Extensive clinical and imaging research has characterized the neural networks mediating the adaptive distribution of spatial attention. In everyday behavior, the distribution of attention is guided not only by extrapersonal targets but also by mental representations of their spatial layout. We used eventrelated functional magnetic resonance imaging to identify the neural system involved in directing attention to locations in arrays held as mental representations, and to compare it with the system for directing spatial attention to locations in the external world. We found that these two crucial aspects of spatial cognition are subserved by extensively overlapping networks. However, we also found that a region of right parietal cortex selectively participated in orienting attention to the extrapersonal space, whereas several frontal lobe regions selectively participated in orienting attention within on-line mental representations.

Event-related functional magnetic resonance imaging was used to identify brain areas involved in spatial attention and determine whether these operate unimodally or supramodally for vision and touch. On a trial-by-trial basis, a symbolic auditory cue indicated the most likely side for the subsequent target, thus directing covert attention to one side. A subsequent target appeared in vision or touch on the cued or uncued side. Invalidly cued trials (as compared with valid trials) activated the temporo-parietal junction and regions of inferior frontal cortex, regardless of target modality. These brain areas have been associated with multimodal spatial coding in physiological studies of the monkey brain and were linked to a change in the location that must be attended to in the present study. The intraparietal sulcus and superior frontal cortex were also activated in our task, again, regardless of target modality, but did not show any specificity for invalidly cued trials. These results identify a supramodal network for spatial attention and reveal differential activity for inferior circuits involving the temporo-parietal junction and inferior frontal cortex (specific to invalid trials) versus more superior intraparietal-frontal circuits (common to valid and invalid trials).

The involvement of the medial temporal-lobe region in allocentric mapping of the environment has been observed in human lesion and functional imaging work. Cognitive models of environmental learning ascribe a key role to salient landmarks in representing large-scale space. In the present experiments we examined the neural substrates of the topographical memory acquisition process when environmental landmarks were more specifically identifiable. Using positron emission tomography (PET), we measured regional cerebral blood flow changes while normal subjects explored and learned in a virtual reality environment. One experiment involved an environment containing salient objects and textures that could be used to discriminate different rooms. Another experiment involved a plain empty environment in which rooms were distinguishable only by their shape. Learning in both cases activated a network of bilateral occipital, medial parietal, and occipito-temporal regions. The presence of salient objects and textures in an environment additionally resulted in increased activity in the right parahippocampal gyrus. This region was not activated during exploration of the empty environment. These findings suggest that encoding of salient objects into a representation of large-scale space is a critical factor in instigating parahippocampal involvement in topographical memory formation in humans and accords with previous studies implicating parahippocampal areas in the encoding of object location.