Learning alters theta-nested gamma oscillations in inferotemporal cortex

How coupled brain rhythms influence cortical information processing to support learning is unresolved. Local field potential and neuronal activity recordings from 64- electrode arrays in sheep inferotemporal cortex showed that visual discrimination learning increased the amplitude of theta oscillations during stimulus presentation. Coupling between theta and gamma oscillations, the theta/gamma ratio and the regularity of theta phase were also increased, but not neuronal firing rates. A neural network model with fast and slow inhibitory interneurons was developed which generated theta nested gamma. By increasing N-methyl-D-aspartate receptor sensitivity similar learning-evoked changes could be produced. The model revealed that altered theta nested gamma could potentiate downstream neuron responses by temporal desynchronization of excitatory neuron output independent of changes in overall firing frequency. This learning-associated desynchronization was also exhibited by inferotemporal cortex neurons. Changes in theta nested gamma may therefore facilitate learning-associated potentiation by temporal modulation of neuronal firing

Inhibitory synchrony as a mechanism for attentional gain modulation

Recordings from area V4 of monkeys have revealed that when the focus of attention is on a visual stimulus within the receptive field of a cortical neuron, two distinct changes can occur: The firing rate of the neuron can change and there can be an increase in the coherence between spikes and the local field potential in the gamma-frequency range (30-50 Hz). The hypothesis explored here is that these observed effects of attention could be a consequence of changes in the synchrony of local interneuron networks. We performed computer simulations of a Hodgkin-Huxley type neuron driven by a constant depolarizing current, I, representing visual stimulation and a modulatory inhibitory input representing the effects of attention via local interneuron networks. We observed that the neuron's firing rate and the coherence of its output spike train with the synaptic inputs was modulated by the degree of synchrony of the inhibitory inputs. The model suggest that the observed changes in firing rate and coherence of neurons in the visual cortex could be controlled by top-down inputs that regulated the coherence in the activity of a local inhibitory network discharging at gamma frequencies.Comment: J.Physiology (Paris) in press, 11 figure

LFP beta amplitude is predictive of mesoscopic spatio-temporal phase patterns

Beta oscillations observed in motor cortical local field potentials (LFPs) recorded on separate electrodes of a multi-electrode array have been shown to exhibit non-zero phase shifts that organize into a planar wave propagation. Here, we generalize this concept by introducing additional classes of patterns that fully describe the spatial organization of beta oscillations. During a delayed reach-to-grasp task in monkey primary motor and dorsal premotor cortices we distinguish planar, synchronized, random, circular, and radial phase patterns. We observe that specific patterns correlate with the beta amplitude (envelope). In particular, wave propagation accelerates with growing amplitude, and culminates at maximum amplitude in a synchronized pattern. Furthermore, the occurrence probability of a particular pattern is modulated with behavioral epochs: Planar waves and synchronized patterns are more present during movement preparation where beta amplitudes are large, whereas random phase patterns are dominant during movement execution where beta amplitudes are small

Perception-related modulations of local field potential power and coherence in primary visual cortex of awake monkey during binocular rivalry

Cortical synchronization at γ-frequencies (35–90 Hz) has been proposed to define the connectedness among the local parts of a perceived visual object. This hypothesis is still under debate. We tested it under conditions of binocular rivalry (BR), where a monkey perceived alternations among conflicting gratings presented singly to each eye at orthogonal orientations. We made multi-channel microelectrode recordings of multi-unit activity (MUA) and local field potentials (LFP) from striate cortex (V1) during BR while the monkey indicated his perception by pushing a lever. We analyzed spectral power and coherence of MUA and LFP over 4–90 Hz. As in previous work, coherence of γ-signals in most pairs of recording locations strongly depended on grating orientation when stimuli were presented congruently in both eyes. With incongruent (rivalrous) stimulation LFP power was often consistently modulated in consonance with the perceptual state. This was not visible in MUA. These perception-related modulations of LFP occurred at low and medium frequencies (<30 Hz), but not at γ-frequencies. Perception-related modulations of LFP coherence were also restricted to the low–medium range. In conclusion, our results do not support the expectation that γ-synchronization in V1 is related to the perceptual state during BR, but instead suggest a perception-related role of synchrony at low and medium frequencies

An Interneuron Circuit Reproducing Essential Spectral Features of Field Potentials

This document is the Accepted Manuscript version of the following article: Reinoud Maex, ‘An Interneuron Circuit Reproducing Essential Spectral Features of Field Potentials’, Neural Computation, March 2018. Under embargo until 22 June 2018. The final, definitive version of this paper is available online at doi: https://doi.org/10.1162/NECO_a_01068. © 2018 Massachusetts Institute of Technology. Content in the UH Research Archive is made available for personal research, educational, and non-commercial purposes only. Unless otherwise stated, all content is protected by copyright, and in the absence of an open license, permissions for further re-use should be sought from the publisher, the author, or other copyright holder.Recent advances in engineering and signal processing have renewed the interest in invasive and surface brain recordings, yet many features of cortical field potentials remain incompletely understood. In the present computational study, we show that a model circuit of interneurons, coupled via both GABA(A) receptor synapses and electrical synapses, reproduces many essential features of the power spectrum of local field potential (LFP) recordings, such as 1/f power scaling at low frequency (< 10 Hz) , power accumulation in the γ-frequency band (30–100 Hz), and a robust α rhythm in the absence of stimulation. The low-frequency 1/f power scaling depends on strong reciprocal inhibition, whereas the α rhythm is generated by electrical coupling of intrinsically active neurons. As in previous studies, the γ power arises through the amplifica- tion of single-neuron spectral properties, owing to the refractory period, by parameters that favour neuronal synchrony, such as delayed inhibition. The present study also confirms that both synaptic and voltage-gated membrane currents substantially contribute to the LFP, and that high-frequency signals such as action potentials quickly taper off with distance. Given the ubiquity of electrically coupled interneuron circuits in the mammalian brain, they may be major determinants of the recorded potentials.Peer reviewe

Large-scale changes in cortical dynamics triggered by repetitive somatosensory electrical stimulation.

BackgroundRepetitive somatosensory electrical stimulation (SES) of forelimb peripheral nerves is a promising therapy; studies have shown that SES can improve motor function in stroke subjects with chronic deficits. However, little is known about how SES can directly modulate neural dynamics. Past studies using SES have primarily used noninvasive methods in human subjects. Here we used electrophysiological recordings from the rodent primary motor cortex (M1) to assess how SES affects neural dynamics at the level of single neurons as well as at the level of mesoscale dynamics.MethodsWe performed acute extracellular recordings in 7 intact adult Long Evans rats under ketamine-xylazine anesthesia while they received transcutaneous SES. We recorded single unit spiking and local field potentials (LFP) in the M1 contralateral to the stimulated arm. We then compared neural firing rate, spike-field coherence (SFC), and power spectral density (PSD) before and after stimulation.ResultsFollowing SES, the firing rate of a majority of neurons changed significantly from their respective baseline values. There was, however, a diversity of responses; some neurons increased while others decreased their firing rates. Interestingly, SFC, a measure of how a neuron's firing is coupled to mesoscale oscillatory dynamics, increased specifically in the δ-band, also known as the low frequency band (0.3- 4 Hz). This increase appeared to be driven by a change in the phase-locking of broad-spiking, putative pyramidal neurons. These changes in the low frequency range occurred without a significant change in the overall PSD.ConclusionsRepetitive SES significantly and persistently altered the local cortical dynamics of M1 neurons, changing both firing rates as well as the SFC magnitude in the δ-band. Thus, SES altered the neural firing and coupling to ongoing mesoscale dynamics. Our study provides evidence that SES can directly modulate cortical dynamics

A computational study on altered theta-gamma coupling during learning and phase coding

There is considerable interest in the role of coupling between theta and gamma oscillations in the brain in the context of learning and memory. Here we have used a neural network model which is capable of producing coupling of theta phase to gamma amplitude firstly to explore its ability to reproduce reported learning changes and secondly to memory-span and phase coding effects. The spiking neural network incorporates two kinetically different GABAA receptor-mediated currents to generate both theta and gamma rhythms and we have found that by selective alteration of both NMDA receptors and GABAA,slow receptors it can reproduce learning-related changes in the strength of coupling between theta and gamma either with or without coincident changes in theta amplitude. When the model was used to explore the relationship between theta and gamma oscillations, working memory capacity and phase coding it showed that the potential storage capacity of short term memories, in terms of nested gamma-subcycles, coincides with the maximal theta power. Increasing theta power is also related to the precision of theta phase which functions as a potential timing clock for neuronal firing in the cortex or hippocampus

Membrane resonance enables stable and robust gamma oscillations

Neuronal mechanisms underlying beta/gamma oscillations (20-80 Hz) are not completely understood. Here, we show that in vivo beta/gamma oscillations in the cat visual cortex sometimes exhibit remarkably stable frequency even when inputs fluctuate dramatically. Enhanced frequency stability is associated with stronger oscillations measured in individual units and larger power in the local field potential. Simulations of neuronal circuitry demonstrate that membrane properties of inhibitory interneurons strongly determine the characteristics of emergent oscillations. Exploration of networks containing either integrator or resonator inhibitory interneurons revealed that: (i) Resonance, as opposed to integration, promotes robust oscillations with large power and stable frequency via a mechanism called RING (Resonance INduced Gamma); resonance favors synchronization by reducing phase delays between interneurons and imposes bounds on oscillation cycle duration; (ii) Stability of frequency and robustness of the oscillation also depend on the relative timing of excitatory and inhibitory volleys within the oscillation cycle; (iii) RING can reproduce characteristics of both Pyramidal INterneuron Gamma (PING) and INterneuron Gamma (ING), transcending such classifications; (iv) In RING, robust gamma oscillations are promoted by slow but are impaired by fast inputs. Results suggest that interneuronal membrane resonance can be an important ingredient for generation of robust gamma oscillations having stable frequency

Spiking Dynamics during Perceptual Grouping in the Laminar Circuits of Visual Cortex

Grouping of collinear boundary contours is a fundamental process during visual perception. Illusory contour completion vividly illustrates how stable perceptual boundaries interpolate between pairs of contour inducers, but do not extrapolate from a single inducer. Neural models have simulated how perceptual grouping occurs in laminar visual cortical circuits. These models predicted the existence of grouping cells that obey a bipole property whereby grouping can occur inwardly between pairs or greater numbers of similarly oriented and co-axial inducers, but not outwardly from individual inducers. These models have not, however, incorporated spiking dynamics. Perceptual grouping is a challenge for spiking cells because its properties of collinear facilitation and analog sensitivity to inducer configurations occur despite irregularities in spike timing across all the interacting cells. Other models have demonstrated spiking dynamics in laminar neocortical circuits, but not how perceptual grouping occurs. The current model begins to unify these two modeling streams by implementing a laminar cortical network of spiking cells whose intracellular temporal dynamics interact with recurrent intercellular spiking interactions to quantitatively simulate data from neurophysiological experiments about perceptual grouping, the structure of non-classical visual receptive fields, and gamma oscillations.CELEST, an NSF Science of Learning Center (SBE-0354378); SyNAPSE program of the Defense Advanced Research Project Agency (HR001109-03-0001); Defense Advanced Research Project Agency (HR001-09-C-0011

Gamma-band synchronization in the macaque hippocampus and memory formation

Increasing evidence suggests that neuronal synchronization in the gamma band (30–100 Hz) may play an important role in mediating cognitive processes. Gamma-band synchronization provides for the optimal temporal relationship between two signals to produce the long-term synaptic changes that have been theorized to underlie memory formation. Although neuronal populations in the hippocampus oscillate in the gamma range, the role of these oscillations in memory formation is still unclear. To address this issue, we recorded neuronal activity in the hippocampus while macaque monkeys performed a visual recognition memory task. During the encoding phase of this task, hippocampal neurons displayed gamma-band synchronization. Additionally, enhanced gamma-band synchronization during encoding predicted greater subsequent recognition memory performance. These changes in synchronization reflect enhanced coordination among hippocampal neurons and may facilitate synaptic changes necessary for successful memory encoding