The Spatial Reach of Neuronal Coherence and Spike-field Coupling across the Human Neocortex

Neuronal coherence is thought to be a fundamental mechanism of communication in the brain, where synchronized field potentials coordinate synaptic and spiking events to support plasticity and learning. Although the spread of field potentials has garnered great interest, little is known about the spatial reach of phase synchronization, or neuronal coherence. Functional connectivity between different brain regions is known to occur across long distances, but the locality of coherence within a brain region is understudied. Here we used simultaneous recordings from electrocorticography (ECoG) grids and high-density microelectrode arrays to estimate the spatial reach of neuronal coherence and spike-field coherence (SFC) across frontal, temporal, and occipital cortices during cognitive tasks in humans. We observed the strongest coherence within a 2-3 cm distance from the microelectrode arrays, potentially defining an effective range for local communication. This range was relatively consistent across brain regions, spectral frequencies, and cognitive tasks. The magnitude of coherence showed power law decay with increasing distance from the microelectrode arrays, where the highest coherence occurred between ECoG contacts, followed by coherence between ECoG and deep cortical LFP, and then SFC (i.e., ECoG > LFP > SFC). The spectral frequency of coherence also affected its magnitude. Alpha coherence (8-14 Hz) was generally higher than other frequencies for signals nearest the microelectrode arrays, whereas delta coherence (1-3 Hz) was higher for signals that were farther away. Action potentials in all brain regions were most coherent with the phase of alpha oscillations, which suggests that alpha waves could play a larger, more spatially local role in spike timing than other frequencies. These findings provide a deeper understanding of the spatial and spectral dynamics of neuronal coherence, further advancing knowledge about how activity propagates across the human brain.

Neuronal Coherence Agent for Shared Intentionality: A Hypothesis of Neurobiological Processes Occurring during Social Interaction

The present interdisciplinary study discusses the physical foundations of the neurobiological processes occurring during social interaction. The review of the literature establishes the difference between Intentionality and Intention, thereby proposing the theoretical basis of Shared Intentionality in humans. According to the present study, Shared Intentionality in humans (Goal-directed coherence of biological systems), which is the ability among social organisms to instantly select just one stimulus for the entire group, is the outcome of evolutionary development. Therefore, this interaction modality should be the preferred, archetypal, and most propagated modality in organisms, attributed to the Model of Hierarchical Complexity Stage 3. This characteristic of biological systems facilitates the training of the new members of the group and also ensures efficient cooperation among the members of the group without requiring communication. In humans, Shared Intentionality contributes to the learning of newborns. The neurons of a mature organism may teach the neonate neurons regarding the fitting reactions to the excitatory inputs of the specific structural organization. This enables the neonate neurons to develop a Long-Term Potentiation that links particular stimuli with specific embodied sensorimotor neural networks. The present report discusses three possible neuronal coherence agents that could involve quantum mechanisms in cells, thereby enabling the distribution of the quality of goal-directed coherence in biological systems (Shared Intentionality in humans). Recently reported case studies conducted online with the task of conveying the meaning of numerosity to the children of age 18–33 months revealed the occurrence of Shared Intentionality in mother-child dyads in the absence of sensory cues between the two, which promoted cognitive development in the children. The findings of these case studies support the concept of physical foundations and the hypothesis of the neurophysiological process of social interaction proposed in the present study.

Functional inhibition across a visuomotor communication channel coordinates looking and reaching

Understanding how natural behaviors are controlled depends on understanding the neural mechanisms of multiregional communication. Eye-hand coordination, a natural behavior shared by primates, is controlled by the posterior parietal cortex (PPC), a brain structure that expanded substantially in primate evolution. Here, we show that neurons within the saccade and reach regions within PPC communicate over a visuomotor channel to coordinate looking and reaching. During gaze-anchoring behavior, when saccades are transiently-inhibited by coordinated reaches, PPC neuron firing rates covary with beta-frequency (15-25 Hz) neuronal coherence. Decreases in parietal saccade neuron spiking correlated with gaze-anchoring behavior when the channel was “open” and not “closed”. Functional inhibition across beta-frequency-coherent communication channels may be a general mechanism for flexibly coordinating our natural behavior.One Sentence SummaryInhibitory communication through a visuomotor channel mediates the coordination of eye and hand movements.

Distinct sensorimotor feedback loops for dynamic and static control of primate precision grip

Volitional limb motor control involves dynamic and static muscle actions. It remains elusive how such distinct actions are controlled through separated or shared neural circuits. Here we explored the potential separation for dynamic and static controls in the primate hand actions, by investigating the neuronal coherence between local 1eld potentials (LFPs) of the spinal cord and the forelimb electromyographic activity (EMGs), and LFPs of the motor cortex and the EMGs during the performance of a precision grip in macaque monkeys. We observed the emergence of beta-range coherence with EMGs at spinal cord and motor cortex in the separated phases; spinal coherence during the grip phase and cortical coherence during the hold phase. Further, both of the coherence were influenced by bidirectional interactions with reasonable latencies as beta oscillatory cycles. These results indicate that dedicated feedback circuits comprising spinal and cortical structures underlie dynamic and static controls of dexterous hand actions.

Local differences in neuronal activation level decorrelate spatially coherent global fluctuations in gamma rhythms

Neuronal coherence is thought to constitute a unique substrate for information transmission distinct from firing rate. However, since the spatial scale of extracellular oscillations typically exceeds that of firing rates, it is unclear whether coherence complements or compromises the rate code. We examined responses in the macaque primary visual cortex and found that fluctuations in gamma-band (~40Hz) neuronal coherence correlated more with firing rate than oscillations in the local-field-potential (LFP). Although the spatial extent of LFP rhythms was broader, that of neuronal coherence was indistinguishable from firing rates. To identify the mechanism, we developed a statistical technique to isolate the rhythmic component of the spiking process and found that above results are explained by an activation-dependent increase in neuronal sensitivity to gamma-rhythmic input. Such adaptive changes in sensitivity to rhythmic inputs might constitute a fundamental homeostatic mechanism that prevents globally coherent inputs from undermining spatial resolution of the neural code.

Neurophysiological and Computational Principles of Cortical Rhythms in Cognition

Synchronous rhythms represent a core mechanism for sculpting temporal coordination of neural activity in the brain-wide network. This review focuses on oscillations in the cerebral cortex that occur during cognition, in alert behaving conditions. Over the last two decades, experimental and modeling work has made great strides in elucidating the detailed cellular and circuit basis of these rhythms, particularly gamma and theta rhythms. The underlying physiological mechanisms are diverse (ranging from resonance and pacemaker properties of single cells to multiple scenarios for population synchronization and wave propagation), but also exhibit unifying principles. A major conceptual advance was the realization that synaptic inhibition plays a fundamental role in rhythmogenesis, either in an interneuronal network or in a reciprocal excitatory-inhibitory loop. Computational functions of synchronous oscillations in cognition are still a matter of debate among systems neuroscientists, in part because the notion of regular oscillation seems to contradict the common observation that spiking discharges of individual neurons in the cortex are highly stochastic and far from being clocklike. However, recent findings have led to a framework that goes beyond the conventional theory of coupled oscillators and reconciles the apparent dichotomy between irregular single neuron activity and field potential oscillations. From this perspective, a plethora of studies will be reviewed on the involvement of long-distance neuronal coherence in cognitive functions such as multisensory integration, working memory, and selective attention. Finally, implications of abnormal neural synchronization are discussed as they relate to mental disorders like schizophrenia and autism.