Local changes in potassium ions regulate input integration in active dendrites

PLoS Biol. 2024 Dec 4;22(12):e3002935. doi: 10.1371/journal.pbio.3002935. eCollection 2024 Dec.

Abstract

During neuronal activity, the extracellular concentration of potassium ions ([K+]o) increases substantially above resting levels, yet it remains unclear what role these [K+]o changes play in the dendritic integration of synaptic inputs. We here used mathematical formulations and biophysical modeling to explore the role of synaptic activity-dependent K+ changes in dendritic segments of a visual cortex pyramidal neuron, receiving inputs tuned to stimulus orientation. We found that the spatial arrangement of inputs dictates the magnitude of [K+]o changes in the dendrites: Dendritic segments receiving similarly tuned inputs can attain substantially higher [K+]o increases than segments receiving diversely tuned inputs. These [K+]o elevations in turn increase dendritic excitability, leading to more robust and prolonged dendritic spikes. Ultimately, these local effects amplify the gain of neuronal input-output transformations, causing higher orientation-tuned somatic firing rates without compromising orientation selectivity. Our results suggest that local, activity-dependent [K+]o changes in dendrites may act as a "volume knob" that determines the impact of synaptic inputs on feature-tuned neuronal firing.

MeSH terms

  • Action Potentials* / physiology
  • Animals
  • Dendrites* / metabolism
  • Dendrites* / physiology
  • Models, Neurological*
  • Potassium* / metabolism
  • Pyramidal Cells* / metabolism
  • Pyramidal Cells* / physiology
  • Synapses / metabolism
  • Synapses / physiology
  • Visual Cortex* / metabolism
  • Visual Cortex* / physiology

Substances

  • Potassium

Grants and funding

R.N.R. acknowledges support from the Lundbeck Foundation (R370-2021-764). M.S.H acknowledges support from the Lundbeck Foundation and (R347-2020-2250) and the Novo Nordisk Foundation (NNF23OC0085907). M.H.J. acknowledges support from the Independent Research Fund Denmark (9040-00116B) and the Novo Nordisk Foundation (NNF20OC0064978 and NNF24OC0089788). M.S N. acknowledges support from Novo Nordisk Foundation (NNF20OC0064978). A.P. acknowledges support from the Theodore Papazoglou FORTH Synergy Grants. N.T. acknowledges support from French National Centre for Scientific Research (CNRS), the framework of the University of Bordeaux’s IdEx “Investments for the Future” programs (2020 IdEx Junior Chair; GPR BRAIN_2030), Conseil régional Nouvelle-Aquitaine (Bordeaux Neurocampus Junior Chair), the ATIP-Avenir program, Fondation Schlumberger pour l’Education et la Recherche (FSER202401018842), Brain Science Foundation, and Research Foundation for Opto-Science and Technology. None of the sponsors or funders played any role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.