Trial-by-trial variability in cortical responses exhibits scaling of spatial correlations predicted from critical dynamics
Tiago L. Ribeiro,
Peter Jendrichovsky,
Shan Yu,
Daniel A. Martin,
Patrick O. Kanold,
Dante R. Chialvo,
Dietmar Plenz
Affiliations
Tiago L. Ribeiro
Section on Critical Brain Dynamics, National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20892, USA
Peter Jendrichovsky
Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD 21205, USA; Kavli Neuroscience Discovery Institute, Johns Hopkins University, Baltimore, MD 21205, USA
Shan Yu
Section on Critical Brain Dynamics, National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20892, USA; Brainnetome Center, Institute of Automation, Chinese Academy of Sciences, Beijing 100190, China; CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Beijing 100190, China
Daniel A. Martin
Center for Complex Systems & Brain Sciences (CEMSC3), Instituto de Ciencias Físicas, (ICIFI) Escuela de Ciencia y Tecnología, Universidad Nacional de San Martín (UNSAM), San Martín 1650 Buenos Aires, Argentina; Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Godoy Cruz 2290 Buenos Aires, Argentina
Patrick O. Kanold
Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD 21205, USA; Kavli Neuroscience Discovery Institute, Johns Hopkins University, Baltimore, MD 21205, USA
Dante R. Chialvo
Center for Complex Systems & Brain Sciences (CEMSC3), Instituto de Ciencias Físicas, (ICIFI) Escuela de Ciencia y Tecnología, Universidad Nacional de San Martín (UNSAM), San Martín 1650 Buenos Aires, Argentina; Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Godoy Cruz 2290 Buenos Aires, Argentina
Dietmar Plenz
Section on Critical Brain Dynamics, National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20892, USA; Corresponding author
Summary: In the mammalian cortex, even simple sensory inputs or movements activate many neurons, with each neuron responding variably to repeated stimuli—a phenomenon known as trial-by-trial variability. Understanding the spatial patterns and dynamics of this variability is challenging. Using cellular 2-photon imaging, we study visual and auditory responses in the primary cortices of awake mice. We focus on how individual neurons’ responses differed from the overall population. We find consistent spatial correlations in these differences that are unique to each trial and linearly scale with the cortical area observed, a characteristic of critical dynamics as confirmed in our neuronal simulations. Using chronic multi-electrode recordings, we observe similar scaling in the prefrontal and premotor cortex of non-human primates during self-initiated and visually cued motor tasks. These results suggest that trial-by-trial variability, rather than being random noise, reflects a critical, fluctuation-dominated state in the cortex, supporting the brain’s efficiency in processing information.
