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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.sup.1,2,3,4, as if individual neurons were 'obedient members of a huge orchestra'.sup.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 a neuron, measured in vivo, predicted subsequent in vitro estimates of the number of synapses received from its neighbours. Finally, population coupling provides a compact summary of population activity; knowledge of the population couplings of n neurons predicts a substantial portion of their n.sup.2 pairwise correlations. Population coupling therefore represents a novel, simple measure that characterizes the relationship of each neuron to a larger population, explaining seemingly complex network firing patterns in terms of basic circuit variables., Author(s): Michael Okun [sup.1] [sup.2] [sup.3] , Nicholas A. Steinmetz [sup.1] [sup.2] [sup.3] [sup.4] , Lee Cossell [sup.2] [sup.5] , M. Florencia Iacaruso [sup.2] [sup.5] , Ho Ko [sup.2] [sup.7] [...]

Episodic learning and memory retrieval are dependent on hippocampal theta oscillation, thought to rely on the GABAergic network of the medial septum (MS). To test how this network achieves theta synchrony, we recorded MS neurons and hippocampal local field potential simultaneously in anesthetized and awake mice and rats. We show that MS pacemakers synchronize their individual rhythmicity frequencies, akin to coupled pendulum clocks as observed by Huygens. We optogenetically identified them as parvalbumin-expressing GABAergic neurons, while MS glutamatergic neurons provide tonic excitation sufficient to induce theta. In accordance, waxing and waning tonic excitation is sufficient to toggle between theta and non-theta states in a network model of single-compartment inhibitory pacemaker neurons. These results provide experimental and theoretical support to a frequency-synchronization mechanism for pacing hippocampal theta, which may serve as an inspirational prototype for synchronization processes in the central nervous system from Nematoda to Arthropoda to Chordate and Vertebrate phyla. [Display omitted] • MS pacemakers show Huygens synchronization • MS pacemakers are parvalbumin-expressing GABAergic neurons • MS glutamatergic neurons provide tonic excitation sufficient to induce theta • A network model of a homogeneous GABAergic population reproduces experimental data How medial septal (MS) neurons synchronize to generate hippocampal theta oscillation is not well understood. Kocsis et al. find that MS GABAergic neurons synchronize their individual rhythmicity frequencies, similar to coupled pendulum clocks, while MS glutamatergic neurons provide tonic excitatory drive to the pacemaker network sufficient to induce theta. [ABSTRACT FROM AUTHOR]

The zona incerta (ZI) is at the crossroad of almost all major ascending and descending fiber tracts and targets numerous brain centers from the thalamus to the spinal cord. Effective ascending drive of ZI cells has been described, but the role of descending cortical signals in patterning ZI activity is unknown. Cortical control over ZI function was examined during slow cortical waves (1-3 Hz), paroxysmal high-voltage spindles (HVSs), and 5-9 Hz oscillations in anesthetized rats. In all conditions, rhythmic cortical activity significantly altered the firing pattern of ZI neurons recorded extracellularly and labeled with the juxtacellular method. During slow oscillations, the majority of ZI neurons became synchronized to the depth-negative phase ("up state") of the cortical waves to a degree comparable to thalamocortical neurons. During HVSs, ZI cells displayed highly rhythmic activity in tight synchrony with the cortical oscillations. ZI neurons responded to short epochs of cortical 5-9 Hz oscillations, with a change in the interspike interval distribution and with an increase in spectral density in the 5-9 Hz band as measured by wavelet analysis. Morphological reconstruction revealed that most ZI cells have mediolaterally extensive dendritic trees and very long dendritic segments. Cortical terminals established asymmetrical synapses on ZI cells with very long active zones. These data suggest efficient integration of widespread cortical signals by single ZI neurons and strong cortical drive. We propose that the efferent GABAergic signal of ZI neurons patterned by the cortical activity can play a critical role in synchronizing thalamocortical and brainstem rhythms. [ABSTRACT FROM AUTHOR]