What does gamma coherence tell us about inter-regional neural communication?

Abstract

Neural oscillations have been measured and interpreted in multitudinous ways, with a variety of hypothesized functions in physiology, information processing and cognition. Much attention has been paid in recent years to gamma-band (30-100 Hz) oscillations and synchrony, with an increasing interest in 'high gamma' (>100 Hz) signals as mesoscopic measures of inter-regional communication. The biophysical origins of the measured variables are often difficult to precisely identify, however, making their interpretation fraught with pitfalls. Here we discuss how measurements of inter-regional gamma coherence can be prone to misinterpretation and suggest strategies for deciphering the roles that synchronized oscillations across brain networks may play in neural function.

Figure 1

An idealized experimental layout to identify communication by gamma frequency coupling within and across networks. (a) A_DEND and B_DEND recordings designate recordings from the superficial dendritic layers of networks A and B, while A_SOMA and B_SOMA are recording from the deep somatic layers. Tick marks, output action potentials from interneurons (red) and pyramidal cells (blue); lines, LFP traces from electrodes of matching colors. Traces are shown in their respective physical locations on the left and are aligned for easier comparison on the right. In real networks with multiple afferents, high spatial resolution recording techniques from dendritic and somatic layers are needed to obtain interpretable results about the direction of communication. (b) List of signal pairs and the typical coherence measurements found between them.

Figure 2

Fast synaptic patterns delivered to the dendrites may not propagate to the soma. Current injected directly into distal dendrites is low-pass filtered between the input site and the soma. Modified from ref. with permission of Nature Publishing Group.

Figure 3

Dendritic target domains are characterized by gamma coherence. Coherence maps of gamma activity (30–90 Hz) in the hippocampus during exploration. Cell body layers from histological sectioning are overlaid in gray. The 10 seed sites (black dots) served as reference sites, and coherence was calculated between the reference site and the remaining 255 locations recorded by an 8-shank, 256-site silicon probe. LFP-LFP coherence within the same layer is consistently high because the dendritic segments in a given layer receive inputs from a temporally coordinated upstream neuron population. In contrast, gamma coherence across layers is low because upstream populations that target the distinct layers are not necessarily coordinated. The central map does not display coherence but instead indicates groups of electrodes that displayed high coherence with each other, with each group represented by a different (arbitrary) color. Modified from ref. with permission of the American Physiological Society.

Figure 4

The origins of gamma LFP patterns can be revealed with simultaneous multisite recordings of LFP and spiking activity. (a) Multiple gamma patterns in the rat CA1 stratum (str.) pyramidale LFP (top left) are discernible at different frequencies and theta phases during locomotion. High-density silicon electrode arrays spanning multiple layers provide sufficient coverage and spatial resolution to employ independent component analysis to decompose CA1 LFPs into different physiological components. Arrows indicate independent components (ICs) corresponding to currents in str. pyramidale (top right), str. radiatum (bottom left) and str. lacunosum-moleculare (lac.-mol., bottom right) that were at matching frequencies and theta phases to the three gamma sub-bands visible in the str. pyramidale LFP. (b) The fraction of EC3 pyramidal cells (pyr.; red) and interneurons (int.; blue) significantly phase-locked (Rayleigh test P < 0.01) are plotted as a function of frequency for CA1 LFPs. The greatest proportions of EC3 pyramidal cells are locked near 90–100 Hz (arrow). (c) Same as in b, but for CA1 units relative to EC3 LFPs. Few CA1 pyramidal cells (orange) are significantly synchronized with EC3 gamma oscillations, although a larger proportion of CA1 interneurons (cyan) are modulated by slow to medium gamma waves recorded in EC3. Peaks in the phase-locked proportions for both cell types can be seen near 60 Hz (arrows), which is far from the peak locking frequency in the opposite direction (b). Modified from ref. with permission of Elsevier.

Figure 5

Interhemispheric, zero-phase-lag coherence of gamma oscillations. (a) LFPs recorded from the left (L) and right (R) CA1 pyramidal layer of the mouse hippocampus. (b) Co-modulation of theta and gamma power in the two hemispheres. Note that theta power in one hemisphere is co-modulated with gamma power of the other hemisphere (yellow band at 9 Hz and 40–100 Hz, white arrowheads). (c) Spectral power of the LFP from the left hippocampus during wheel running (red) and REM sleep (blue). (d) Coherence spectra between signals derived from the two hippocampi. Note rapidly decreasing coherence in the gamma frequency band (40–100 Hz) and negligible coherence above 100 Hz (high gamma). (e) Phase spectra of the LFP signals derived from the left and right hippocampi. Reproduced from ref. with permission of Elsevier.