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Preconfigured cortico-thalamic neural dynamics constrain movement-associated thalamic activity

Author

Listed:
  • Perla González-Pereyra

    (UNAM Campus Juriquilla)

  • Oswaldo Sánchez-Lobato

    (UNAM Campus Juriquilla)

  • Mario G. Martínez-Montalvo

    (UNAM Campus Juriquilla)

  • Diana I. Ortega-Romero

    (UNAM Campus Juriquilla)

  • Claudia I. Pérez-Díaz

    (UNAM Campus Juriquilla)

  • Hugo Merchant

    (UNAM Campus Juriquilla)

  • Luis A. Tellez

    (UNAM Campus Juriquilla)

  • Pavel E. Rueda-Orozco

    (UNAM Campus Juriquilla)

Abstract

Neural preconfigured activity patterns (nPAPs), conceptualized as organized activity parcellated into groups of neurons, have been proposed as building blocks for cognitive and sensory processing. However, their existence and function in motor networks have been scarcely studied. Here, we explore the possibility that nPAPs are present in the motor thalamus (VL/VM) and their potential contribution to motor-related activity. To this end, we developed a preparation where VL/VM multiunitary activity could be robustly recorded in mouse behavior evoked by primary motor cortex (M1) optogenetic stimulation and forelimb movements. VL/VM-evoked activity was organized as rigid stereotypical activity patterns at the single and population levels. These activity patterns were unable to dynamically adapt to different temporal architectures of M1 stimulation. Moreover, they were experience-independent, present in virtually all animals, and pairs of neurons with high correlations during M1-stimulation also presented higher correlations during spontaneous activity, confirming their preconfigured nature. Finally, subpopulations expressing specific M1-evoked patterns also displayed specific movement-related patterns. Our data demonstrate that the behaviorally related identity of specific neural subpopulations is tightly linked to nPAPs.

Suggested Citation

  • Perla González-Pereyra & Oswaldo Sánchez-Lobato & Mario G. Martínez-Montalvo & Diana I. Ortega-Romero & Claudia I. Pérez-Díaz & Hugo Merchant & Luis A. Tellez & Pavel E. Rueda-Orozco, 2024. "Preconfigured cortico-thalamic neural dynamics constrain movement-associated thalamic activity," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54742-9
    DOI: 10.1038/s41467-024-54742-9
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    1. Yinqing Li & Violeta G. Lopez-Huerta & Xian Adiconis & Kirsten Levandowski & Soonwook Choi & Sean K. Simmons & Mario A. Arias-Garcia & Baolin Guo & Annie Y. Yao & Timothy R. Blosser & Ralf D. Wimmer &, 2020. "Distinct subnetworks of the thalamic reticular nucleus," Nature, Nature, vol. 583(7818), pages 819-824, July.
    2. Michael N. Economo & Sarada Viswanathan & Bosiljka Tasic & Erhan Bas & Johan Winnubst & Vilas Menon & Lucas T. Graybuck & Thuc Nghi Nguyen & Kimberly A. Smith & Zizhen Yao & Lihua Wang & Charles R. Ge, 2018. "Distinct descending motor cortex pathways and their roles in movement," Nature, Nature, vol. 563(7729), pages 79-84, November.
    3. Jorge Gámez & Germán Mendoza & Luis Prado & Abraham Betancourt & Hugo Merchant, 2019. "The amplitude in periodic neural state trajectories underlies the tempo of rhythmic tapping," PLOS Biology, Public Library of Science, vol. 17(4), pages 1-32, April.
    4. Zengcai V. Guo & Hidehiko K. Inagaki & Kayvon Daie & Shaul Druckmann & Charles R. Gerfen & Karel Svoboda, 2017. "Maintenance of persistent activity in a frontal thalamocortical loop," Nature, Nature, vol. 545(7653), pages 181-186, May.
    5. Ana E. Hidalgo-Balbuena & Annie Y. Luma & Ana K. Pimentel-Farfan & Teresa Peña-Rangel & Pavel E. Rueda-Orozco, 2019. "Sensory representations in the striatum provide a temporal reference for learning and executing motor habits," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    6. Xin Jin & Rui M. Costa, 2010. "Start/stop signals emerge in nigrostriatal circuits during sequence learning," Nature, Nature, vol. 466(7305), pages 457-462, July.
    7. Tomáš Hromádka & Michael R DeWeese & Anthony M Zador, 2008. "Sparse Representation of Sounds in the Unanesthetized Auditory Cortex," PLOS Biology, Public Library of Science, vol. 6(1), pages 1-14, January.
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