Voltage-Gated Intrinsic Conductances Shape the Input-Output Relationship of Cortical Neurons in Behaving Primate V1

• Published in: Neuron (Cambridge, Mass.) Vol. 107; no. 1; pp. 185 - 196.e4
• Main Authors: Li, Baowang, Routh, Brandy N., Johnston, Daniel, Seidemann, Eyal, Priebe, Nicholas J.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 08.07.2020; Elsevier Limited
• Subjects: Action Potentials - physiology; Animals; Behavior, Animal - physiology; Brain slice preparation; Depolarization; intracellular recording; intrinsic conductance; Macaca mulatta; Mice; Mice, Inbred C57BL; Models, Neurological; Monkeys & apes; Neurons; Neurons - physiology; primary visual cortex; response selectivity; Visual Cortex - physiology; Visual stimuli; Voltage; intracellular recording; response selectivity; primary visual cortex; intrinsic conductance
• ISSN: 0896-6273; 1097-4199; 1097-4199
• DOI: 10.1016/j.neuron.2020.04.001

Neurons are input-output (I/O) devices—they receive synaptic inputs from other neurons, integrate those inputs with their intrinsic properties, and generate action potentials as outputs. To understand this fundamental process, we studied the interaction between synaptic inputs and intrinsic properties using whole-cell recordings from V1 neurons of awake, fixating macaque monkeys. Our measurements during spontaneous activity and visual stimulation reveal an intrinsic voltage-gated conductance that profoundly alters the integrative properties and visual responses of cortical neurons. This voltage-gated conductance increases neuronal gain and selectivity with subthreshold depolarization and linearizes the relationship between synaptic input and neural output. This intrinsic conductance is found in layer 2/3 V1 neurons of awake macaques, anesthetized mice, and acute brain slices. These results demonstrate that intrinsic conductances play an essential role in shaping the I/O relationship of cortical neurons and must be taken into account in future models of cortical computations. •Neurons in behaving macaque V1 exhibit a large voltage-gated intrinsic conductance•This conductance leads to an increase in membrane resistance with depolarization•This mechanism increases neuronal gain and selectivity to subthreshold depolarization•This nonlinearity should be incorporated into future models of cortical computations Li et al. used whole-cell recording to reveal a large and unexpected voltage-gated intrinsic conductance that dramatically alters the integrative properties of primate V1 neurons. Therefore, a standard computational model of sensory neurons that incorporates linear integration of synaptic inputs followed by a threshold nonlinearity requires revision.