Temporal sequence of attentional modulation in the lateral intraparietal area and middle temporal area during rapid covert shifts of attention

Abstract

In the visual system, spatial attention enhances sensory responses to stimuli at attended locations relative to unattended locations. Which brain structures direct the locus of attention, and how is attentional modulation delivered to structures in the visual system? We trained monkeys on an attention-switch task designed to precisely measure the onset of attentional modulation during rapid shifts of spatial attention. Here we show that attentional modulation appears substantially earlier in the lateral intraparietal area (LIP) than in an anatomically connected lower visual area, the middle temporal area. This temporal sequence of attentional latencies demonstrates that endogenous changes of state can occur in higher visual areas before lower visual areas and satisfies a critical prediction of the hypothesis that LIP is a source of top-down attentional signals to early visual cortex.

Figure 1.

Task design and behavior. A, Attention-switch task. Trials began with the appearance of a fixation point and two peripheral annuli. After fixation, 100% coherent moving dots appeared within the annuli. The monkey released a touch bar to indicate detection of a 53-ms-duration speed increase at either dot patch. Matching fixation point and annulus color indicated the likely location of the speed pulse (85% valid cues). On 40% of trials, the fixation-point color switched mid-trial, indicating that the likely speed-pulse location had switched. After a 400 ms fixed delay, speed-pulse times and cue-switch times were chosen from an exponential distribution (mean of 1 s). B–E, Behavior from neural recording sessions. Monkey M (B, D) and monkey B (C, E) exhibited increased detection frequency (B, C) and decreased reaction times (D, E) when speed pulses occurred at the initially cued location (filled symbols, solid lines) relative to the initially uncued location (open symbols, dashed lines). After cue switches, this behavioral pattern reversed. Error bars are 95% confidence intervals for data pooled across all behavioral sessions (generally smaller than the symbols). All valid/invalid differences were statistically significant (p ≪ 0.001, χ² test for fraction detected, t test for reaction time).

Figure 2.

Example single-neuron responses in LIP and MT. Average neural response rates as a function of time are shown for an LIP (A, B) and an MT (C, D) neuron. Both neurons were from monkey M. Left panels (A, C) show activity on non-switch trials aligned on the initial onset of the moving dots. Right panels (B, D) show activity on switch trials aligned on the cue switch. In each plot, activity is shown separately depending on whether attention was cued into or out of the receptive field of the neuron. Data from each trial were used only up until the time of the speed pulse on that trial.

Figure 3.

Population neural activity in LIP and MT. A, B, LIP average population activity on switch trials aligned on the time of the cue switch for monkey M (A) and monkey B (B). Trials in which the initially cued dot patch was in the receptive field (in–out switches, gray) and out of the receptive field (out–in switches, black) are plotted separately. The sign of the attentional modulation switched shortly after a cue switch. C, D, MT average population activity on switch trials aligned on the time of the cue switch for monkey M (C) and monkey B (D).

Figure 4.

Attentional modulation arises earlier in LIP than MT. LIP data are in gray and MT data are in black for monkey M (A) and monkey B (B). For each neuron, attentional modulation was quantified as an attentional index equal to (R _IN − R _OUT)/(R _IN + R _OUT), where R _IN and R _OUT are the average neural response in spikes per second when attention is directed in or out of the receptive field, respectively (see Materials and Methods). Neural responses from all individual single units with preswitch or postswitch attentional indices >0.03 are plotted (number of cells included: monkey M, MT, 33 of 36; LIP, 49 of 55; monkey B, MT, 19 of 31; LIP, 51 of 63). Responses were aligned vertically by calculating the average spike rate for each neuron from 150 ms before to 50 ms after the cue switch and then subtracting this preswitch activity from each response.

Figure 5.

Single-neuron attentional latencies. LIP data are in gray, and MT data are in black. A–D, Peri-cue-switch spike-rate functions for monkey M out–in switches (A), monkey B out–in switches (B), monkey M in–out switches (C), and monkey B in–out switches (D). Spike-rate functions are aligned vertically to have overlapping spike rates from 0 to 50 ms after the cue switch (A, B, D) or from 0 to 150 ms (C) after the cue switch but are not otherwise scaled. E–M, Cumulative probability distributions for single-neuron attentional latencies. Single-neuron latencies could not be determined for monkey B in–out switches because of the postcue dip in activity. Latencies were determined using deviation-threshold (E–G), spike-rate-threshold (H–J), and slope-threshold (K–M) methods. Inset values are the difference of population medians (ΔM) between the LIP and MT distributions and a p value from a Wilcoxon's rank-sum test for the null hypothesis of no difference between the distributions.

Figure 6.

Neuron-elimination analyses. LIP data are in gray, and MT data are in black. Monkey M (A, C) and monkey B (B, D). A, B, Magnitude of attentional modulation was defined as the difference in spike rate between a postswitch (400 to 800 ms) and preswitch (−400 to 0 ms) time window. Using only cells with preswitch or postswitch attentional indices >0.03, we progressively threw away the LIP neurons with the largest attentional modulation until the magnitude was matched in the two populations. Number of cells thus included the following: monkey M: MT, 33 of 36; LIP, 37 of 55; monkey B: MT, 19 of 31; LIP, 22 of 63. C, D, Elimination of all cells with periswitch dips >2 spikes/s in magnitude. Magnitude of the dip was defined as the difference between the peak of the LIP dip period in monkey B (125–175 ms after switch) and baseline (0–50 ms after switch). Number of cells included the following: monkey M: MT, 21 of 36; LIP, 40 of 55; monkey B: MT, 12 of 31; LIP, 24 of 63.

Figure 7.

Elimination of trials with microsaccades. Periswitch activity on out–in trials for LIP and MT populations for all trials (solid lines) and after elimination of trials with microsaccades within 500 ms after a cue switch (dashed lines), for monkey M (A) and monkey B (B). Elimination of trials with microsaccades did not alter the average attentional latency in either area.