Where and when to pay attention: the neural systems for directing attention to spatial locations and to time intervals as revealed by both PET and fMRI

Abstract

Although attention is distributed across time as well as space, the temporal allocation of attention has been less well researched than its spatial counterpart. A temporal analog of the covert spatial orientation task [Posner MI, Snyder CRR, Davidson BJ (1980) Attention and the detection of signals. J Exp Psychol Gen 109:160-174] was developed to compare the neural systems involved in directing attention to spatial locations versus time intervals. We asked whether there exists a general system for allocating attentional resources, independent of stimulus dimension, or whether functionally specialized brain regions are recruited for directing attention toward spatial versus temporal aspects of the environment. We measured brain activity in seven healthy volunteers by using positron emission tomography (PET) and in eight healthy volunteers by using functional magnetic resonance imaging (fMRI). The task manipulated cued attention to spatial locations (S) and temporal intervals (T) in a factorial design. Symbolic central cues oriented subjects toward S only (left or right), toward T only (300 msec or 1500 msec), toward both S and T simultaneously, or provided no information regarding S or T. Subjects also were scanned during a resting baseline condition. Behavioral data showed benefits and costs for performance during temporal attention similar to those established for spatial attention. Brain-imaging data revealed a partial overlap between neural systems involved in the performance of spatial versus temporal orientation of attention tasks. Additionally, hemispheric asymmetries revealed preferential right and left parietal activation for spatial and temporal attention, respectively. Parietal cortex was activated bilaterally by attending to both dimensions simultaneously. This is the first direct comparison of the neural correlates of attending to spatial versus temporal cues.

Fig. 1.

a, Attentional cues used to direct subjects’ attention to a particular target location or stimulus-onset time. The neutral cue provides neither spatial nor temporal information, the spatial (Space) cue directs the subjects’ attention to the left or right, the temporal (Time) cue directs attention to a short or long stimulus-onset time, and the spatiotemporal (Space–Time) cue directs attention to both location and stimulus-onset time. b, A typical trial, which in this example directs the subjects’ attention to a long stimulus-onset time, with no information about the target’s location. The attentional cue is on for 100 msec, the cue-target interval is either 300 or 1500 msec (short/long cue), and finally the target appears for 50 msec in either the left or right box.

Fig. 2.

Areas commonly activated by spatial and temporal orienting of attention, as measured by PET. Activations arenumbered according to Table 3.

Fig. 3.

A, Areas preferentially activated by (a) spatial orienting, (b) temporal orienting, and (c) spatiotemporal orienting of attention, as measured by PET. B, Anatomical localization of the preferential activation of (a) the right intraparietal sulcus by spatial orienting (S), (b) the left intraparietal sulcus by temporal orienting (T), and (c) the bilateral intraparietal sulcus by spatiotemporal orienting (ST), as measured by fMRI. Coronal slices from three separate individuals (S1, S2,S3) are shown for each condition. The left side of the figure corresponds to the left side of the brain.