SUMMARY 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 inter-areal 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 inter-areal influences were predominantly directed from V1 to V4. We propose that selective synchronization renders relevant input effective, thereby modulating effective connectivity.
Current theories propose that coherence of oscillatory brain activity in the gamma band (30-80 Hz) constitutes an avenue for communication among remote neural populations. However, reports documenting stimulus dependency and time variability of gamma frequency suggest that distant neuronal populations may, at any one time, operate at different frequencies precluding synchronization. To test this idea, we recorded from macaque V1 and V2 simultaneously while presenting gratings of varying contrast. Although gamma frequency increased with stimulus contrast in V1 and V2 (by ∼25 Hz), V1-V2 gamma coherence was maintained for all contrasts. Moreover, while gamma frequency fluctuated by ∼15 Hz during constant contrast stimulation, this fluctuation was highly correlated between V1 and V2. The strongest coherence connections showed a layer-specific pattern, matching feedforward anatomical connectivity. Hence, gamma coherence among remote populations can occur despite large stimulus-induced and time-dependent changes in gamma frequency, allowing communication through coherence to operate without a stimulus independent, fixed-frequency gamma channel.
Humans’ ability to rapidly and accurately detect, identify, and classify faces under variable conditions derives from a network of brain regions highly tuned to face information. The fusiform face area (FFA) is thought to be a computational hub for face processing, however temporal dynamics of face information processing in FFA remains unclear. Here we use multivariate pattern classification to decode the temporal dynamics of expression-invariant face information processing using electrodes placed directly upon FFA in humans. Early FFA activity (50-75 ms) contained information regarding whether participants were viewing a face. Activity between 200-500 ms contained expression-invariant information about which of 70 faces participants were viewing along with the individual differences in facial features and their configurations. Long-lasting (500+ ms) broadband gamma frequency activity predicted task performance. These results elucidate the dynamic computational role FFA plays in multiple face processing stages and indicate what information is used in performing these visual analyses.
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.adaptation | learning | oscillation | plasticity | priming S timulus repetition typically leads to reduced neuronal firing rates and reduced functional MRI blood oxygen leveldependent signals, whereas behavior that is based on stimulus processing is not affected or is enhanced (1). Different models have been proposed to reconcile these behavioral and neurophysiological findings (1). In a "fatigue model," neuronal responses are reduced in proportion to their amplitude, leaving relative response patterns unchanged; in a "sharpening model," neurons that code features irrelevant to identification of a stimulus exhibit repetition suppression, leading to a sparser and sharpened representation of the repeated stimulus; and in a "facilitation model," stimulus repetition leads to faster stimulus processing, and thereby smaller overall neuronal activity. Gotts and coworkers (2-4) suggested a "synchronization model" in which stimulus repetition leads to reduced firing rates accompanied by increased synchronization. The increased synchronization might explain how less-activated neuronal groups can maintain their impact onto postsynaptic neurons and, ultimately, behavior, while reducing metabolic costs at the same time. The synchronization model has received support from a number of studies in human subjects, using source-localized magnetoencephalography. Ghuman et al. (5) report enhanced ...
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.
Using high-density electrocorticographic recordings – from awake-behaving monkeys – and dynamic causal modelling, we characterised contrast dependent gain control in visual cortex, in terms of synaptic rate constants and intrinsic connectivity. Specifically, we used neural field models to quantify the balance of excitatory and inhibitory influences; both in terms of the strength and spatial dispersion of horizontal intrinsic connections. Our results allow us to infer that increasing contrast increases the sensitivity or gain of superficial pyramidal cells to inputs from spiny stellate populations. Furthermore, changes in the effective spatial extent of horizontal coupling nuance the spatiotemporal filtering properties of cortical laminae in V1 — effectively preserving higher spatial frequencies. These results are consistent with recent non-invasive human studies of contrast dependent changes in the gain of pyramidal cells elaborating forward connections — studies designed to test specific hypotheses about precision and gain control based on predictive coding. Furthermore, they are consistent with established results showing that the receptive fields of V1 units shrink with increasing visual contrast.
Performing different tasks, such as generating motor movements or processing sensory input, requires the recruitment of specific networks of neuronal populations. Previous studies suggested that power variations in the alpha band (8–12 Hz) may implement such recruitment of task-specific populations by increasing cortical excitability in task-related areas while inhibiting population-level cortical activity in task-unrelated areas (Klimesch et al., 2007; Jensen and Mazaheri, 2010). However, the precise temporal and spatial relationships between the modulatory function implemented by alpha oscillations and population-level cortical activity remained undefined. Furthermore, while several studies suggested that alpha power indexes task-related populations across large and spatially separated cortical areas, it was largely unclear whether alpha power also differentially indexes smaller networks of task-related neuronal populations. Here we addressed these questions by investigating the temporal and spatial relationships of electrocorticographic (ECoG) power modulations in the alpha band and in the broadband gamma range (70–170 Hz, indexing population-level activity) during auditory and motor tasks in five human subjects and one macaque monkey. In line with previous research, our results confirm that broadband gamma power accurately tracks task-related behavior and that alpha power decreases in task-related areas. More importantly, they demonstrate that alpha power suppression lags population-level activity in auditory areas during the auditory task, but precedes it in motor areas during the motor task. This suppression of alpha power in task-related areas was accompanied by an increase in areas not related to the task. In addition, we show for the first time that these differential modulations of alpha power could be observed not only across widely distributed systems (e.g., motor vs. auditory system), but also within the auditory system. Specifically, alpha power was suppressed in the locations within the auditory system that most robustly responded to particular sound stimuli. Altogether, our results provide experimental evidence for a mechanism that preferentially recruits task-related neuronal populations by increasing cortical excitability in task-related cortical areas and decreasing cortical excitability in task-unrelated areas. This mechanism is implemented by variations in alpha power and is common to humans and the non-human primate under study. These results contribute to an increasingly refined understanding of the mechanisms underlying the selection of the specific neuronal populations required for task execution.
Guanine nucleotide dissociation inhibitors (GDIs) regulate both GDP/GTP and membrane association/dissociation cycles of Rho/Rac and Rab proteins. RhoGDI-3 is distinguishable from other rhoGDI proteins by its partial association with a detergent-resistant subcellular fraction. Here, we investigate the activity of this unusual rhoGDI using confocal laser scanning microscopy, immuno-isolation, and rhoGDI-3 mutants. We establish that the noncytosolic fraction of rhoGDI-3 is associated with the Golgi apparatus. The domain involved in this association is the unique N-terminal segment of rhoGDI-3 predicted to form an amphipathic a helix. This peptide is indispensable for Golgi association of rhoGDI-3 and sufficient to address a green fluorescent protein to the Golgi apparatus. Site-directed mutations, decreasing the hydrophobic surface of the helix, localize rhoGDI-3 into the cytoplasm. We establish that rhoGDI-3 is able to inhibit activation of the RhoG protein and to target this protein to the Golgi apparatus. Furthermore, we demonstrate the importance of the rhoGDI-3 N-terminal segment for both Golgi targeting and stability of the cytoplasmic RhoG/rhoGDI-3 complex. RhoGDI-3 is the first example of a GDI directly involved in the delivery of a Rho protein to a specific subcellular compartment.
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