Conrado A. Bosman

Attentional stimulus selection through selective synchronization between monkey visual areas.

A central motif in neuronal networks is convergence, linking several input neurons to one target neuron. In visual cortex, convergence renders target neurons responsive to complex stimuli. Yet, convergence typically sends multiple stimuli to a target, and the behaviorally relevant stimulus must be selected. We used two stimuli, activating separate electrocorticographic V1 sites, and both activating an electrocorticographic V4 site equally strongly. When one of those stimuli activated one V1 site, it gamma synchronized (60-80 Hz) to V4. When the two stimuli activated two V1 sites, primarily the relevant one gamma synchronized to V4. Frequency bands of gamma activities showed substantial overlap containing the band of interareal coherence. The relevant V1 site had its gamma peak frequency 2-3 Hz higher than the irrelevant V1 site and 4-6 Hz higher than V4. Gamma-mediated interareal influences were predominantly directed from V1 to V4. We propose that selective synchronization renders relevant input effective, thereby modulating effective connectivity.

Visual areas exert feedforward and feedback influences through distinct frequency channels

Visual cortical areas subserve cognitive functions by interacting in both feedforward and feedback directions. While feedforward influences convey sensory signals, feedback influences modulate feedforward signaling according to the current behavioral context. We investigated whether these interareal influences are subserved differentially by rhythmic synchronization. We correlated frequency-specific directed influences among 28 pairs of visual areas with anatomical metrics of the feedforward or feedback character of the respective interareal projections. This revealed that in the primate visual system, feedforward influences are carried by theta-band (∼ 4 Hz) and gamma-band (∼ 60-80 Hz) synchronization, and feedback influences by beta-band (∼ 14-18 Hz) synchronization. The functional directed influences constrain a functional hierarchy similar to the anatomical hierarchy, but exhibiting task-dependent dynamic changes in particular with regard to the hierarchical positions of frontal areas. Our results demonstrate that feedforward and feedback signaling use distinct frequency channels, suggesting that they subserve differential communication requirements.

A MEMS-based flexible multichannel ECoG-electrode array.

We present a micromachined 252-channel ECoG (electrocorticogram)-electrode array, which is made of a thin polyimide foil substrate enclosing sputtered platinum electrode sites and conductor paths. The array subtends an area of approximately 35 mm by 60 mm and is designed to cover large parts of a hemisphere of a macaque monkeys cortex. Eight omnetics connectors are directly soldered to the foil. This leads to a compact assembly size which enables a chronic implantation of the array and allows free movements of the animal between the recording sessions. The electrode sites are 1 mm in diameter and were characterized by electrochemical impedance spectroscopy. At 1 kHz, the electrode impedances vary between 1.5 kOmega and 5 kOmega. The yield of functioning electrodes in three assembled devices is 99.5%. After implantation of a device with 100% working electrodes, standard electrocorticographic signals can be obtained from every electrode. The response to visual stimuli can be measured with electrodes lying on the visual cortex. After an implantation time of 4.5 months, all electrodes are still working and no decline in signal quality could be observed.

A Microsaccadic Rhythm Modulates Gamma-Band Synchronization and Behavior

Rhythms occur both in neuronal activity and in behavior. Behavioral rhythms abound at frequencies at or below 10 Hz. Neuronal rhythms cover a very wide frequency range, and the phase of neuronal low-frequency rhythms often rhythmically modulates the strength of higher-frequency rhythms, particularly of gamma-band synchronization (GBS). Here, we study stimulus-induced GBS in awake monkey areas V1 and V4 in relation to a specific form of spontaneous behavior, namely microsaccades (MSs), small fixational eye movements. We found that MSs occur rhythmically at a frequency of ∼3.3 Hz. The rhythmic MSs were predicted by the phase of the 3.3 Hz rhythm in V1 and V4 local field potentials. In turn, the MSs modulated both visually induced GBS and the speed of visually triggered behavioral responses. Fast/slow responses were preceded by a specific temporal pattern of MSs. These MS patterns induced perturbations in GBS that in turn explained variability in behavioral response speed. We hypothesize that the 3.3 Hz rhythm structures the sampling and exploration of the environment through building and breaking neuronal ensembles synchronized in the gamma-frequency band to process sensory stimuli.

Functions of gamma-band synchronization in cognition: from single circuits to functional diversity across cortical and subcortical systems

Gamma‐band activity (30–90 Hz) and the synchronization of neural activity in the gamma‐frequency range have been observed in different cortical and subcortical structures and have been associated with different cognitive functions. However, it is still unknown whether gamma‐band synchronization subserves a single universal function or a diversity of functions across the full spectrum of cognitive processes. Here, we address this question reviewing the mechanisms of gamma‐band oscillation generation and the functions associated with gamma‐band activity across several cortical and subcortical structures. Additionally, we raise a plausible explanation of why gamma rhythms are found so ubiquitously across brain structures. Gamma band activity originates from the interplay between inhibition and excitation. We stress that gamma oscillations, associated with this interplay, originate from basic functional motifs that conferred advantages for low‐level system processing and multiple cognitive functions throughout evolution. We illustrate the multifunctionality of gamma‐band activity by considering its role in neural systems for perception, selective attention, memory, motivation and behavioral control. We conclude that gamma‐band oscillations support multiple cognitive processes, rather than a single one, which, however, can be traced back to a limited set of circuit motifs which are found universally across species and brain structures.

Stimulus repetition modulates gamma-band synchronization in primate visual cortex

Significance When a visual stimulus repeats multiple times, visual cortical neurons show decreasing firing rate responses, yet neither perception nor stimulus-related behavior is compromised. We show that stimulus repetition leads to increased neuronal gamma-band (∼40–90 Hz) synchronization within and between early and higher visual areas. The enhanced gamma-band synchronization likely maintains effective stimulus signaling in the face of dwindling firing rates. We also show that synchronization to the gamma rhythm increases for spikes in general and for those of putative interneurons, whereas it decreases for spikes of putative excitatory neurons if they are not strongly stimulus-driven. Thus, inhibitory interneurons might create increasingly precise gamma-band synchronization, and thereby prune the stimulus representation by pyramidal cells to be sparser and more efficient. When a sensory stimulus repeats, neuronal firing rate and functional MRI blood oxygen level-dependent responses typically decline, yet perception and behavioral performance either stay constant or improve. An additional aspect of neuronal activity is neuronal synchronization, which can enhance the impact of neurons onto their postsynaptic targets independent of neuronal firing rates. We show that stimulus repetition leads to profound changes of neuronal gamma-band (∼40–90 Hz) synchronization. Electrocorticographic recordings in two awake macaque monkeys demonstrated that repeated presentations of a visual grating stimulus resulted in a steady increase of visually induced gamma-band activity in area V1, gamma-band synchronization between areas V1 and V4, and gamma-band activity in area V4. Microelectrode recordings in area V4 of two additional monkeys under the same stimulation conditions allowed a direct comparison of firing rates and gamma-band synchronization strengths for multiunit activity (MUA), as well as for isolated single units, sorted into putative pyramidal cells and putative interneurons. MUA and putative interneurons showed repetition-related decreases in firing rate, yet increases in gamma-band synchronization. Putative pyramidal cells showed no repetition-related firing rate change, but a decrease in gamma-band synchronization for weakly stimulus-driven units and constant gamma-band synchronization for strongly driven units. We propose that the repetition-related changes in gamma-band synchronization maintain the interareal stimulus signaling and sharpen the stimulus representation by gamma-synchronized pyramidal cell spikes.

Visual Cortical Gamma-Band Activity During Free Viewing of Natural Images

Gamma-band activity in visual cortex has been implicated in several cognitive operations, like perceptual grouping and attentional selection. So far, it has been studied primarily under well-controlled visual fixation conditions and using well-controlled stimuli, like isolated bars or patches of grating. If gamma-band activity is to subserve its purported functions outside of the laboratory, it should be present during natural viewing conditions. We recorded neuronal activity with a 252-channel electrocorticographic (ECoG) grid covering large parts of the left hemisphere of 2 macaque monkeys, while they freely viewed natural images. We found that natural viewing led to pronounced gamma-band activity in the visual cortex. In area V1, gamma-band activity during natural viewing showed a clear spectral peak indicative of oscillatory activity between 50 and 80 Hz and was highly significant for each of 65 natural images. Across the ECoG grid, gamma-band activity during natural viewing was present over most of the recorded visual cortex and absent over most remaining cortex. After saccades, the gamma peak frequency slid down to 30–40 Hz at around 80 ms postsaccade, after which the sustained 50- to 80-Hz gamma-band activity resumed. We propose that gamma-band activity plays an important role during natural viewing.

A DCM study of spectral asymmetries in feedforward and feedback connections between visual areas V1 and V4 in the monkey

This paper reports a dynamic causal modeling study of electrocorticographic (ECoG) data that addresses functional asymmetries between forward and backward connections in the visual cortical hierarchy. Specifically, we ask whether forward connections employ gamma-band frequencies, while backward connections preferentially use lower (beta-band) frequencies. We addressed this question by modeling empirical cross spectra using a neural mass model equipped with superficial and deep pyramidal cell populations—that model the source of forward and backward connections, respectively. This enabled us to reconstruct the transfer functions and associated spectra of specific subpopulations within cortical sources. We first established that Bayesian model comparison was able to discriminate between forward and backward connections, defined in terms of their cells of origin. We then confirmed that model selection was able to identify extrastriate (V4) sources as being hierarchically higher than early visual (V1) sources. Finally, an examination of the auto spectra and transfer functions associated with superficial and deep pyramidal cells confirmed that forward connections employed predominantly higher (gamma) frequencies, while backward connections were mediated by lower (alpha/beta) frequencies. We discuss these findings in relation to current views about alpha, beta, and gamma oscillations and predictive coding in the brain.

How to detect the Granger-causal flow direction in the presence of additive noise?

Granger-causality metrics have become increasingly popular tools to identify directed interactions between brain areas. However, it is known that additive noise can strongly affect Granger-causality metrics, which can lead to spurious conclusions about neuronal interactions. To solve this problem, previous studies have proposed the detection of Granger-causal directionality, i.e. the dominant Granger-causal flow, using either the slope of the coherency (Phase Slope Index; PSI), or by comparing Granger-causality values between original and time-reversed signals (reversed Granger testing). We show that for ensembles of vector autoregressive (VAR) models encompassing bidirectionally coupled sources, these alternative methods do not correctly measure Granger-causal directionality for a substantial fraction of VAR models, even in the absence of noise. We then demonstrate that uncorrelated noise has fundamentally different effects on directed connectivity metrics than linearly mixed noise, where the latter may result as a consequence of electric volume conduction. Uncorrelated noise only weakly affects the detection of Granger-causal directionality, whereas linearly mixed noise causes a large fraction of false positives for standard Granger-causality metrics and PSI, but not for reversed Granger testing. We further show that we can reliably identify cases where linearly mixed noise causes a large fraction of false positives by examining the magnitude of the instantaneous influence coefficient in a structural VAR model. By rejecting cases with strong instantaneous influence, we obtain an improved detection of Granger-causal flow between neuronal sources in the presence of additive noise. These techniques are applicable to real data, which we demonstrate using actual area V1 and area V4 LFP data, recorded from the awake monkey performing a visual attention task.

Proceedings of the Third International Workshop on Advances in Electrocorticography

The Third International Workshop on Advances in Electrocorticography (ECoG) was convened in Washington, DC, on November 10-11, 2011. As in prior meetings, a true multidisciplinary fusion of clinicians, scientists, and engineers from many disciplines gathered to summarize contemporary experiences in brain surface recordings. The proceedings of this meeting serve as evidence of a very robust and transformative field but will yet again require revision to incorporate the advances that the following year will surely bring.