The effect of age on inhibition of return is independent of non-ocular response inhibition

Inhibition of return (IOR) refers to the slowing of a response to a target stimulus presented in the same location as a previous stimulus. Increased IOR has been observed in older adults, despite a reduction in other 'inhibitory' processes. However, cue-target tasks have been used in all previous studies and because of this, IOR may have been overestimated due to non-ocular response inhibition associated with withholding a response from the cue. Could increased levels of response inhibition account for the observations of increased IOR in older adults? This confound can be circumvented by using a target-target paradigm, in which a response is made to all stimuli. We tested three groups of 24 subjects: young (mean 22.5 years), young-old (mean 61.9 years) and old-old (mean 74.8 years). Subjects completed both visual cue-target and target-target tasks with identical inter-stimulus intervals of 1400 and 1800ms. IOR magnitude increased with age in both the cue-target task and the target-target task. Furthermore, the magnitude of visual IOR was found to increase with age even when individual differences in baseline response speed were taken into account. Thus, there appears to be a genuine increase in IOR magnitude with age.     

Neural correlates of spatial and non-spatial inhibition of return (IOR) in attentional orienting

Exogenous orienting of attention typically produces an early facilitatory effect and a later inhibitory effect, i.e., inhibition of return (IOR). IOR occurs not only in spatial but also in non-spatial domains. Although neural mechanisms associated with spatial IOR have been well established, neural correlates underlying non-spatial IOR remain to be elucidated. In this fMRI study, we compared neural correlates of spatial and non-spatial IOR by adopting a 2 (cue type: location vs. color) x 2 (stimulus onset asynchrony, SOA: long vs. short) x 2 (cue validity: cued vs. uncued) factorial design. Behaviorally, spatial cueing induced the typical biphasic (i.e., the early facilitatory and later inhibitory) effects, while color cueing induced inhibitory effects at both short and long SOAs. Neurally, we found both shared and specific neural correlates of spatial and non-spatial IOR. As compared with short SOA (cued and uncued trials combined), spatial and color cueing at long SOA conjointly activated bilateral precentral gyrus and bilateral lateral occipital cortex, while spatial cueing, but not color cueing, specifically activated bilateral superior parietal cortex. Moreover, left middle frontal gyrus and left inferior frontal gyrus showed significantly higher neural activity in cued trials than in uncued trials during color-based IOR, but not during location-based IOR, implying that episodic retrieval process in the prefrontal cortex may be involved to inhibit old object representations during non-spatial IOR [Grison, S., Paul, M. A., Kessler, K., & Tipper, S. P. (2005). Inhibition of object identity in inhibition of return: Implications for encoding and retrieving inhibitory processes. Psychonomic Bulletin & Review, 12, 553-558; Tipper, S. P., Grison, S., & Kessler, K. (2003). Long-term inhibition of return of attention. Psychological Science, 14, 19-25]. Theoretical implications of the shared and differential neural activity associated with spatial and non-spatial IOR are discussed.     

Deficient inhibition of return for emotional faces in depression

Depression is a commonly-occurred mental disorder. Researchers have highlighted the attentional bias of depressive disorders, although results have been mixed. The cue-target task has often been used to explore attentional bias; a particular phenomenon revealed by such studies is the inhibition of return (IOR). However, cue-target task has seldom been used so far in the study of depressed patients. The aim of the present study was to investigate the IOR phenomenon in depressed individuals in cue-target task using emotional faces as cues.Control participants who had never suffered depression (NC), participants who had experienced at least two depressive episodes in their lives but were currently remitted (RMD), and participants diagnosed with a current major depressive disorder (MDD), were recruited using BDI, BAI, HDRS and DSM-IV as tools. Seventeen participants in each group completed a cue-target task in a behavioral experiment that comprised three kinds of experimental condition, two cue types and four face types. Each participant also completed a simpler cue-target task in an event-related potential (ERP) experiment. In cue-target task, a target appeared after a cue and the participant responded to its location.In the behavioral experiment, it was found that when the stimulus onset asynchrony (SOA) was 14 ms, the NC and RMD participants had IOR effects for all faces and MDD participants for angry and sad faces. When the SOA was 250 ms, all three groups all had cue validity for sad faces but the effect was much more marked for the MDD group. When the SOA was 750 ms, the NC participants had an IOR effect for sad faces, the RMD participants had cue validity for angry, happy and sad faces, and the MDD participants had cue validity for sad faces and an IOR effect for angry faces. In the ERP experiment, the NC participants showed bigger P3 amplitude for happy cue compared with the other groups, smaller P1 amplitude for happy faces in the invalid cue condition than for other faces, smaller P1 amplitude for sad faces in the valid cue condition than for happy faces, bigger P3 amplitude for happy faces in the valid cue condition compared with MDD participants, and bigger P3 amplitude for sad faces in the invalid cue condition compared with other groups. The RMD participants had larger P3 amplitude for sad cue than for other faces, larger P3 amplitude for happy faces in the valid cue condition compared with MDD participants, and smaller P3 amplitude for sad faces in the invalid cue condition compared with NC participants. The MDD participants had larger P1 amplitude for sad cue compared with other groups, larger P3 amplitude for sad cue than for other face cues, smaller P3 amplitude for sad faces in the invalid cue condition compared with NC participants, and smaller P3 amplitude for happy faces in the valid cue condition compared with other groups.It can be concluded that the MDD participants had cue validity and deficient IOR for negative stimuli. The deficient inhibition of negative stimuli renders them unable to eliminate the interference of negative stimuli and causes the maintenance and development of depression. The RMD participants had cue validity and deficient IOR for both positive and negative stimuli, which enables them to perceive positive and negative stimuli sufficiently and to maintain emotional balance.     

Orbitofrontal cortex mediates inhibition of return

Recent accounts have proposed that orbitofrontal cerebral cortex mediates the control of behavior based on emotional feedback and its somatic correlates. Here, we describe the performance of a patient with circumscribed damage to orbitofrontal cortex during a task that requires switching between sensory-motor mappings, contingent on the occurrence of positive and negative reward feedbacks. In this test, normal subjects and other patients with prefrontal damage show an increase in latencies for eye movements towards locations at which a negative feedback was presented on the preceding trial. In contrast, our patient does not show this reward-dependent inhibition of return effect on saccades. She was also found to make an increased rate of ocular refixations during visual search and used a disorganized search strategy in a token foraging task. These findings suggest that orbital regions of the prefrontal cortex mediate an inhibitory effect on actions directed towards locations that have been subject to negative reinforcement. Further, this mechanism seems to play a role in controlling natural search and foraging behavior.     

Space-based but not object-based inhibition of return is impaired in Parkinson's disease

Impairments in certain aspects of attention have frequently been reported in Parkinson's disease (PD), including reduced inhibition of return (IOR). Recent evidence suggests that IOR can occur when attention is directed at objects or locations, but previous investigations of IOR in PD have not systematically compared these two frames of reference. The present study compared the performance of 18 nondemented patients with PD and 18 normal controls on an IOR task with two conditions. In the “object-present” condition, objects surrounded the cues and targets so that attention was cued to both a spatial location and to a specific object. In the “object-absent” condition, surrounding objects were not presented so that attention was cued only to a spatial location. When participants had to rely on space-based cues, PD patients demonstrated reduced IOR compared to controls. In contrast, when objects were present in the display and participants could use object-based cues, PD patients exhibited normal IOR. These results suggest that PD patients are impaired in inhibitory aspects of space-based attention, but are able to overcome this impairment when their attention can be directed at object-based frames of reference. This dissociation supports the view that space-based and object-based components of attention involve distinct neurocognitive processes.     

Manual response preparation disrupts spatial attention: An electrophysiological investigation of links between action and attention

Previous behavioural and neuroscience studies have shown that the systems involved in the control of attention and action are functionally and anatomically linked. We used behavioural and event-related brain potential measures to investigate whether such links are mandatory or merely optional. Cues presented at the start of each trial instructed participants to shift attention to the left or right side and to simultaneously prepare to a finger movement with their left or right hand. In different trials, cues were followed by a central Go signal, requiring execution of the prepared manual response (motor task), or by a peripheral visual stimulus, which required a target-non-target discrimination only when presented on the cued side (attention task). Lateralised ERP components indicative of covert attention shifts were found when attention and action were directed to the same side (same side condition), but not when attention and action were directed to opposite sides (opposite sides condition). Likewise, effects of spatial attention on the processing of peripheral visual stimuli were present only when attention and action were directed to the same side, but not in the opposite sides condition. These results demonstrate that preparing a manual response on one side severely disrupts the attentional selection of visual stimuli on the other side, and suggest that it is not possible to simultaneously direct attention and action to different locations in space. They support the hypothesis that the control of spatial attention and action are implemented by shared brain circuits, and are therefore linked in a mandatory fashion.     

Cognitive inhibition of number/length interference in a Piaget-like task: Evidence by combining ERP and MEG

ObjectiveWe combined event-related potential (ERP) and magnetoencephalography (MEG) acquisition and analysis to investigate the electrophysiological markers of the inhibitory processes involved in the number/length interference in a Piaget-like numerical task.MethodsEleven healthy subjects performed four gradually interfering conditions with the heuristic “length equals number” to be inhibited. Low resolution tomography reconstruction was performed on the combined grand averaged electromagnetic data at the early (N1, P1) and late (P2, N2, P3_early and P3_late) latencies. Every condition was analyzed at both scalp and regional brain levels.ResultsThe inhibitory processes were visible on the late components of the electromagnetic brain activity. A right P2-related frontal orbital activation reflected the change of strategy in the inhibitory processes. N2-related SMA/cingulate activation revealed the first occurrence of the stimuli processing to be inhibited. Both P3 components revealed the working memory processes operating in a medial temporal complex and the mental imagery processes subtended by the precuneus.ConclusionsSimultaneous ERP and MEG signal acquisition and analysis allowed to describe the spatiotemporal patterns of neural networks involved in the inhibition of the “length equals number” interference.SignificanceCombining ERP and MEG ensured a sensitivity which could be reached previously only through invasive intracortical recordings.     

The N400 potential could index a semantic inhibition

In this theoretical study, I briefly review some of the first hypotheses as to the functional significance of the N400 potential. I then summarize the view that the amplitude of the N400 is proportional to difficulty and indexes the efforts deployed by the brain to integrate the meaning of a stimulus in its context. While this view accounts for many literature data, its shortcomings are also pointed out. The need for various inhibition processes is then emphasized together with the idea that integration difficulty may vary with the amount of inhibition to be performed. Consequently, I stress the view that N400 amplitude could index inhibition rather than integration. The fact that, when presented with incongruous sentence endings, subjects are aware of the meanings of both the sentence frame and the ending has an important consequence on this N400 inhibition view. It means that disconfirmed contexts are not inhibited in some conditions, such as when incongruency is relevant in the situation. To account for this fact, the inhibition the N400 could index has to start only once this relevance is coded, that is, at or after the activation of situational representations. We then show that the idea that the N400 reflects such a late inhibition process may account for literature data that are difficult to account for by the integration view. Further studies are thus needed to test this inhibition idea.     

Effects of task context and fluctuations of attention on neural activity supporting performance of the stroop task

The influence of task context and transient fluctuations in attentional control on neural processes supporting performance of the Stroop task was investigated using event-related brain potentials. Task context was manipulated by varying the proportion of congruent and incongruent trials across different blocks of trials, and fluctuations of attentional control were considered by examining differences between trials eliciting faster and slower responses. The amplitudes of the N450, thought to reflect the suppression of a conceptual level processing system, and a temporo-parietal slow wave, thought to index the processing of color information, were greater when trials were mostly congruent in comparison to when trials were mostly incongruent. These findings indicate that the neural systems supporting inhibition and color processing are modulated by task demands. For the N450 the effect of task context interacted with the efficiency of attentional control being present for those trials eliciting faster responses and not for those trials eliciting slower responses. This finding is consistent with those from a growing number of studies indicating that the neural systems supporting attentional control are transient in nature, tending to fluctuate in efficiency over time.     

Watching where you look: modulation of visual processing of foveal stimuli by spatial attention

Two experiments investigated the effect of sustained selective spatial attention upon the perceptual analysis of stimuli within the center of gaze. Spatial attention has typically been studied in relation to peripheral stimuli, and its relevance to the processing of central stimuli has remained relatively ignored. Here, behavioral measures in normal human volunteer participants showed that focused spatial attention can also influence responses to central stimuli, over and beyond the advantage conferred by their foveation. Event-related potentials (ERPs) showed that the action of attention upon foveal stimuli included the modulation of perceptual processing in extrastriate visual areas. Surprisingly, the visual modulation revealed an intriguing and consistent pattern of hemispheric asymmetry, in both experiments. These findings show that in addition to the established right hemisphere dominance of the brain areas that direct attention, the consequences of directed attention may also be asymmetrical.     

The influence of caffeine on spatial-selective attention: an event-related potential study.

OBJECTIVES: Following the indications of previous studies that caffeine might have a specific effect on the processing of spatial information compared with other types of information, the present study investigated the influence of caffeine on an often used spatial-selective attention task. METHODS: Event-related potentials (ERPs) were recorded from 11 participants under conditions of caffeine (250 mg) and placebo. RESULTS: Spatial-selective attention effects were reflected in the ERPs as more positive going occipital P1 and broadly distributed P2 components, and more negative going occipital-temporal N1 and broadly distributed N2 components. A treatment effect was found as a more positive going frontal P2 component in the caffeine condition, whereas interactions between treatment and attention were observed for P2 and N2 components, but not for P1 and N1 components. CONCLUSIONS: This pattern of results suggests that caffeine has no specific influence on spatial-selective attention, but rather, has a more general facilitating effect on perceptual processing, as well as a possible effect on the frontal control mechanisms, i.e. focusing attention and increasing selectivity.     

Orbito‐frontal cortex mechanism of inhibition of return in current and remitted depression

Deficient inhibition of return (IOR) for emotional materials is an important cognitive biomarker of depression. However, its neural mechanism and role in depression remission remain largely unknown. Using functional magnetic resonance imaging (fMRI), this study observed the neural foundation of inhibition of return in individuals with current (n = 30) and remitted (n = 27) depression and in healthy controls (n = 33), by using a cue‐target task. The results showed that individuals with remitted depression (RMD) possessed a nonavoidant attention model for sad faces, which indicated a cue validity and was correlated with enhanced task‐ and resting‐state activation and function connectivity in orbitofrontal cortex (OFC). The patients with major depressive disorder (MDD), in contrast, displayed an IOR effect for all faces, which indicated a strategy of attention avoidance due to the high cognitive burden in the cue‐target task, and was correlated with decreased resting‐state activation and function connectivity in OFC. Moreover, the hippocampus, a less‐known cortex in IOR, showed a contrary model, that is, lower activation in depression remission and higher task‐ and resting‐state activation in depressive episodes. The results suggest the OFC mechanism of the IOR effect in remitted depression and the hippocampus mechanism of the IOR effect in depressive episodes, which offer potential biomarkers for the clinical treatment of depression.     

An ERP study of preparatory and inhibitory mechanisms in a cued saccade task

The present study uses event-related potentials (ERPs) to investigate the neurophysiological correlates of the mechanisms involved in selection of locations for saccades. Participants performed a task in which both target and distractor locations were cued on a trial-by-trial basis. Participants were instructed to make an eye movement to the cued target location and to ignore elements at the distractor location. This experimental set-up allowed the investigation of the mechanisms involved in the top-down preparation and inhibition of locations for an eye movement. When comparing responses to leftward and rightward pointing cues, we observed an early directing attention negativity (EDAN) and an anterior directing attention negativity (ADAN) effect in the cue-target interval. These effects were similar to those observed in studies investigating attentional allocation, suggesting a close link between shifts of spatial attention and the preparation of eye movements. These components were followed by a late widespread contralateral negativity (LDAN) that was assumed to reflect both the oculomotor programming of the upcoming eye movement as well as attentional orienting. Furthermore, a new component was observed related to top-down inhibition of the distractor location. In response to the distractor cue, an early positivity above the right hemisphere (RLIP) was revealed. Finally, no modulations of early target-evoked ERP components were observed, suggesting that these components are unaffected when no further processing is required at the cued location.     

Transient inhibition of the dorsolateral prefrontal cortex disrupts attention-based modulation of tactile stimuli at early stages of somatosensory processing

Damage to the dorsolateral prefrontal cortex (DLPFC) impairs gating of irrelevant sensory information at early cortical processing stages. We investigated how transient inhibition of DLPFC impacts early event-related potentials (ERPs) arising from relevant or irrelevant vibrotactile stimuli to the fingertips. Specifically, we hypothesized that suppression of DLPFC using continuous theta burst stimulation (cTBS) would result in reduced attention-based modulation of tactile ERPs generated at early stages of cortical somatosensory processing. Participants received vibrotactile stimulation to the second and fifth digit on the left hand and reported target stimuli on one digit only (as instructed) in one of three groups following: (1) cTBS over DLPFC (40 s; 600 pulses of 3 stimuli at 50 Hz repeated at 5 Hz using 80% of resting motor threshold for abductor pollicis brevis), (2) sham stimulation, or (3) no stimulation. ERP amplitudes for the P50, N70, P100, N140 and long latency positivity (LLP) were quantified for attended and non-attended trials at C4, CP4, and CP3 electrodes. There was no effect of attention on the P50 and N70 however the P100, N140 and LLP were modulated with attention. The P100 and LLP were significantly more positive during trials where the stimuli were attended to, while the N140 was enhanced for non-attended stimuli. Comparisons between groups revealed a reduction in P100 attention-based modulation for the cTBS group versus sham and no-stimulation groups. While the P100 was clearly reduced for non-attended stimuli relative to attended stimuli in the sham and no-stimulation groups, this effect was attenuated following cTBS. The reduction in attentional modulation of the P100 following cTBS suggests that the DLPFC contributes to filtering irrelevant somatosensory information at early cortical processing stages. Notably the influence of the DLPFC in attention-based modulation was evident even within digits of the same hand. The present results support the use of cTBS as an effective means of transiently suppressing DLPFC excitability.     

Cortical control of Inhibition of Return: Exploring the causal contributions of the left parietal cortex

Inhibition of Return (IOR) refers to longer response times (RTs) when processing information from an already inspected spatial location. This effect encourages orienting towards novel locations and may be hence adaptive to efficiently explore our environment. In a previous study (Bourgeois, Chica, Valero-Cabre, & Bartolomeo, 2013), we demonstrated that repetitive Transcranial Magnetic Stimulation (rTMS) over right hemisphere parietal sites, such as the intra-parietal sulcus (IPS), or the temporo-parietal junction (TPJ), lastingly interfered with manual but not saccadic IOR, for ipsilateral right-sided targets. For contralateral left-sided targets, rTMS over the right IPS, but not over the right TPJ, impaired both manual and saccadic IOR. In the present study, we investigated hemispheric differences in the cortical control of IOR by stimulating left parietal sites with the same design. Contrary to the stimulation of the right hemisphere, rTMS over the left IPS or TPJ did not produce significant modulations of either manual or saccadic IOR. This evidence extends to IOR the validity of current models of hemispheric asymmetries in the control of visuospatial attention.     

The puzzle of spontaneous alternation and inhibition of return: How they might fit together

Two isolated spatial phenomena share a similar “been there; done that” effect on spatial behavior. Originally discovered in rodent learning experiments, spontaneous alternation is a tendency for the organism to visit a different arm in a T‐maze on subsequent trials. Originally discovered in human studies of attention, inhibition of return is a tendency for the organism to orient away from a previously attended location. Whereas spontaneous alternation was identified by O'Keefe & Nadel as dependent on an intact hippocampus, inhibition of return is dependent on neural structures that participate in oculomotor control (the superior colliculus, parietal and frontal cortex). Despite the isolated literatures, each phenomenon has been assumed to reflect a basic novelty‐seeking process, avoiding places previously visited or locations attended. In this commentary, we explore and compare the behavioral manifestations and neural underpinnings of these two phenomena, and suggest what is still needed to determine whether they operate in parallel or serial.     

Specific proactive and generic reactive inhibition

Inhibition concerns the capacity to suppress on-going response tendencies. Patient data and results from neuro-imaging and magnetic-stimulation studies point to a proactive mechanism involving top-down control signals that potentiate inhibitory sensory-motor connections, depending on whether possibly necessary inhibition is anticipated or not. The proactive mechanism is manifest in stronger sensory-cortex responses to stop signals yielding successful inhibition, observed as a modulation of short-latency human evoked potentials (N1) which may overlap with generic mechanisms for infrequent-event detection. A second, reactive, mechanism would be much more independent of the specific inhibition context, and generalize to situations in which behavioral interrupt is not dictated by task demands but invoked by the salience of task-irrelevant but potentially distracting events. The reactive mechanism is visible in a longer-latency human event-related potential termed frontal P3 (fP3) which is elicited by (successful) stop stimuli and most likely originates from dorsal-medial prefrontal cortex (preSMA), and is dissociated from the proactive mechanism pharmacologically and by individual differences. Implications may arise for more personalized treatments of disorders such as ADHD.     

Comparative analysis of event-related potentials during Go/NoGo and CPT: decomposition of electrophysiological markers of response inhibition and sustained attention

Neuropsychological tests target specific cognitive functions; however, numerous cognitive subcomponents are involved in each test. The aim of this study was to decompose the components of two frontal executive function tests, Go/NoGo (GNG) and cued continuous performance task (CPT), by analyzing event-related potentials (ERPs) of 24 subjects both in time and time-frequency domains. In the time domain, P1, N1, P2, N2 and P3 peak amplitudes and latencies and mean amplitudes of 100 ms time windows of the post-P3 time period were measured. For GNG, the N1 amplitude and for both GNG and CPT N2 amplitudes were significantly higher in the NoGo condition compared with the Go condition. P3 had a central maximum in the NoGo conditions of both paradigms in contrast to a parietal maximum in the Go conditions. All peaks except P1 and mean amplitudes of the post-P3 period were more positive in CPT compared to those of GNG. N1, N2 and P3 latencies were longer for the NoGo condition than the Go condition in the CPT. In time-frequency analyses, the NoGo condition evoked higher theta coefficients than the Go condition, whereas the CPT and GNG paradigms differed mainly in the delta band. These results suggest that theta component reflects response inhibition in both GNG and CPT, whereas delta component reflects the more demanding sustained attention requirement of the CPT. The latency prolongation observed with the NoGo condition of the CPT paradigm was thought to be due to perseverance/inhibition conflict enhanced by the primer stimuli in CPT.     

Electrophysiological correlates of spatial orienting towards angry faces: a source localization study

The goal of this study was to examine behavioral and electrophysiological correlates of involuntary orienting toward rapidly presented angry faces in non-anxious, healthy adults using a dot-probe task in conjunction with high-density event-related potentials and a distributed source localization technique. Consistent with previous studies, participants showed hypervigilance toward angry faces, as indexed by facilitated response time for validly cued probes following angry faces and an enhanced P1 component. An opposite pattern was found for happy faces suggesting that attention was directed toward the relatively more threatening stimuli within the visual field (neutral faces). Source localization of the P1 effect for angry faces indicated increased activity within the anterior cingulate cortex, possibly reflecting conflict experienced during invalidly cued trials. No modulation of the early C1 component was found for affect or spatial attention. Furthermore, the face-sensitive N170 was not modulated by emotional expression. Results suggest that the earliest modulation of spatial attention by face stimuli is manifested in the P1 component, and provide insights about mechanisms underlying attentional orienting toward cues of threat and social disapproval.