The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex

Abstract

When images are stabilized on the retina, visual perception fades. During voluntary visual fixation, however, constantly occurring small eye movements, including microsaccades, prevent this fading. We previously showed that microsaccades generated bursty firing in the primary visual cortex (area V-1) in the presence of stationary stimuli. Here we examine the neural activity generated by microsaccades in the lateral geniculate nucleus (LGN), and in the area V-1 of the awake monkey, for various functionally relevant stimulus parameters. During visual fixation, microsaccades drove LGN neurons by moving their receptive fields across a stationary stimulus, offering a likely explanation of how microsaccades block fading during normal fixation. Bursts of spikes in the LGN and area V-1 were associated more closely than lone spikes with preceding microsaccades, suggesting that bursts are more reliable than are lone spikes as neural signals for visibility. In area V-1, microsaccade-generated activity, and the number of spikes per burst, was maximal when the bar stimulus centered over a receptive field matched the cell's optimal orientation. This suggested burst size as a neural code for stimuli optimality (and not solely stimuli visibility). As expected, burst size did not vary with stimulus orientation in the LGN. To address the effectiveness of microsaccades in generating neural activity, we compared activity correlated with microsaccades to activity correlated with flashing bars. Onset responses to flashes were about 7 times larger than the responses to the same stimulus moved across the cells' receptive fields by microsaccades, perhaps because of the relative abruptness of flashes.

Figure 1

Comparison between microsaccades and flashes. (A) Microsaccades increase spike probabilities in the presence of a stationary bar in the LGN (thick pink trace; n = 57 neurons) and area V-1 (thick black trace; n = 308 neurons). The correlation between microsaccades and spikes disappears in the absence of visual stimulation in the LGN (thin pink trace; n = 42 neurons) and V-1 (thin gray trace; n = 37 neurons). Microsaccades increase spike probabilities in the LGN (thick purple trace; n = 48 neurons) and area V-1 (thick gray trace; n = 6 neurons) when a flashing bar is on. Starts of all microsaccades are aligned at the vertical line. (B) The probability of a spike after a flashing bar turns on is ≈7 times higher than the probability of a spike after a microsaccade when that same flashing bar is on. The same data set from A (LGN and V-1: purple and black traces) have been replotted and realigned to the flashing bar onset (vertical line).

Figure 2

Probability of microsaccades before bursts of different sizes (1–8 spikes per burst). Surface plots and the corresponding contour plots are presented for each burst size. (A) Probability of microsaccades before bursts, in the presence of an optimally oriented bar, for a single V-1 cell. (B) Same V-1 cell as in A, with orthogonal bar. Greenish flat planes for burst sizes 3–8 indicate absence of those burst sizes. (C) Microsaccade probabilities for a single LGN cell in the presence of a vertical bar. (D) Same LGN cell as C, with a horizontal bar. ISI, 1–100 ms; latency, time between the first spike in the burst and the previous microsaccade (1–200 ms).

Figure 3

(A) Average probability of spikes after microsaccades in V-1, for optimal (red) and orthogonal (blue) orientations (n = 11; each cell was tested in both the optimal and orthogonal conditions). (B) Average probability of spikes after microsaccades in the LGN, for horizontal (red) and vertical (blue) orientations (n = 20; each neuron was tested for both orientations). (C and D) Distribution of peak probabilities of previous microsaccades before bursts of all sizes tested. Optimal latencies and ISIs were selected for each individual neuron. (C) V-1 population with optimally (red) and orthogonally (blue) oriented bars (same neurons as in A). (D) LGN population with horizontal (red) and vertical (blue) bars (same neurons as in B). (Insets in C and D) Average probability of a microsaccade before all burst sizes, for the two different orientations tested. Error bars in C and D indicate the SEM.