Task-related coupling from high- to low-frequency signals among visual cortical areas in human subdural recordings

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Abstract

Cortical cooperativity during cognitive demands includes high- and low-frequency activities, which raises the question whether there are interdependencies between fast and slow processes and how they are reflected in electrical brain signals. We had the opportunity to record signals intracranially from occipital visual areas in an epileptic patient and quantified inter-areal signal coupling while the patient performed a visual delayed-match-to-sample task. We computed coherence, phase consistency and amplitude envelope correlation and we also determined inter-frequency coupling through correlation between low-frequency signal components and amplitude envelopes of high-frequency components. There was a pronounced task-related increase of correlation between gamma-band (28–70 Hz) signal envelopes from a superior (occipital) and low-frequency (0–3.5 Hz) signals from an inferior (occipital) visual area, lasting for approximately 1 s and possibly reflecting a short-term memory encoding process. The correlational delay between envelopes and low-frequency components was 40 ms. In contrast, coherence, phase consistency and envelope correlation showed event-, but no task-related changes of intra-areal and no changes of inter-areal coupling. Our data suggest a specific effect of gamma-activity in the superior onto low-frequency activity in the inferior area. We argue that temporal dispersion of conduction delays might prevent coherent transmission of high-frequency signals and thus account for the absence of gamma-coherence. As such dispersion is a general property of long-range projections, envelope-to-signal correlation possibly reflects a general neuronal mechanism. Hence, our method provides a powerful tool for detecting such inter-areal interactions not visible with conventional linear coupling measures.

Introduction

For understanding the principles of cognitive processing in the brain, it is crucial to gain knowledge of the neuronal mechanisms of cortico–cortical interactions. Enhanced gamma-range (30–70 Hz) activity in intracranial, in scalp EEG and in MEG recordings is a candidate broadly discussed as reflecting neuronal processes of cognitive relevance (reviews, e.g. Basar-Eroglu et al., 1996, Sauvé, 1999, Singer, 1999, Tallon-Baudry and Bertrand, 1999, Eckhorn, 2000, Müller et al., 2000, Karakas et al., 2001). Investigation of perception- or task-related coupling between signals in the gamma-range has, therefore, been pursued in many studies, and in fact, several cases of this type of coupling have been reported so far (e.g. Lachaux et al., 1999, Miltner et al., 1999, Rodriguez et al., 1999, Haig et al., 2000, Klemm et al., 2000). Especially in intracranial recordings, however, coupling among gamma-signals has often been found to be restricted to a spatial range between a few millimeters and approximately 1 cm and to drop to noise levels across larger distances (Bullock et al., 1995, Menon et al., 1996, Steriade et al., 1996, Jürgens et al., 1996, Gross and Gotman, 1999, Frien and Eckhorn, 2000), at least when using conventional linear coupling measures like cross-correlation or spectral coherence. We have, therefore, previously proposed amplitude-envelope correlation as one alternative measure that can detect coupling between gamma-amplitude modulations despite the absence of coherence (Bruns et al., 2000). Apart from this, however, it has been proposed that high-frequency population signals are mainly associated with more local processes, whereas long-range interactions are mediated by low-frequency signals (Schanze and Eckhorn, 1997, von Stein and Sarnthein, 2000). The reason for a limited signal coupling range at high frequencies might be that different axon diameters and thus conduction velocities within a population of projection fibres might lead to an increasing temporal dispersion with increasing cortical distance, so that coherent long-range signal transmission is limited to lower frequencies. Therefore, given that local and global processes manifest themselves through high- and low-frequency signals, respectively, global interaction of local processes should cause interdependence and hence some kind of coupling between high- and low-frequency signals, instances of which have increasingly often been reported recently (Bullock et al., 1997, Schanze and Eckhorn, 1997, von Stein et al., 2000, Schack et al., 2002). We found a special form of such inter-frequency interaction, namely the correlation between low-frequency signal components and amplitude envelopes of high-frequency signal components, between non-phase-coupled patches in the visual cortex of awake monkeys (Bruns et al., 2001). We, therefore, wondered whether this coupling type might more generally occur across larger distances between sites not showing coherent activities. Hence, in the present study we applied this coupling measure to human subdural recordings from different visual areas, apart from quantifying coupling between identical frequencies by means of coherence, phase consistency and amplitude envelope correlation.

For studying interactions between cortical areas, it would be most desirable to have both the high spatial resolution of intracortical microelectrodes and the complete spatial coverage attainable with scalp EEG recordings. Subdurally implanted electrode grids constitute an interesting compromise between these extremes. On the one hand, as they are in direct contact with the cortical surface, their spatial integration profile drops off much faster than for scalp electrodes, which leads to a higher spatial resolution with integration areas in the order of 1 cm2 (scalp integration areas: ≥10 cm2). On the other hand, unlike most microelectrode arrays, subdural grids often contain tens of contacts at regular spacing and typically cover regions comprising two or more cortical areas. In addition, muscle or eyeblink artifacts are negligible in subdural as opposed to scalp recordings. For addressing the question of inter-areal coupling mechanisms, we, therefore, investigated intracranial recordings obtained from epileptic patients with subdural electrodes implanted for clinical diagnostics.

We used a visual delayed-match-to-sample paradigm with different tasks designed to differentially activate the ventral and dorsal visual subsystems, respectively, (e.g. Ungerleider and Mishkin, 1982, Haxby et al., 1991). The aim of the experiment was not to provide support for any of the current concepts concerning the putative roles of the visual pathways. We rather wanted to achieve a functional dissociation that would allow us to distinguish cognitive processes associated with a certain short-term memory task from stimulus-driven cortical responses. Part of this work has been presented previously in abstract form (Bruns et al., 2001).

Section snippets

Subjects

Subdural recordings were obtained from epileptic patients undergoing presurgical evaluation in the Bethel Epilepsy Surgery Program (Bielefeld, Germany). In order to study cortico–cortical interactions between visual areas, we needed subjects with electrodes situated over at least two different visual areas. For identifying such candidates, we used the results of electrical cortical stimulation, which is routinely carried out by neurologists during clinical diagnostics. One out of seven

Psychophysical measures

Of the seven subjects investigated, one perfectly met the demands for the present study. The total performance of this subject in the two sessions was 96% in the figure task, 81% in the spatial task, and 98% in the control task. The total numbers of trials thus included in the analysis were 77, 73 and 75, respectively. Reaction times were 1129±216 ms (figure), 1751±430 ms (spatial), and 1598±234 ms (control) (medians±mean absolute deviations). (Reaction times in the control task resulted from

Discussion

The most important finding of the presented work is the pronounced task-related increase of correlation between envelopes of gamma-signals from an early visual area and low-frequency signals from a higher visual area. The increase occurred at the end of the first stimulus presentation in the figure task, lasted for approximately 1 s and was maximal at a correlational delay of 40 ms between gamma-envelopes and low-frequency signals. It was not visible with common linear correlation measures like

Conclusion

We presented a case of highly specific and significant inter-areal correlation between gamma-envelopes and low-frequency signals. Cortico–cortical interaction here was much more determined by specific signal transmission between distant recording sites than by spatial neighborhood. The interaction was directed from a lower to a higher visual area, it was cognitively relevant and possibly gated by some top-down process playing a role in short-term memory encoding. Envelope-to-signal correlation

Acknowledgements

We thank Dr Hennric Jokeit and Dr Alois Ebner for their cooperation and organizational help at the Bethel Epilepsy Center. We also thank the Bethel Epilepsy Center EEG staff, especially Ralf Dernbach, for technical assistance in recording the subdural signals. This work was supported by DFG grant EC 53/9-3 given to R.E.

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