In this paper we examined the initial responses of LIP neurons to flashed stimuli. Most neurons with visual activity had a rapid, precisely timed on-response that was often followed by a brief period of inactivity. These data show that LIP receives a temporally precise message signaling the onset of a new stimulus; this information could be used to direct attention rapidly toward the new stimulus.
Latencies for the ring stimuli ranged from 34 to 60 msec (mean, 41.4 msec) and increased to 42–76 msec (mean, 49.5 msec) when the target was presented in the RF. These latencies are generally shorter than those reported originally for the posterior parietal cortex as a whole (Bushnell et al., 1981
) or for LIP (Barash et al., 1991
). There are several possible reasons for this difference, such as stimulus size, contrast, duration, location in RF, bin size (2 msec compared with 20 msec), and the method used to confirm stimulus onset. In addition, it is possible that because we had only two target and four probe locations the animals learned to anticipate the stimulus onsets, and the resultant “expectancy” shortened latency. However, this is very unlikely to be the case, for several reasons. First, the stimulus timings and locations were randomized from trial to trial. Second, on some trials no target or distractor appeared in the RF. In these trials we found no response at the time that the target or distractor might have been expected to appear in RF (J.W. Bisley and M.E. Goldberg, unpublished observations). Finally, the latencies to the probe and distractor at the locus of attention (where the monkey was presumably expecting the stimulus) were no different from the latencies to these stimuli elsewhere.
Bair et al. (2002)
have shown onset latencies ranging from 30 to 50 msec in area MT, an area receiving information directly from V1 and projecting to LIP. The middle superior temporal (MST) area is another direct recipient of MT projections (like LIP), and Kawano et al. (1994)
found that MST latencies range from 37 to 86 msec, with a mean of 47.1 msec. The range and distribution of these data are very similar to those shown in . Thus, the latencies measured in the current study are consistent with previous results and highlight the speed with which information can pass through the visual system.
We show here that prior attention allocation has no effect on the magnitude or latency of the initial burst. Attention factors similarly have no effect on the onset response in lower areas, such as MT, V2, and V4 (Treue, 2001
). The only substantial factor found to affect latency was stimulus type: latencies to the rings were shorter than latencies to the probes, which were in turn shorter than latencies to the target or distractor. Such differences related to stimulus characteristics could simply mirror similar differences observed in the input areas (Reich et al., 2001
). In most neurons the response to the task-irrelevant distractor was characterized by an initial burst followed by a brief pause in activity, and then often followed by a more sustained visual response. It was only this later activity that was affected by prior attention allocation. The lack of influence of attention factors on latency and response magnitude, combined with the fact that the latencies are extremely short and only slightly longer than those in area MT, strongly suggests that the initial burst is a pure visual response that travels quickly through the visual system. We speculate that it arises from input through a rapid V1–MT–LIP connection (Andersen et al., 1990
) in the magnocellular pathway.
Although the actual function of LIP is still a matter of dispute (Dickinson et al., 2003
), most studies agree that it has a complicated, cognitive function that transcends simple visual analysis (Andersen and Buneo, 2003
; Bisley and Goldberg, 2003b
). The activity of neurons in LIP has been related to decision making (Roitman and Shadlen, 2002
), reward value (Platt and Glimcher, 1999
), time keeping (Leon and Shadlen, 2003
), saccade planning (Snyder et al., 1998
), and salience (Gottlieb et al., 1998
). We found that only the later sustained visual activity, emerging ~40–50 msec after the beginning of the response, reflects these more cognitive functions. The pause in visual activity between the onset burst and the later sustained visual response could represent a period during which the purely sensory response that travels quickly through the visual system has ended, but the longer latency visual response that is subject to cognitive modulation has not yet occurred. It is also possible that the pause represents a period of inhibition brought about by neighboring LIP neurons; however, the lack of a clear relationship between the initial visual response and the presence or absence of inactivity suggests that this may not be the case.
In addition to the short latencies, we found that most neurons had little variation in latency across trials. This, coupled with high firing rates during the burst, produced highly reproducible first spike times. These responses were as precise as those seen to stimulus changes in the LGN (Reinagel and Reid, 2000
) and in area MT (Buracas et al., 1998
); adding to the growing body of literature indicating that timing precision is not diminished at successive stages of visual processing. A coincidence detector could look at the precisely timed burst of activity from these neurons and detect the timing of stimulus onset with high precision (Lisman, 1997
). If the activity across LIP is used to allocate attention, this would allow a quick and reliable orienting of attention to suddenly appearing stimuli, a trait that would be evolutionarily advantageous.