Andreas K. Kreiter

Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex

Neurons in area 17 of cat visual cortex display oscillatory responses that can synchronize across spatially separate columns in a stimulus-specific way. Response synchronization has now been shown to occur also between neurons in area 17 of the right and left cerebral hemispheres. This synchronization was abolished by section of the corpus callosum. Thus, the response synchronization is mediated by corticocortical connections. These data are compatible with the hypothesis that temporal synchrony of neuronal discharges serves to bind features within and between the visual hemifields.

Temporal coding in the visual cortex: new vistas on integration in the nervous system

Although our knowledge of the cellular components of the cortex is accumulating rapidly, we are still largely ignorant about how distributed neuronal activity can be integrated to contribute to unified perception and behaviour. In the visual system, it is still unresolved how responses of feature-detecting neurons can be bound into representations of perceptual objects. Recent crosscorrelation studies show that visual cortical neurons synchronize their responses depending on how coherent features are in the visual field. These results support the hypothesis that temporal correlation of neuronal discharges may serve to bind distributed neuronal activity into unique representations. Furthermore, these studies indicate that neuronal responses with an oscillatory temporal structure may be particularly advantageous as carrier signals for such a temporal coding mechanism. Based on these recent findings, it is suggested here that binding of neuronal activity by a temporal code may provide a solution to the problem of integration in distributed neuronal networks.

Oscillatory Neuronal Responses in the Visual Cortex of the Awake Macaque Monkey

An important step in early visual processing is the segmentation of scenes. Features constituting individual objects have to be grouped together and segregated from those of other figures or the background. It has been proposed that this grouping could be achieved by synchronizing the fine temporal structure of responses from neurons excited by an individual figure. In the cat visual cortex evidence has been obtained that responses of feature‐selective neurons have a distinctive oscillatory structure and can synchronize both within and across cortical areas, the synchronization depending on stimulus configuration. Here we investigate the generality of oscillatory responses and their synchronization and specifically whether these phenomena occur in extrastriate areas of the visual cortex of the awake behaving primate. We find in the caudal superior temporal sulcus of the macaque monkey (Macaca fascicularis) that adjacent neurons can synchronize their responses, in which case their discharges exhibit an oscillatory temporal structure. During such periods of local synchrony spatially separated cell groups can also synchronize their responses if activated with a single stimulus. These findings resemble those described previously for the cat visual cortex, except that in the awake monkey the oscillatory episodes tend to be of shorter duration and exhibit more variability of oscillation frequency.

Sustained and transient oscillatory responses in the gamma and beta bands in a visual short-term memory task in humans.

In a visual delayed matching-to-sample task, compared to a control condition, we had previously identified different components of the human EEG that could reflect the rehearsal of an object representation in short-term memory (Tallon-Baudry et al., 1998). These components were induced oscillatory activities in the gamma (24-60 Hz) and beta (15-20 Hz) bands, peaking during the delay at occipital and frontal electrodes, and two negativities in the evoked potentials. Sustained activities (lasting until the end of the delay) are more likely to reflect the continuous rehearsing process in memory than transient (ending before the end of the delay) activities. Nevertheless, since the delay duration we used in our previous experiment was fixed and rather short, it was difficult to discriminate between sustained and transient components. Here we used the same delayed matching-to-sample task, but with variable delay durations. The same oscillatory components in the gamma and beta bands were observed again during the delay. The only components that showed a sustained time course compatible with a memory rehearsing process were the occipital gamma and frontal beta induced activities. These two activities slowly decreased with increasing delay duration, while the performance of the subjects decreased in parallel. No sustained response could be found in the evoked potentials. These results support the hypothesis that objects representations in visual short-term memory consist of oscillating synchronized cell assemblies.

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.

Visually induced gamma-band responses in human electroencephalographic activity- a link to animal studies

Visual presentation of an object produces firing patterns in cell assemblies representing the features of the object. Based on theoretical considerations and animal experiments, it has been suggested that the binding of neuronal representations of the various features is achieved through synchronization of the oscillatory firing patterns. The present study demonstrates that stimulus-induced gamma-band responses can be recorded non-invasively from human subjects attending to a single moving bar. This finding indicates the synchronization of oscillatory activity in a large group of cortical neurons. Gamma-band responses were not as apparent in the presence of two independently moving stimuli, suggesting that the neuronal activity patterns of different objects are not synchronized. These results open a new paradigm for investigating the mechanisms of feature binding and association building in relation to subjective perception.

Testing non-linearity and directedness of interactions between neural groups in the macaque inferotemporal cortex

Information processing in the visual cortex depends on complex and context sensitive patterns of interactions between neuronal groups in many different cortical areas. Methods used to date for disentangling this functional connectivity presuppose either linearity or instantaneous interactions, assumptions that are not necessarily valid. In this paper a general framework that encompasses both linear and non-linear modelling of neurophysiological time series data by means of Local Linear Non-linear Autoregressive models (LLNAR) is described. Within this framework a new test for non-linearity of time series and for non-linearity of directedness of neural interactions based on LLNAR is presented. These tests assess the relative goodness of fit of linear versus non-linear models via the bootstrap technique. Additionally, a generalised definition of Granger causality is presented based on LLNAR that is valid for both linear and non-linear systems. Finally, the use of LLNAR for measuring non-linearity and directional influences is illustrated using artificial data, reference data as well as local field potentials (LFPs) from macaque area TE. LFP data is well described by the linear variant of LLNAR. Models of this sort, including lagged values of the preceding 25 to 60 ms, revealed the existence of both uni- and bi-directional influences between recording sites.

Stimulus dependent intercolumnar synchronization of single unit responses in cat area 17.

Recent concepts of cortical information processing suggest that visual stimuli are represented by ensembles of synchronously firing neurones. This hypothesis predicts that individual cells in separate columns of the visual cortex should synchronize their discharges in response to a single coherent stimulus and fire asynchronously when each neurone responds to a different stimulus. To test this prediction, we recorded simultaneously with two stereotrodes from single units with non-overlapping, colinearly arranged receptive fields in area 17 of the anaesthetized cat. In support of the hypothesis, cell pairs activated by the same long bar stimulus discharged in synchrony, and fired with no or diminished temporal correlation when each neurone was activated by an independent light bar.

Switching Neuronal Inputs by Differential Modulations of Gamma-Band Phase-Coherence

Receptive fields (RFs) of cortical sensory neurons increase in size along consecutive processing stages. When multiple stimuli are present in a large visual RF, a neuron typically responds to an attended stimulus as if only that stimulus were present. However, the mechanism by which a neuron selectively responds to a subset of its inputs while discarding all others is unknown. Here, we show that neurons can switch between subsets of their afferent inputs by highly specific modulations of interareal gamma-band phase-coherence (PC). We measured local field potentials, single- and multi-unit activity in two male macaque monkeys (Macaca mulatta) performing an attention task. Two small stimuli were placed on a screen; the stimuli were driving separate local V1 populations, while both were driving the same local V4 population. In each trial, we cued one of the two stimuli to be attended. We found that gamma-band PC of the local V4 population with multiple subpopulations of its V1 input was differentially modulated. It was high with the input subpopulation representing the attended stimulus, while simultaneously it was very low between the same V4 population and the other input-providing subpopulation representing the irrelevant stimulus. These differential modulations, which depend on stimulus relevance, were also found in the locking of spikes from V4 neurons to the gamma-band oscillations of the V1 input subpopulations. This rapid, highly specific interareal locking provides neurons with a powerful dynamic routing mechanism to select and process only the currently relevant signals.

Rapid contour integration in macaque monkeys

Integration of oriented elements into a contour has been investigated extensively in human psychophysics whereas electrophysiological experiments exploring the neuronal mechanism of contour integration were most often done with macaque monkeys. To bridge the gap between human psychophysics and physiology we estimated spatial and temporal constraints of contour integration in two macaque monkeys. Our results show that contour integration in monkeys depends in a similar way on element distance and alignment between contour path and contour elements as in human subjects. The grouping process was surprisingly fast: In a backward masking experiment we show that a stimulus duration of 30-60 ms is sufficient to perceive a contour and to identify its shape.