Synchronization in primate cerebellar granule cell layer local field potentials: basic anisotropy and dynamic changes during active expectancy

Abstract

The cerebellar cortex is remarkable for its organizational regularity, out of which task-related neural networks should emerge. In Purkinje cells, both complex and simple spike network patterns are evident in sensorimotor behavior. However, task-related patterns of activity in the granule cell layer (GCL) have been less studied. We recorded local field potential (LFP) activity simultaneously in pairs of GCL sites in monkeys performing an active expectancy (lever-press) task, in passive expectancy, and at rest. LFP sites were selected when they showed strong 10-25 Hz oscillations; pair orientation was in stereotaxic sagittal and coronal (mainly), and diagonal. As shown previously, LFP oscillations at each site were modulated during the lever-press task. Synchronization across LFP pairs showed an evident basic anisotropy at rest: sagittal pairs of LFPs were better synchronized (more than double the cross-correlation coefficients) than coronal pairs, and more than diagonal pairs. On the other hand, this basic anisotropy was modifiable: during the active expectancy condition, where sagittal and coronal orientations were tested, synchronization of LFP pairs would increase just preceding movement, most notably for the coronal pairs. This lateral extension of synchronization was not observed in passive expectancy. The basic pattern of synchronization at rest, favoring sagittal synchrony, thus seemed to adapt in a dynamic fashion, potentially extending laterally to include more cerebellar cortex elements. This dynamic anisotropy in LFP synchronization could underlie GCL network organization in the context of sensorimotor tasks.

Keywords: cerebellar cortex; granule cell layer; network activity; oscillations; sensorimotor; synchronization.

Figure 1

Cerebellar cortex GCL simultaneous LFP recordings at rest, monkey F. (A,B) Simultaneous LFPs recorded sagittally or coronally. Estimated positions of the recording pairs shown, based on reconstruction from electrolytic lesions. Two periods are highlighted, one with low (yellow box) and one with strong (green box) oscillations. (C,F) Fast Fourier Transforms (FFT) for each recording site, for each selected period. (D,E) Cross-correlation for each selected period. Recording sites, field potential and FFT traces are color-matched.

Figure 2

Oscillation and synchronization properties of cerebellar GCL LFPs during rest. (A,B) Relationship between the 10–25 Hz oscillatory content (% of the LFP signal between 10–25 Hz) at both recording sites for a sagittal and a coronal pair in monkey F. Linear correlation value (r), regression line and 95% confidence interval indicated. (C) Averaged cross-correlograms (s.d., gray area) for multiple windows (n = 1250) for a sagittal and a coronal pair in monkey Z. (D) Mean and standard deviation for cross-correlation and concomitance coefficients in relation to both the lateral and the total distances between the two recorded sites for each monkey (K, F, and Z).

Figure 3

Modulation of cerebellar LFP oscillations and synchronization of LFPs in the active condition, for a sagittal pair and a coronal pair. (A,B) Modulation of the 10–25 Hz oscillations across the trial, as shown by the temporal spectral evolution (TSE). Grey area: reward window, vertical line, stimulus onset. Line colors: A. blue-anterior, red-posterior; B. blue-medial, red-lateral. The different delays Ps, Dl1, Dl2, and Dl3 are indicated. (C,D) Cross-correlation coefficients for the same experiments. (E,F) Cross-correlogram for the same experiments (abscissa: time in the trial; ordinate: lag; color: height in the correlogram). Parts A to F: typical results illustrated by data recorded in monkey F. (G,H) Cross-correlation of LFPs in all conditions (active, passive, and rest), for each delay (Ps, Dl1, Dl2, and Dl3), for both monkeys F and K. Means and s.e.m. indicated; *p < 0.05 (Tukey post-hoc) of this value (active condition) vs. other active condition delays, and passive and rest conditions.