Laminar differences in gamma and alpha coherence in the ventral stream

Abstract

Attention to a stimulus enhances both neuronal responses and gamma frequency synchrony in visual area V4, both of which should increase the impact of attended information on downstream neurons. To determine whether gamma synchrony is common throughout the ventral stream, we recorded from neurons in the superficial and deep layers of V1, V2, and V4 in two rhesus monkeys. We found an unexpected striking difference in gamma synchrony in the superficial vs. deep layers. In all three areas, spike-field coherence in the gamma (40-60 Hz) frequency range was largely confined to the superficial layers, whereas the deep layers showed maximal coherence at low frequencies (6-16 Hz), which included the alpha range. In the superficial layers of V2 and V4, gamma synchrony was enhanced by attention, whereas in the deep layers, alpha synchrony was reduced by attention. Unlike these major differences in synchrony, attentional effects on firing rates and noise correlation did not differ substantially between the superficial and deep layers. The results suggest that synchrony plays very different roles in feedback and feedforward projections.

Fig. 1.

Attentional modulation of SFC in areas V1, V2, and V4. (A) On alternating blocks of trials, monkeys were cued to attend to a moving grating either inside (top) or outside (bottom) of the recorded neuron's RF. Red traces represent SFC in each area, with attention directed INTO the neuron's RF. Blue traces represent SFC with attention directed OUT of the RF. The magnitude of coherence as a function of frequency is shown for superficial recordings (B–D) and deep recordings (E–G) for areas V1 (B and E), V2 (C and E), and V4 (E and G). Shaded areas represent SEM.

Fig. 2.

Laminar effects in area V4. (A) Distribution of coherence in gamma- and alpha-bands for superficial and deep recordings in area V4. Superficial layer recordings (red) demonstrated stronger gamma-band coherence, whereas deep layer recordings (blue) demonstrated stronger alpha-band coherence. (B) Attentional effects across superficial and deep layer recordings in area V4. Contrast indices (In − Out/In + Out) of the effects of attention were calculated for several measures. Superficial recordings are shown in black, and deep recordings are shown in gray. *P < 0.05; **P < 0.01. All comparisons are sign tests, relative to zero.