Anna C. Nobre

Top-down modulation: bridging selective attention and working memory

Selective attention, the ability to focus our cognitive resources on information relevant to our goals, influences working memory (WM) performance. Indeed, attention and working memory are increasingly viewed as overlapping constructs. Here, we review recent evidence from human neurophysiological studies demonstrating that top-down modulation serves as a common neural mechanism underlying these two cognitive operations. The core features include activity modulation in stimulus-selective sensory cortices with concurrent engagement of prefrontal and parietal control regions that function as sources of top-down signals. Notably, top-down modulation is engaged during both stimulus-present and stimulus-absent stages of WM tasks; that is, expectation of an ensuing stimulus to be remembered, selection and encoding of stimuli, maintenance of relevant information in mind and memory retrieval.

Covert Visual Spatial Orienting and Saccades: Overlapping Neural Systems

We used functional magnetic resonance imaging (fMRI) to investigate the functional anatomical relationship between covert orienting of visual spatial attention and execution of saccadic eye movements. Brain areas engaged by shifting spatial attention covertly and by moving the eyes repetitively toward visual targets were compared and contrasted directly within the same subjects. The two tasks activated highly overlapping neural systems and showed that common parietal and frontal regions are more activated during the covert task than the overt oculomotor condition. The possible nature of the relationship between these two operations is discussed.

Orienting attention in time: behavioural and neuroanatomical distinction between exogenous and endogenous shifts.

Temporal orienting of attention is the ability to focus resources at a particular moment in time in order to optimise behaviour, and is associated with activation of left parietal and premotor cortex [Coull, J. T., Nobre, A. C. 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. Journal of Neuroscience, 1998, 18, 7426-7435]. In the present experiment, we explored the behavioural and anatomical correlates of temporal orienting to foveal visual stimuli, in order to eliminate any spatial attention confounds. We implemented a two-way factorial design in an event-related fMRI study to examine the factors of trial validity (predictability of target by cue), length of delay (cue-target interval), and their interaction. There were two distinct types of invalid trial: those where attention was automatically drawn to a premature target and those where attention was voluntarily shifted to a delayed time-point. Reaction times for valid trials were shorter than those for invalid trials, demonstrating appropriate allocation of attention to temporal cues. All trial-types activated a shared system, including frontoparietal areas bilaterally, showing that this network is consistently associated with attentional orienting and is not specific to spatial tasks. Distinct brain areas were sensitive to cue-target delays and to trial validity. Long cue-target intervals activated areas involved in motor preparation: supplementary motor cortex, basal ganglia and thalamus. Invalid trials, where temporal expectancies were breached, showed enhanced activation of left parietal and frontal areas, and engagement of orbitofrontal cortex bilaterally. Finally, trial validity interacted with length of delay. Appearance of targets prematurely selectively activated visual extrastriate cortex; while postponement of target appearance selectively activated right prefrontal cortex. These findings suggest that distinct brain areas are involved in redirecting attention based upon sensory events (bottom-up, exogenous shifts) and based upon cognitive expectations (top-down, endogenous shifts).

Hunger selectively modulates corticolimbic activation to food stimuli in humans.

Functional magnetic resonance imaging (fMRI) was used to determine whether visual responses to food in the human amygdala and related corticolimbic structures would be selectively altered by changes in states of hunger. Participants viewed images of motivationally relevant (food) and motivationally irrelevant (tool) objects while undergoing fMRI in alternately hungry and satiated conditions. Food-related visual stimuli elicited greater responses in the amygdala, parahippocampal gyrus. and anterior fusiform gyrus when participants were in a hungry state relative to a satiated state. The state-dependent activation of these brain structures did not generalize to the motivationally irrelevant objects. These results support the hypothesis that the amygdala and associated inferotemporal regions are involved in the integration of subjective interoceptive states with relevant sensory cues processed along the ventral visual stream.

Language-related field potentials in the anterior-medial temporal lobe: I. Intracranial distribution and neural generators.

Field potentials were recorded from intracranial electrodes in humans to study language-related processing. Subjects viewed sentences in which each word was presented successively in the center of a video monitor. Half of the sentences ended normally, while the other half ended with a semantically anomalous word. The anomalous sentence-ending words elicited a large negative field potential with a peak latency near 400 msec, which was focally distributed bilaterally in the anterior medial temporal lobe (AMTL), anterior to the hippocampus and near the amygdala. Subdural electrodes positioned near the collateral sulcus just inferior and lateral to the amygdala recorded a positive field potential at the same latency. This spatial distribution of voltage suggested that this language-sensitive field potential was generated in the neocortex near the collateral sulcus and anterior fusiform gyrus. Additional task-related field potentials were recorded in the hippocampus. The AMTL field potential at 400 msec shares characteristics with the N400 potential recorded from scalp electrodes that has been associated with semantic processing.

Orienting Attention to Locations in Internal Representations

Three experiments investigated whether it is possible to orient selective spatial attention to internal representations held in working memory in a similar fashion to orienting to perceptual stimuli. In the first experiment, subjects were either cued to orient to a spatial location before a stimulus array was presented (pre-cue), cued to orient to a spatial location in working memory after the array was presented (retro-cue), or given no cueing information (neutral cue). The stimulus array consisted of four differently colored crosses, one in each quadrant. At the end of a trial, a colored cross (probe) was presented centrally, and subjects responded according to whether it had occurred in the array. There were equivalent patterns of behavioral costs and benefits of cueing for both pre-cues and retro-cues. A follow-up experiment used a peripheral probe stimulus requiring a decision about whether its color matched that of the item presented at the same location in the array. Replication of the behavioral costs and benefits of pre-cues and retro-cues in this experiment ruled out changes in response criteria as the only explanation for the effects. The third experiment used event-related potentials (ERPs) to compare the neural processes involved in orienting attention to a spatial location in an external versus an internal spatial representation. In this task, subjects responded according to whether a central probe stimulus occurred at the cued location in the array. There were both similarities and differences between ERPs to spatial cues toward a perception versus an internal spatial representation. Lateralized early posterior and later frontal negativities were observed for both preand retro-cues. Retro-cues also showed additional neural processes to be involved in orienting to an internal representation, including early effects over frontal electrodes.

The hazards of time.

Temporal expectations are continuously formed and updated, and interact with expectations about other relevant attributes of events, in order to optimise our interaction with unfolding sensory stimulation. In this paper, we will highlight some evidence revealing the pervasive effects of temporal expectations in modulating perception and action, and reflect on the current state of understanding about their underlying neural systems and mechanisms.

The large-scale neural network for spatial attention displays multifunctional overlap but differential asymmetry.

Functional magnetic resonance imaging (fMRI) was used to determine the brain regions activated by two types of covert visuospatial attentional shifts: one based on exogenous spatial priming and the other on foveally presented cues which endogenously regulated the direction of spatial expectancy. Activations were seen in the cortical and subcortical components of a previously characterized attentional network, namely, the frontal eye fields, posterior parietal cortex, the cingulate gyrus, the putamen, and the thalamus. Additional activations occurred in the anterior insula, dorsolateral prefrontal cortex, temporo-occipital cortex in the middle and inferior temporal gyri, the supplementary motor area, and the cerebellum. Direct comparisons showed a nearly complete overlap in the location of activations resulting from the two tasks. However, the spatial priming task displayed a more pronounced rightward asymmetry of parietal activation, and a conjunction analysis showed that the area of posterior parietal cortex jointly activated by both tasks was more extensive in the right hemisphere. Furthermore, the posterior parietal and temporo-occipital activations were more pronounced in the task of endogenous attentional shifts. The results show that both exogenous (based on spatial priming) and endogenous (based on expectancy cueing) shifts of attention are subserved by a common network of cortical and subcortical regions. However, the differences between the two tasks, especially in the degree of rightward asymmetry, suggests that the pattern of activation within this network may show variations that reflect the specific attributes of the attentional task.

The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention.

The purpose of this study was to identify brain regions underlying internally generated anticipatory biases toward locations where significant events are expected to occur. Subjects fixated centrally and responded to peripheral targets preceded by a spatially valid (predictive), invalid (misleading), or neutral central cue while undergoing fMRI scanning. In some validly cued trials, reaction time was significantly shorter than in trials with neutral cues, indicating that the cue had successfully induced a spatial redistribution of motivational valence, manifested as expectancy. The largest cue benefits led to selectively greater activations within the posterior cingulate and medial prefrontal cortex. These two areas thus appear to establish a neural interface between attention and motivation. An inverse relationship to cue benefit was seen in the parietal cortex, suggesting that spatial expectancy may entail the inhibition of attention-related areas to reduce distractibility by events at irrelevant locations.

The Response of Left Temporal Cortex to Sentences

The meaning of a sentence differs from the sum of the meanings of its constituents. Left anterior temporal cortex responds to sentences more strongly than to unconnected words. We hypothesized that the anterior temporal response to sentences is due to this difference in meaning (compositional semantics). Using positron emission tomography (PET), we studied four experimental conditions (2 2 factorial design): In one condition, subjects read normal sentences. In a second condition, they read grammatically correct sentences containing numerous semantic violations (semantically random sentences). In a third condition, we scrambled the word order within the normal sentences, and, in a fourth condition, the word order was scrambled within the semantically random sentences. The left anterior temporal pole responded strongly to sentences compared to scrambled versions of sentences. A similar although weaker response occurred in the left anterior superior temporal sulcus and the left posterior middle temporal gyrus. A subset of voxels within the left anterior temporal pole responded more to semantically random sentences and their scrambled versions than to normal sentences and the corresponding scrambled versions (main effect of semantic randomness). Finally, the grammatical and the semantic factor interacted in a subset of voxels within the anterior temporal pole: Activity was higher when subjects read normal sentences compared to their scrambled versions but not for semantically random sentences compared to their corresponding scrambled versions. The effects of grammar and meaning and, most importantly, the interaction between grammatical and semantic factors are compatible with the hypothesis that the left anterior temporal pole contributes to the composition of sentence meaning.