The tuning of tuning: How adaptation influences single cell information transfer

PLoS Comput Biol. 2024 May 13;20(5):e1012043. doi: 10.1371/journal.pcbi.1012043. eCollection 2024 May.

Abstract

Sensory neurons reconstruct the world from action potentials (spikes) impinging on them. To effectively transfer information about the stimulus to the next processing level, a neuron needs to be able to adapt its working range to the properties of the stimulus. Here, we focus on the intrinsic neural properties that influence information transfer in cortical neurons and how tightly their properties need to be tuned to the stimulus statistics for them to be effective. We start by measuring the intrinsic information encoding properties of putative excitatory and inhibitory neurons in L2/3 of the mouse barrel cortex. Excitatory neurons show high thresholds and strong adaptation, making them fire sparsely and resulting in a strong compression of information, whereas inhibitory neurons that favour fast spiking transfer more information. Next, we turn to computational modelling and ask how two properties influence information transfer: 1) spike-frequency adaptation and 2) the shape of the IV-curve. We find that a subthreshold (but not threshold) adaptation, the 'h-current', and a properly tuned leak conductance can increase the information transfer of a neuron, whereas threshold adaptation can increase its working range. Finally, we verify the effect of the IV-curve slope in our experimental recordings and show that excitatory neurons form a more heterogeneous population than inhibitory neurons. These relationships between intrinsic neural features and neural coding that had not been quantified before will aid computational, theoretical and systems neuroscientists in understanding how neuronal populations can alter their coding properties, such as through the impact of neuromodulators. Why the variability of intrinsic properties of excitatory neurons is larger than that of inhibitory ones is an exciting question, for which future research is needed.

MeSH terms

  • Action Potentials* / physiology
  • Adaptation, Physiological* / physiology
  • Animals
  • Computational Biology
  • Computer Simulation
  • Mice
  • Models, Neurological*
  • Neurons / physiology
  • Sensory Receptor Cells / physiology
  • Somatosensory Cortex / physiology

Grants and funding

This work was supported by grants from the European Commission (Horizon2020, nr. 918 660328), European Regional Development Fund (MIND, nr. 122035) and the Netherlands Organisation for Scientific Research (NWO-ALW Open Competition, nr. 920 824.14.022) to TC and by the Netherlands Organisation for Scientific Research (NWO 921 Veni Research Grant, nr. 863.150.25) to FZ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.