Orientation selectivity and noise correlation in awake monkey area V1 are modulated by the gamma cycle

Abstract

Gamma-band synchronization adjusts the timing of excitatory and inhibitory inputs to a neuron. Neurons in the visual cortex are selective for stimulus orientation because of dynamic interactions between excitatory and inhibitory inputs. We hypothesized that these interactions and hence also orientation selectivity vary during the gamma cycle. We determined for each spike its phase relative to the gamma cycle. As a function of gamma phase, we then determined spike rates and their orientation selectivity. Orientation selectivity was modulated by gamma phase. The firing rate of spiking activity that occurred close to a neuron's mean gamma phase of firing was most orientation selective. This stimulus-selective signal could best be conveyed to postsynaptic neurons if it were not corrupted by noise correlations. Noise correlations between firing rates were modulated by gamma phase such that they were not statistically detectable for the spiking activity occurring close to a neuron's mean gamma phase of firing. Thus, gamma-band synchronization produces spiking activity that carries maximal stimulus selectivity and minimal noise correlation in its firing rate, and at the same time synchronizes this spiking activity for maximal impact on postsynaptic targets.

Fig. 1.

Example of gamma phase-dependent orientation selectivity based on equal-width phase bins, and phase bins with equal number of spikes. (A) Spike probability (y axis) as a function of the phase of the LFP (x axis, 0 = mean phase). (B) Bars show the equally wide and nonoverlapping phase bins. Average spike rate (y axis) across stimulus orientations (x axis) for each phase bin (in different panels). The dashed horizontal line denotes the average spike rate across orientations. The panels show that orientation tuning becomes apparent only for spike distributions around the mean phase. (C) OSI [1 − circular variance] (y axis) for phase-dependent spike counts across phase bins (x axis). The color of the rectangle in each panel denotes the phase bin from Fig. 1B from which the phase-dependent spike counts were used to compute the OSI. (D and E) Same format and example neuron as in B and C, but now for phase bins containing identical number of spikes. The color of the rectangle in each panel denotes the phase bin from Fig. 1D from which the phase-dependent spike counts were used to compute the OSI.

Fig. 2.

Population results for gamma phase-dependent orientation selectivity. (A and B) Normalized OSI for phase-dependent spike counts for each phase-binning type. OSI was normalized by subtracting the minimum OSI across phase bins for each cell separately, before group averaging. The x axes denote the phase bin center. Arrows indicate the mean phase bin. For the binning with equal bin widths and equal spike counts per bin, the x axis replicates the gamma cycle twice to illustrate the cyclic modulation. For all panels, error bars denote SEM. (C) Proportion of spikes across phase bins with the two types of phase binning illustrated in A and B. Dashed line shows the 12.5% level reflecting equal distribution of spikes across phase bins. (D) Across-cell distribution of gamma phases at which orientation selectivity was estimated to be highest.

Fig. 3.

Frequency specificity of gamma phase-dependent orientation selectivity. Modulation of phase bin-dependent changes of OSI (y axis) across frequencies (x axis) for the binning, ensuring equal spike counts per bin (Fig. 2B). Modulation depth indexes the peak-to-trough modulation depth of a cosine fit to the OSI across phase bins per frequency. Gray bars on top of each graph highlight frequencies with statistically significant phase bin-dependent tuning (see Methods for details).

Fig. 4.

Relationship spike-LFP phase locking and orientation selectivity. Raw OSI values (y axis) as function of Z-score–transformed PPC values. Every dot represents a cell.

Fig. 5.

Gamma phase modulates noise correlation. (A) Noise correlation (y axis) as a function of gamma phase (x axis) at which the spikes occurred relative to the LFP. Zero denotes the mean phase. Phase bins contained an equal number of spikes (Fig. 2C). (B) Proportional change in noise correlation relative to the mean phase bin (y axis) as a function of the distance of the bin centers to the mean phase. *P < 0.05; **P < 0.01; error bars show SEM.