Laminar analysis of visually evoked activity in the primary visual cortex

Abstract

Studying the laminar pattern of neural activity is crucial for understanding the processing of neural signals in the cerebral cortex. We measured neural population activity [multiunit spike activity (MUA) and local field potential, LFP] in Macaque primary visual cortex (V1) in response to drifting grating stimuli. Sustained visually driven MUA was at an approximately constant level across cortical depth in V1. However, sustained, visually driven, local field potential power, which was concentrated in the γ-band (20-60 Hz), was greatest at the cortical depth corresponding to cortico-cortical output layers 2, 3, and 4B. γ-band power also tends to be more sustained in the output layers. Overall, cortico-cortical output layers accounted for 67% of total γ-band activity in V1, whereas 56% of total spikes evoked by drifting gratings were from layers 2, 3, and 4B. The high-resolution layer specificity of γ-band power, the laminar distribution of MUA and γ-band activity, and their dynamics imply that neural activity in V1 is generated by laminar-specific mechanisms. In particular, visual responses of MUA and γ-band activity in cortico-cortical output layers 2, 3, and 4B seem to be strongly influenced by laminar-specific recurrent circuitry and/or feedback.

Fig. 1.

Population activity measured in V1. (A) Multiunit activity (MUA) to the drifting grating stimulus. The MUA averaged from 300 to 2,000 ms after stimulus onset was taken to be the steady-state MUA. The MUA response over the first 200 ms after stimulus onset was termed the MUA transient response. (B) Absolute spectrogram of the LFPs to the drifting grating stimulus is coded by color. Between 20 and 60 Hz (marked by two horizontal dashed lines), there is sustained power after stimulus onset (marked by the first vertical dashed line). (C) The raw power spectrum was converted into the relative power spectrum by normalizing by the power during the blank period at each frequency (Inset). (D) Sustained power spectrum of the LFP to the drifting grating stimulus. We defined the average power in the LFP from 300 to 2,000 ms after stimulus onset as the sustained power spectrum. (E) Dynamics of γ-power. We defined the power between 20 and 60 Hz at each time as the instantaneous γ-power.

Fig. 2.

Laminar pattern of MUA dynamics in V1. (A) Dynamics of MUA plotted as a function of cortical depth; x axis represents the time after stimulus onset, and colors represent the MUA. Horizontal dashed lines define the borders of V1 cortical laminae. (B) Running averages of the sustained (red-shaded curve) and transient (blue-shaded curve) MUA. The length of sliding window is 100 μm in cortical space, and the shaded regions represent the SEM. MUA activity is in units of impulses per millisecond. (C) Sustain indices (sustained MUA divided by transient MUA) are plotted as a function of cortical depth. The length of sliding window is 100 μm in cortical space, and the shaded regions represent the SEM. (D) Population-averaged MUA time waveforms are plotted for different cortical layers. The colored shaded regions in D represent the SEM.

Fig. 3.

Laminar pattern of LFP power spectrum in V1. (A) Power spectrum of the LFP plotted as a function of cortical depth; x axis represents the frequencies, and colors represent the power at each frequency. Horizontal dashed lines define the borders of different cortical layers in V1. Two vertical lines mark 20 and 60 Hz. Power spectrum was the averaged relative power in the period of 300–2,000 ms after stimulus onset. (B) Running average of the peak γ-band in different layers. The length of the sliding window is 100 μm in cortical space, and the gray-shaded region represents the SEM within the corresponding sliding window. (C) Population-averaged power spectra of the LFP are plotted for different cortical layers. The gray-shaded regions in C represent the SEM.

Fig. 4.

Laminar pattern of γ-band dynamics in V1. (A) Dynamics of γ-power plotted as a function of cortical depth; x axis represents the time after stimulus onset, and colors represent the γ-power. Horizontal dashed lines define the borders of V1 cortical laminae. The vertical line marks 300 ms after stimulus onset. (B) Running averages of the sustained (red-shaded curve) and transient (blue-shaded curve) LFP γ-power. The length of sliding window is 100 μm in cortical space, and the shaded regions represent the SEM. (C) Sustain indices (sustained γ-power divided by transient γ-power for the LFP) are plotted as a function of cortical depth. The length of sliding window is 100 μm in cortical space, and the shaded regions represent the SEM. (D) Population-averaged γ-dynamics are plotted for different cortical layers. The shaded regions represent the SEM.

Fig. 5.

Laminar pattern of population activity in V1. (A) Demonstration of the laminar structure of Macaque V1. (B) FAD of sustained spike activity in different layers. (C) FAD of transient spike activity in different layers. (D) FAD of the sustained γ-power in different layers. (E) FAD of the transient γ-power in different layers.