Diverse coupling of neurons to populations in sensory cortex

• Published in: Nature (London) 2015-05, Vol.521 (7553), p.511-515
• Main Authors: Okun, Michael, Steinmetz, Nicholas A., Cossell, Lee, Iacaruso, M. Florencia, Ko, Ho, Barthó, Péter, Moore, Tirin, Hofer, Sonja B., Mrsic-Flogel, Thomas D., Carandini, Matteo, Harris, Kenneth D.
• Format: Article
• Language: English
• Subjects: 14/35; 14/69; 631/378/2613/1875; 64/110; 64/60; 9/30; 9/74; Analysis; Animals; Cerebral cortex; Female; Humanities and Social Sciences; letter; Macaca mulatta; Male; Mice; Models, Neurological; multidisciplinary; Neural circuitry; Neurology; Neurons; Neurons - cytology; Neurons - physiology; Neurophysiology; Optogenetics; Physiological aspects; Science; Sensory receptors; Structure; Synapses - physiology; Visual Cortex - cytology; Visual Cortex - physiology
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature14273

Exploring the relationship between population coupling and neuronal activity reveals that neighbouring neurons can differ in their coupling to the overall firing rate of the population, the circuitry of which may potentially help to explain the complex activity patterns in cortical populations. Cortical neurons and large-scale firing patterns The neurons that make up the cerebral cortex are diverse in their connectivity and function, raising the question of how activity between individual neurons is coordinated. Michael Okun et al . show that neurons in mouse and primate sensory cortex differ in the strength with which their activity correlates with the activity of the larger neuronal population in which they reside. This 'population coupling' is a stable feature, largely independent of sensory preference and cell class and also evident in the absence of sensory stimuli. Neurons with strong population coupling receive more synaptic inputs from their neighbours and are largely controlled by the local network, whereas those with weak coupling receive fewer inputs and seem to function autonomously. The diversity in how individual neurons' activities relate to the population rate, and the circuit mechanisms underlying this diversity, may help to explain the complex activity patterns in cortical populations. A large population of neurons can, in principle, produce an astronomical number of distinct firing patterns. In cortex, however, these patterns lie in a space of lower dimension 1 , 2 , 3 , 4 , as if individual neurons were “obedient members of a huge orchestra” 5 . Here we use recordings from the visual cortex of mouse ( Mus musculus ) and monkey ( Macaca mulatta ) to investigate the relationship between individual neurons and the population, and to establish the underlying circuit mechanisms. We show that neighbouring neurons can differ in their coupling to the overall firing of the population, ranging from strongly coupled ‘choristers’ to weakly coupled ‘soloists’. Population coupling is largely independent of sensory preferences, and it is a fixed cellular attribute, invariant to stimulus conditions. Neurons with high population coupling are more strongly affected by non-sensory behavioural variables such as motor intention. Population coupling reflects a causal relationship, predicting the response of a neuron to optogenetically driven increases in local activity. Moreover, population coupling indicates synaptic connectivity; the population coupling of