A Distinct Class of Bursting Neurons with Strong Gamma Synchronization and Stimulus Selectivity in Monkey V1

• Published in: Neuron (Cambridge, Mass.) Mass.), 2020-01, Vol.105 (1), p.180-197.e5
• Main Authors: Onorato, Irene, Neuenschwander, Sergio, Hoy, Jennifer, Lima, Bruss, Rocha, Katia-Simone, Broggini, Ana Clara, Uran, Cem, Spyropoulos, Georgios, Klon-Lipok, Johanna, Womelsdorf, Thilo, Fries, Pascal, Niell, Cristopher, Singer, Wolf, Vinck, Martin
• Format: Article
• Language: English
• Subjects: Action Potentials - physiology; Animals; bursting; Cebinae; cell class; cell type; Conditioning, Operant - physiology; Cortical Synchronization - physiology; excitatory; Female; Frequency dependence; gamma; Gamma Rhythm - physiology; Information processing; interneuron; Interneurons; Macaca mulatta; Male; Mice; Monkeys & apes; Neural Inhibition - physiology; Neurons; Neurons - physiology; Orientation behavior; orientation tuning; oscillation; Oscillations; Pacemakers; Photic Stimulation; Rhythms; Sensory integration; Somatosensory cortex; Synchronization; Visual cortex; Visual Cortex - physiology
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2019.09.039

Cortical computation depends on interactions between excitatory and inhibitory neurons. The contributions of distinct neuron types to sensory processing and network synchronization in primate visual cortex remain largely undetermined. We show that in awake monkey V1, there exists a distinct cell type (››30% of neurons) that has narrow-waveform (NW) action potentials and high spontaneous discharge rates and fires in high-frequency bursts. These neurons are more stimulus selective and phase locked to 30- to 80-Hz gamma oscillations than other neuron types. Unlike other neuron types, their gamma-phase locking is highly predictive of orientation tuning. We find evidence for strong rhythmic inhibition in these neurons, suggesting that they interact with interneurons to act as excitatory pacemakers for the V1 gamma rhythm. We did not find a similar class of NW bursting neurons in L2-L4 of mouse V1. Given its properties, this class of NW bursting neurons should be pivotal for the encoding and transmission of stimulus information. •A distinct neuron type with thin spikes and high burst propensity in monkey V1•These neurons are present in both Old World and New World monkeys, but not in mice•They show relatively strong gamma (30–80 Hz) rhythmicity and stimulus selectivity•Firing suppression contributes to their orientation tuning and gamma rhythmicity Onorato et al. find a specialized V1 neuron type that has narrow-spike waveforms, fires in high-frequency bursts, is strongly phase locked to 30- to 80-Hz oscillations, and is highly stimulus-selective. This neuron class is found in both Old World and New World monkeys, but not in mice.