Dissociating top-down attentional control from selective perception and action.

Research into the neural mechanisms of attention has revealed a complex network of brain regions that are involved in the execution of attention-demanding tasks. Recent advances in human neuroimaging now permit investigation of the elementary processes of attention being subserved by specific components of the brain's attention system. Here we describe recent studies of spatial selective attention that made use of positron emission tomography (PET), functional magnetic resonance imaging (fMRI), and event-related brain potentials (ERPs) to investigate the spatio-temporal dynamics of the attention-related neural activity. We first review the results from an event-related fMRI study that examined the neural mechanisms underlying top-down attentional control versus selective sensory perception. These results defined a fronto-temporal-parietal network involved in the control of spatial attention. Activity in these areas biased the neural activity in sensory brain structures coding the spatial locations of upcoming target stimuli, preceding a modulation of subsequent target processing in visual cortex. We then present preliminary evidence from a fast-rate event-related fMRI study of spatial attention that demonstrates how to disentangle the potentially overlapping hemodynamic responses elicited by temporally adjacent stimuli in studies of attentional control. Finally, we present new analyses from combined neuroimaging (PET) and event-related brain potential (ERP) studies that together reveal the timecourse of activation of brain regions implicated in attentional control and selective perception.

Hippocampal, parahippocampal and occipital-temporal contributions to associative and item recognition memory: an fMRI study.

The temporal lobe regions involved in memory retrieval were examined using fMRI. During an associative recognition test, participants made memory judgments about the study color of previously presented drawings of objects, and during item recognition tests they made old/new judgments about previously studied objects or new objects. Associative recognition compared with old item recognition led to activations in bilateral hippocampal and parahippocampal regions, as well as in the left middle occipital gyrus. Old item recognition compared with new item recognition led to activation in the left middle occipital gyrus and the left middle temporal gyrus, and relative deactivations in bilateral hippocampal regions. The results indicate that partially distinct temporal lobe regions are involved during recognition memory for item and associative information.

Tracking the influence of reflexive attention on sensory and cognitive processing.

Previously, we demonstrated that reflexive attention facilitates early visual processing during form discrimination (Hopfinger & Mangun, 1998). In the present study, we tested whether reflexive facilitation of early visual processing will be generated when task load is low (simple luminance detection). Target stimuli that were preceded at short cue-to-target intervals by irrelevant visual events (cues) elicited an enhanced sensory (P1) event-related potential (ERP) component as well as an enhanced longer latency, cognitive ERP component (P300). At long cue-to-target intervals, facilitation in these ERP components was no longer observed, and, although inhibition of return (IOR) was observed in reaction times, the ERPs did not show an inhibition of sensory processing. These results provide converging evidence that reflexive attention transiently facilitates neural processing of visual inputs at multiple stages of analysis (i.e., sensory processing and higher order cognitive processing) but question the view that IOR is manifest at the earliest visual cortical stages of analysis.

Error processing and the rostral anterior cingulate: an event-related fMRI study.

The anterior cingulate is believed to play a crucial role in the regulation of thought and action. Recent evidence suggests that the anterior cingulate may play a role in the detection of inappropriate responses. We used event-related functional magnetic resonance imaging techniques to examine the neural responses to appropriate (correct rejects and correct hits) and inappropriate (errors of commission) behavioral responses during a go/no-go task. Analyses of the inappropriate responses revealed extensive activation in the rostral anterior cingulate cortex and in the left lateral frontal cortex. These areas were not activated for correctly classified trials (correct rejects and correct hits). These data suggest that the rostral anterior cingulate and left lateral frontal cortex are integral components of the brain's error checking system.

A study of analysis parameters that influence the sensitivity of event-related fMRI analyses.

To assess the effect of various analysis parameters on the sensitivity of event-related fMRI analyses, 36 analyses were performed on a single fMRI data-set, varying parameters along four axes: (1) resampled voxel size; (2) spatial smoothing; (3) temporal smoothing; and (4) the set of basis functions used to model event-related responses. Sensitivity (i.e., the probability of detecting an activation given it exists) was assessed in terms of Z scores and by a metric for corrected P values, the negative log of the expected Euler characteristic. Sixteen brain regions distributed across cortical and subcortical areas were included in the meta-analysis. Main effects on sensitivity were found for resampled voxel size, spatial smoothing, temporal smoothing, and the set of basis functions chosen. The analysis parameters that generally produced the most sensitive analyses were a 2-mm(3) resampled voxel size, 10-mm spatial smoothing, 4-s temporal smoothing, and a basis set comprising a hemodynamic response function and its temporal derivative.

The neural mechanisms of top-down attentional control.

Selective visual attention involves dynamic interplay between attentional control systems and sensory brain structures. We used event-related functional magnetic resonance imaging (fMRI) during a cued spatial-attention task to dissociate brain activity related to attentional control from that related to selective processing of target stimuli. Distinct networks were engaged by attention-directing cues versus subsequent targets. Superior frontal, inferior parietal and superior temporal cortex were selectively activated by cues, indicating that these structures are part of a network for voluntary attentional control. This control biased activity in multiple visual cortical areas, resulting in selective sensory processing of relevant visual targets.

Covariations in ERP and PET measures of spatial selective attention in human extrastriate visual cortex.

In a previous study using positron emission tomography (PET), we demonstrated that focused attention to a location in the visual field produced increased regional cerebral blood flow in the fusiform gyrus contralateral to the attended hemifield (Heinze et al. [1994]: Nature 372:543). We related these effects to modulations in the amplitude of the P1 component (80-130 msec latency) of the visual event-related brain potentials (ERPs) recorded from the same subjects, under the identical stimulus and task conditions. Here, we replicate and extend these findings by showing that attention effects in the fusiform gyrus and the P1 component were similarly modulated by the perceptual load of the task. When subjects performed a perceptually demanding symbol-matching task within the focus of spatial attention, the fusiform activity and P1 component of the ERP were of greater magnitude than when the subjects performed a less perceptually demanding task that required only luminance detection at the attended location. In the latter condition, both the PET and ERP attention effects were reduced. In addition, in the present data significant activations were also obtained in the middle occipital gyrus contralateral to the attended hemifield, thereby demonstrating that multiple regions of extrastriate visual cortex are modulated by spatial attention. The findings of covariations between the P1 attention effect and activity in the posterior fusiform gyrus reinforce our hypothesis that common neural sources exist for these complementary, but very different measures of human brain activity.