Sergio Neuenschwander

Neural synchrony in cortical networks: history, concept and current status

Following the discovery of context-dependent synchronization of oscillatory neuronal responses in the visual system, the role of neural synchrony in cortical networks has been expanded to provide a general mechanism for the coordination of distributed neural activity patterns. In the current paper, we present an update of the status of this hypothesis through summarizing recent results from our laboratory that suggest important new insights regarding the mechanisms, function and relevance of this phenomenon. In the first part, we present recent results derived from animal experiments and mathematical simulations that provide novel explanations and mechanisms for zero and nero-zero phase lag synchronization. In the second part, we shall discuss the role of neural synchrony for expectancy during perceptual organization and its role in conscious experience. This will be followed by evidence that indicates that in addition to supporting conscious cognition, neural synchrony is abnormal in major brain disorders, such as schizophrenia and autism spectrum disorders. We conclude this paper with suggestions for further research as well as with critical issues that need to be addressed in future studies.

Rapid feature selective neuronal synchronization through correlated latency shifting

Spontaneous brain activity could affect processing if it were structured, . We show that neuron pairs in cat primary visual cortex exhibited correlated fluctuations in response latency, particularly when they had overlapping receptive fields or similar orientation preferences. Correlations occurred within and across hemispheres, but only when local field potentials (LFPs) oscillated in the gamma-frequency range (40–70 Hz). In this range, LFP fluctuations preceding response onset predicted response latencies; negative (positive) LFPs were associated with early (late) responses. Oscillations below 10 Hz caused covariations in response amplitude, but exhibited no columnar selectivity or coordinating effect on latencies. Thus, during high gamma activity, spontaneous activity exhibits distinct, column-specific correlation patterns. Consequently, cortical cells undergo coherent fluctuations in excitability that enhance temporal coherence of responses to contours that are spatially contiguous or have similar orientation. Because synchronized responses are more likely than dispersed responses to undergo rapid and joint processing, spontaneous activity may be important in early visual processes.

Neuronal assemblies: necessity, signature and detectability.

The ease with which highly developed brains can generate representations of a virtually unlimited diversity of perceptual objects indicates that they have developed very efficient mechanisms to analyse and represent relations among incoming signals. Here, we propose that two complementary strategies are applied to cope with these combinatorial problems. First, elementary relations are represented by the tuned responses of individual neurons that acquire their specific response properties (feature selectivity) through appropriate convergence of input connections in hierarchically structured feed-forward architectures. Second, complex relations that cannot be represented economically by the responses of individual neurons are represented by assemblies of cells that are generated by dynamic association of individual, featureselective cells. The signature identifying the responses of an assembly as components of a coherent code is thought to be the synchronicity of the respective discharges. The compatibility of this hypothesis is examined in the context of recent data on the dynamics of synchronization phenomena, the dependence of synchronization on central states and the relations between the synchronization behaviour of neurons and perception.

Neural synchrony correlates with surface segregation rules.

To analyse an image, the visual system must decompose the scene into its relevant parts. Identifying distinct surfaces is a basic operation in such analysis, and is believed to precede object recognition. Two superimposed gratings moving in different directions (plaid stimuli) may be perceived either as two surfaces, one being transparent and sliding on top of the other (component motion) or as a single pattern whose direction of motion is intermediate to the component vectors (pattern motion). The degree of transparency, and hence the perception, can be manipulated by changing only the luminance of the grating intersections. Here we show that neurons in two visual cortical areas—A18 and PMLS—synchronize their discharges when responding to contours of the same surface but not when responding to contours belonging to different surfaces. The amplitudes of responses correspond to previously described rate predictions for component and pattern motion, but, in contrast to synchrony, failed to reflect the transition from component to pattern motion induced by manipulating the degree of transparency. Thus, dynamic changes in synchronization could encode, in a context-dependent way, relations among simultaneous responses to spatially superimposed contours and thereby bias their association with distinct surfaces.

A new look at gamma? High- (>60 Hz) γ-band activity in cortical networks: Function, mechanisms and impairment

γ-band oscillations are thought to play a crucial role in information processing in cortical networks. In addition to oscillatory activity between 30 and 60 Hz, current evidence from electro- and magnetoencephalography (EEG/MEG) and local-field potentials (LFPs) has consistently shown oscillations >60 Hz (high γ-band) whose function and generating mechanisms are unclear. In the present paper, we summarize data that highlights the importance of high γ-band activity for cortical computations through establishing correlations between the modulation of oscillations in the 60-200 Hz frequency and specific cognitive functions. Moreover, we will suggest that high γ-band activity is impaired in neuropsychiatric disorders, such as schizophrenia and epilepsy. In the final part of the paper, we will review physiological mechanisms underlying the generation of high γ-band oscillations and discuss the functional implications of low vs. high γ-band activity patterns in cortical networks.

Gamma-Phase Shifting in Awake Monkey Visual Cortex

Gamma-band synchronization is abundant in nervous systems. Typically, the strength or precision of gamma-band synchronization is studied. However, the precise phase with which individual neurons are synchronized to the gamma-band rhythm might have interesting consequences for their impact on further processing and for spike timing-dependent plasticity. Therefore, we investigated whether the spike times of individual neurons shift systematically in the gamma cycle as a function of the neuronal activation strength. We found that stronger neuronal activation leads to spikes earlier in the gamma cycle, i.e., we observed gamma-phase shifting. Gamma-phase shifting occurred on very rapid timescales. It was particularly pronounced for periods in which gamma-band synchronization was relatively weak and for neurons that were only weakly coupled to the gamma rhythm. We suggest that gamma-phase shifting is brought about by an interplay between overall excitation and gamma-rhythmic synaptic input and has interesting consequences for neuronal coding, competition, and plasticity.

Activity patterns in human motion-sensitive areas depend on the interpretation of global motion

Numerous imaging studies have contributed to the localization of motion-sensitive areas in the human brain. It is, however, still unclear how these areas contribute to global motion perception. Here, we investigate with functional MRI whether the motion-sensitive area hMT+/V5 is involved in perceptual segmentation and integration of motion signals. Stimuli were overlapping moving gratings that can be perceived either as two independently moving, transparent surfaces or as a single surface moving in an intermediate direction. We examined whether motion-sensitive area hMT+/V5 is involved in mediating the switches between the two percepts. The data show differential activation of hMT+/V5 with perceptual switches, suggesting that these are associated with a reconfiguration of cell assemblies in this area.

Synchronous oscillations in the cat retina

Retinal ganglion cells exhibit oscillatory responses which are precisely synchronized over large distances. Here we examined, with multi-electrode recordings, the time course of synchronization during spontaneous and stimulus-driven oscillatory activity. Spontaneous discharges showed synchronized oscillations at approximately 30 Hz, which were occasionally associated with slower superimposed oscillations in the range of 1-5 Hz. Stationary stimuli or moving gratings induced synchronous oscillations at higher frequencies (mean of 79.0 +/- 20.0 Hz for OFF- and 91.7 +/- 11.7 Hz for ON-responses), with time lags of a few milliseconds. At response onset, the first few oscillatory cycles were occasionally time locked to the stimulus. Thereafter, synchronization became independent of stimulus coordination and was exclusively due to neuronal interactions. Oscillatory modulation emerged rapidly and was sustained throughout the responses while oscillation frequency decreased gradually. This periodic patterning of responses persisted despite brief and local occlusion of stimuli, suggesting that synchronous oscillations emerge from population dynamics and entrain cells even if they are intermittently silenced.

Extraction of Network Topology From Multi-Electrode Recordings: Is there a Small-World Effect?

The simultaneous recording of the activity of many neurons poses challenges for multivariate data analysis. Here, we propose a general scheme of reconstruction of the functional network from spike train recordings. Effective, causal interactions are estimated by fitting generalized linear models on the neural responses, incorporating effects of the neurons’ self-history, of input from other neurons in the recorded network and of modulation by an external stimulus. The coupling terms arising from synaptic input can be transformed by thresholding into a binary connectivity matrix which is directed. Each link between two neurons represents a causal influence from one neuron to the other, given the observation of all other neurons from the population. The resulting graph is analyzed with respect to small-world and scale-free properties using quantitative measures for directed networks. Such graph-theoretic analyses have been performed on many complex dynamic networks, including the connectivity structure between different brain areas. Only few studies have attempted to look at the structure of cortical neural networks on the level of individual neurons. Here, using multi-electrode recordings from the visual system of the awake monkey, we find that cortical networks lack scale-free behavior, but show a small, but significant small-world structure. Assuming a simple distance-dependent probabilistic wiring between neurons, we find that this connectivity structure can account for all of the networks’ observed small-world ness. Moreover, for multi-electrode recordings the sampling of neurons is not uniform across the population. We show that the small-world-ness obtained by such a localized sub-sampling overestimates the strength of the true small-world structure of the network. This bias is likely to be present in all previous experiments based on multi-electrode recordings.

Brightness Induction: Rate Enhancement and Neuronal Synchronization as Complementary Codes

In cat visual cortex, we investigated with parallel recordings from multiple units the neuronal correlates of perceived brightness. The perceived brightness of a center grating was changed by varying the orientation or the relative spatial phase of a surrounding grating. Brightness enhancement by orientation contrast is associated with an increase of discharge rates of responses to the center grating but not with changes in spike synchronization. In contrast, if brightness enhancement is induced by phase offset, discharge rates are unchanged but synchronization increases between neurons responding to the center grating. The changes in synchronization correlate well with changes in perceived brightness that were assessed in parallel in human subjects using the same stimuli. These results indicate that in cerebral cortex the modulation of synchronicity of responses is used as a mechanism complementary to rate changes to enhance the saliency of neuronal responses.