns. Specifically, we observed play-neutral/tickling-inhibited and tickling/play-neutral units in dorsolateral and dorsomedial periaqueductal gray columns. In contrast, strongly play/tickling-excited units mapped to the lateral columns and were suppressed by anxiogenic conditions. Optogenetic inactivation of lateral periaqueductal columns disrupted ticklishness and play. We conclude that the lateral periaqueductal gray columns are decisive for play and laughter.

Keywords: Neuropixels; affective neuroscience; instinctive behaviors; laughter; midbrain; optogenetics; periaqueductal gray; play; tickling; vocalizations.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Neurons / physiology
Periaqueductal Gray* / physiology
Rats
Touch / physiology
Touch Perception*