Attentional systems in target and distractor processing: a combined ERP and fMRI study

doi:10.1016/j.neuroimage.2003.12.034

NeuroImage

Volume 22, Issue 2, June 2004, Pages 530-540

https://doi.org/10.1016/j.neuroimage.2003.12.034 Get rights and content

Abstract

The interplay of “top-down” and “bottom-up” regulated mechanisms is of particular relevance for the rapid (re-)focusing of attention to environmental changes. The purpose of the study was to explore the differential contributions of frontoparietal attentional networks involved in top-down and stimulus-driven processing to the detection of “target” and “distractor” events in a visual three-stimulus oddball paradigm. Thirteen healthy subjects underwent separate event-related potential (ERP) and whole-brain functional magnetic resonance imaging (fMRI) measurements during the oddball task. The targets, which were difficult to detect, elicited a classical posterior P3b whereas the distractor stimuli were followed by a centro-frontal P3a ERP. The fMRI data showed activation of the temporoparietal junction (TPJ) bilaterally and right prefrontal cortex associated with both the target and distractor conditions. This network has previously been described as an attentional system that is predominantly stimulus driven and that responds to rare events. Furthermore, target processing produced bilateral perisylvian activity, which has been related to the “retrieval mode”. Processing of the distractors activated the frontal eye fields (FEFs) and bilateral superior parietal cortex, areas engaged in attention switching and voluntary allocation of attention. Additional left prefrontal activation suggested an involvement of the cortical system for working memory encoding. Our results thus demonstrate that distractor and target processing engage a common neuronal system for the detection of rare events, but also task-specific subsystems related to attention and memory processes.

Section snippets

Subjects

Thirteen right-handed subjects (six females and seven male: mean age, 29; SD, 6.53 years; age range, 19–42) were recruited from an academic environment. All subjects were free from neurological and psychiatric disorders and gave informed consent to participation in the study. The study was approved by the local ethics committee.

Study design (stimuli and procedure)

A three-stimulus oddball paradigm was tested separately in EEG and fMRI sessions. A session included two different task types (circle task and square task) that differed

Behavioral data

Table 2 summarizes the behavioral results. The descriptive statistic indicated that the mean hit rates, response times, and the error rates were satisfactory and comparable to the results of the visual “difficult” condition of Comerchero and Polich (1999). Furthermore, there were no significant differences between the EEG and fMRI sessions in the behavioral data. To test this, we performed repeated measurement t tests of mean response time, hit rate, and error rate based on an a priori alpha

Discussion

The main goal of this study was to distinguish the neuroanatomical correlates of cognitive processes that are shared by target and distractor detection from those that are specific to one of the tasks. The same subjects underwent EEG and fMRI measurements while performing an identical oddball task. The behavioral data showed that the rate of successfully recognized targets was nearly identical during EEG and fMRI measurements, indicating that (a) the task was sufficiently difficult to demand

Conclusion

We investigated the interplay of the brain networks for top-down and stimulus-driven attentional control during a visual oddball paradigm. Both target and distractor detection were characterized by the engagement of a ventrolateral frontoparietal network, which indicates a common mechanism of rare-event detection in both conditions. A second dorsolateral frontoparietal network was engaged particularly in the distractor condition. This finding is compatible with a top-down regulated

Acknowledgements

C.B. was supported by an Alzheimer Forschung Initiative (AFI) grant. We thank Ruxandra Sireteanu and Konrad Maurer for constant support and advice and Michael Russ for advice on technical questions.

References (61)

P Baudena et al.
Intracerebral potentials to rare target and distractor auditory and visual stimuli: III. Frontal cortex
Electroencephalogr. Clin. Neurophysiol.
(1995)
K.J Bruin et al.
Response priming in a go/nogo task: do we have to explain the go/nogo N2 effect in terms of response activation instead of inhibition?
Clin. Neurophysiol.
(2001)
R.L Buckner et al.
Functional-anatomic study of episodic retrieval using fMRI: I. Retrieval effort versus retrieval success
Neuroimage
(1998)
M.D Comerchero et al.
P3a and P3b from typical auditory and visual stimuli
Clin. Neurophysiol.
(1999)
E Courchesne et al.
Stimulus novelty, task relevance and the visual evoked potential in man
Electroencephalogr. Clin. Neurophysiol.
(1975)
J Downar et al.
The effect of task relevance on the cortical response to changes in visual and auditory stimuli: an event-related fMRI study
Neuroimage
(2001)
E Formisano et al.
Tracking the mind's image in the brain I: time-resolved fMRI during visuospatial mental imagery
Neuron
(2002)
D Friedman et al.
The novelty P3: an event-related brain potential (ERP) sign of the brain's evaluation of novelty
Neurosci. Biobehav. Rev.
(2001)
K.J Friston et al.
Analysis of fMRI time-series revisited
Neuroimage
(1995)
E Halgren et al.
Intracerebral potentials to rare target and distractor auditory and visual stimuli: II. Medial, lateral and posterior temporal lobe
Electroencephalogr. Clin. Neurophysiol.
(1995)

E Halgren et al.

Intracerebral potentials to rare target and distractor auditory and visual stimuli: I. Superior temporal plane and parietal lobe

Electroencephalogr. Clin. Neurophysiol.

(1995)

Y.-W Jeon et al.

P3a from passive visual stimulus task

Clin. Neurophysiol.

(2001)

T.L Jernigan et al.

Brain activation during word identification and word recognition

Neuroimage

(1998)

R.T Knight

Decreased response to novel stimuli after prefrontal lesions in man

Electroencephalogr. Clin. Neurophysiol.

(1984)

D.E.J Linden et al.

Cortical capacity constraints for visual working memory: dissociation of fMRI load effects in a fronto-parietal network

NeuroImage

(2003)

K.D Merboldt et al.

Functional MRI of the human amygdala?

Neuroimage

(2001)

D Prvulovic et al.

Functional imaging of visuospatial processing in Alzheimer's disease

Neuroimage

(2002)

C.C Ruff et al.

The role of the anterior cingulate cortex in conflict processing: evidence from reverse stroop interference

Neuroimage

(2001)

M.D Rugg et al.

The role of the prefrontal cortex in recognition memory and memory for source: an fMRI study

Neuroimage

(1999)

D.B Smith et al.

Auditory averaged evoked potentials in man during selective binaural listening

Electroencephalogr. Clin. Neurophysio.l

(1970)

N.K Squires et al.

Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man

Electroencephalogr. Clin. Neurophysiol.

(1975)

E Wojciulik et al.

The generality of parietal involvement in visual attention

Neuron

(1999)

F Barcelo et al.

Think differently: a brain orienting response to task novelty

NeuroReport

(2002)

G.M Boynton et al.

Linear systems analysis of functional magnetic resonance imaging in human V1

J. Neurosci.

(1996)

R Cabeza et al.

Neural bases of learning and memory: functional neuroimaging evidence

Curr. Opin. Neurol.

(2000)

V.P Clark et al.

Responses to rare visual target and distractor stimuli using event-related fMRI

J. Neurophysiol.

(2000)

M Corbetta et al.

Control of goal-directed and stimulus-driven attention in the brain

Nat. Rev., Neurosci.

(2002)

K.R Daffner et al.

The central role of the prefrontal cortex in directing attention to novel events

Brain

(2000)

K.R Daffner et al.

Disruption of attention to novel events after frontal lobe injury in humans

J. Neurol., Neurosurg. Psychiatry

(2000)

R Desimone et al.

Neural mechanisms of selective visual attention

Annu. Rev. Neurosci.

(1995)

Cited by (256)

Functional network properties in schizophrenia and bipolar disorder assessed with high-density electroencephalography
2024, Progress in Neuro-Psychopharmacology and Biological Psychiatry
The study of the cortical functional network properties in schizophrenia (SZ) may benefit from the use of graph theory parameters applied to high-density electroencephalography (EEG). Connectivity Strength (CS) assesses global synchrony of the network, and Shannon Graph Complexity (SGC) summarizes the network distribution of link weights and allows distinguishing between primary and secondary pathways. Their joint use may help in understanding the underpinnings of the functional network hyperactivation and task-related hypomodulation previously described in psychoses.
We used 64-sensor EEG recordings during a P300 oddball task in 128 SZ patients (96 chronic, CR, and 32 first episodes, FE), as well as 46 bipolar disorder (BD) patients, and 92 healthy controls (HC). Pre-stimulus and modulation (task-response minus pre-stimulus windows values) of CS and SGC were assessed in the theta band (4–8 Hz) and the broadband (4–70 Hz).
Compared to HC, SZ patients (CR and FE) showed significantly higher pre-stimulus CS values in the broadband, and both SZ and BD patients showed lower theta-band CS modulation. SGC modulation values, both theta-band and broadband, were also abnormally reduced in CR patients. Statistically significant relationships were found in the theta band between SGC modulation and both CS pre-stimulus and modulation values in patients. CS altered measures in patients were additionally related to their cognitive outcome and negative symptoms. A primary role of antipsychotics in these results was ruled out.
Our results linking SGC and CS alterations in psychotic patients supported a hyperactive and hypomodulatory network mainly involving connections in secondary pathways.
Dopaminergic and norepinephrinergic modulation of endogenous event-related potentials: A systematic review and meta-analysis
2023, Neuroscience and Biobehavioral Reviews
Event-related potentials (ERPs) represent the cortical processing of sensory, motor or cognitive functions invoked by particular events or stimuli. A current theory posits that the catecholaminergic neurotransmitters dopamine (DA) and norepinephrine (NE) modulate a number of endogenous ERPs during various cognitive processes. This manuscript aims to evaluate a leading neurotransmitter hypothesis with a systematic overview and meta-analysis of pharmacologic DA and NE manipulation of specific ERPs in healthy subjects during executive function. Specifically, the frontally-distributed P3a, N2, and N_e/ERN (or error-related negativity) are supposedly modulated primarily by DA, whereas the parietally-distributed P3b is thought to be modulated by NE. Based on preceding research, we refer to this distinction between frontally-distributed DA-sensitive and parietally-distributed NE-sensitive ERP components as the Extended Neurobiological Polich (ENP) hypothesis. Our systematic review and meta-analysis indicate that this distinction is too simplistic and many factors interact with DA and NE to influence these specific ERPs. These may include genetic factors, the specific cognitive processes engaged, or elements of study design, i.e. session or sequence effects or data-analysis strategies.
How low can you go? Measuring human event-related brain potentials from a two-channel EEG system
2023, International Journal of Psychophysiology
Over the past ten years, there has been a rapid increase in the availability and use of mobile electroencephalography (mEEG) in research. Indeed, researchers using mEEG have recorded EEG and event-related brain potentials in a wide range of environments - for example, while walking (Debener et al., 2012), riding a bike (Scanlon et al., 2020), or even in a shopping mall (Krigolson et al., 2021). However, given that low-cost, ease-of-use, and setup speed provide the primary advantages of an mEEG system over large array traditional EEG systems, an important and unresolved question is just how many electrodes does an mEEG system need to collect research-quality EEG data? Here, we tested whether or not a two-channel forehead-mounted mEEG system – the “Patch” – could measure event-related brain potentials within their established amplitude and latency characteristics (Luck, 2014). In the present study, participants performed a visual oddball task while we recorded EEG data from the Patch. Our results demonstrated that we could capture and quantify the N200 and P300 event-related brain potential components using a minimal electrode array forehead-mounted EEG system. Our data further support the idea that mEEG can be used for quick and rapid EEG-based assessments, such as measuring the impact of concussions on the sports field (Fickling et al., 2021) or assessing the impact of stroke severity in a hospital (Wilkinson et al., 2020).
Perceiving social injustice during arrests of Black and White civilians by White police officers: An fMRI investigation
2022, NeuroImage
From social media to courts of law, recordings of interracial police officer-civilian interactions are now widespread and publicly available. People may be motivated to preferentially understand the dynamics of these interactions when they perceive injustice towards those whose communities experience disproportionate policing relative to others (e.g., non-White racial/ethnic groups). To explore these questions, two studies were conducted (study 1 neuroimaging n = 69 and study 2 behavioral n = 58). The fMRI study examined White participants’ neural activity when viewing real-world videos with varying degrees of aggression or conflict of White officers arresting a Black or White civilian. Activity in brain regions supporting social cognition was greater when viewing Black (vs. White) civilians involved in more aggressive police encounters. Additionally, although an independent sample of perceivers rated videos featuring Black and White civilians as similar in overall levels of aggression when civilian race was obscured, participants in the fMRI study (where race was not obscured) rated officers as more aggressive and their use of force as less legitimate when the civilian was Black. In study 2, participants who had not viewed the videos also reported that they believe police are generally more unjustly aggressive towards Black compared with White civilians. These findings inform our understanding of how perceptions of conflict with the potential for injustice shape social cognitive engagement when viewing arrests of Black and White individuals by White police officers.
A resting-state network for novelty: Similar involvement of a global network under rest and task conditions
2022, Psychiatry Research - Neuroimaging
Neuroimaging research provides converging evidence in support of functional networks active under rest conditions. While these networks are typically locally-distributed, a globally-distributed resting-state network (gRSN) was recently identified. The gRSN component is characterized by a scalp topography similar to that of the widely-studied P3 component of the event related potential, thought to represent the brain's response to novelty. In this study, we investigate similarities between the neural generators underlying these two networks to test the hypothesis that the gRSN is a resting-state network for novelty. By using the second-order blind identification (SOBI) algorithm, which works with temporal information, we show that (1) a resting-state component resembling the topography of the P3 can be recovered in all participants; (2) this gRSN component can be modeled with a set of ECDs with high goodness of fit; (3) ECD locations of the gRSN correspond to a network of globally-distributed brain structures overlapping heavily with the networking underlying the P3; and, (4) structures underlying these two networks are similarly involved during task and resting-state conditions. We interpret this as evidence in support of a resting-state network for detection and response to novelty.
Behavioral and electrocortical effects of transcranial alternating current stimulation during advice-guided decision-making
2021, Neuroimage: Reports
In decision-making with uncertain outcomes people may rely on external cues, such as expert advice, even if this information has no predictive value. While the fronto-parietal event-related potential (ERP) components feedback-related negativity (FRN) and P3 are associated with both reward/punishment feedback processing, the relationship between ERP modulation and expert advice during decision making remains unclear. In this double-blind sham-controlled within-subject study transcranial alternating current stimulation (tACS) at an intensity of 1 mA was applied to the frontal cortex in twenty-four healthy volunteers. The aim was to decrease reliance on expert advice by targeting FRN, P3a and P3b components. Following administration of frontal delta (2.5 Hz), theta (5 Hz) and sham tACS, ERPs and advice-guided decision making were evaluated. Results showed a tentative behavioral effect of delta tACS in the response bias. In contrast, theta tACS significantly lowered P3b and P3a amplitudes, but no effects of tACS were observed for the FRN. Effects on electrophysiology and advice following behavior were uncorrelated. Our findings suggest that theta tACS may modulate electrocortical signals and delta tACS advice following, yet the relationship between both remains unresolved.

View all citing articles on Scopus

¹: These authors contributed equally to the work.

View full text

Attentional systems in target and distractor processing: a combined ERP and fMRI study

Abstract

Section snippets

Subjects

Study design (stimuli and procedure)

Behavioral data

Discussion

Conclusion

Acknowledgements

Electroencephalogr. Clin. Neurophysiol.

Clin. Neurophysiol.

Neuroimage

Clin. Neurophysiol.

Electroencephalogr. Clin. Neurophysiol.

Neuroimage

Neuron

Neurosci. Biobehav. Rev.

Neuroimage

Electroencephalogr. Clin. Neurophysiol.

Electroencephalogr. Clin. Neurophysiol.

Clin. Neurophysiol.

Neuroimage

Electroencephalogr. Clin. Neurophysiol.

NeuroImage

Neuroimage

Neuroimage

Neuroimage

Neuroimage

Electroencephalogr. Clin. Neurophysio.l

Electroencephalogr. Clin. Neurophysiol.

Neuron

Think differently: a brain orienting response to task novelty

NeuroReport

Linear systems analysis of functional magnetic resonance imaging in human V1

J. Neurosci.

Neural bases of learning and memory: functional neuroimaging evidence

Curr. Opin. Neurol.

Responses to rare visual target and distractor stimuli using event-related fMRI

J. Neurophysiol.

Control of goal-directed and stimulus-driven attention in the brain

Nat. Rev., Neurosci.

The central role of the prefrontal cortex in directing attention to novel events

Brain

Disruption of attention to novel events after frontal lobe injury in humans

J. Neurol., Neurosurg. Psychiatry

Neural mechanisms of selective visual attention

Annu. Rev. Neurosci.