Clinical Neurophysiology xxx (2014) xxx–xxx

Contents lists available at ScienceDirect

Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph

Effects of stimulus-driven and goal-directed attention on prepulse inhibition of the cortical responses to an auditory pulse Agnès Annic a,b,⇑, Perrine Bocquillon a,b, Jean-Louis Bourriez b, Philippe Derambure a,b, Kathy Dujardin a,c a

Université Lille Nord de France, EA1046 Lille, France Department of Clinical Neurophysiology, Lille University Medical Center, Lille, France c Department of Neurology and Movement Disorders, Lille University Medical Center, Lille, France b

a r t i c l e

i n f o

Article history: Accepted 6 December 2013 Available online xxxx Keywords: Prepulse inhibition Auditory evoked potential Continuous performance test Attention Source localization

h i g h l i g h t s  We evaluated the effect of attention on sensory gating of cortical responses to a pulse.  Stimulus-driven attention influenced prepulse inhibition of the N100 component and goal-directed

attention influenced prepulse inhibition of the P200 component.  Cortical sources of N100 and P200 were modulated by brain areas involved in attention.

a b s t r a c t Objective: Inhibition by a prepulse (prepulse inhibition, PPI) of the response to a startling acoustic pulse is modulated by attention. We sought to determine whether goal-directed and stimulus-driven attention differentially modulate (i) PPI of the N100 and P200 components of the auditory evoked potential (AEP) and (ii) the components’ generators. Methods: 128-channel electroencephalograms were recorded in 26 healthy controls performing an active acoustic PPI paradigm. Startling stimuli were presented alone or either 400 or 1000 ms after a visual prepulse. Three types of prepulse were used: to-be-attended (goal-directed attention), unexpected (stimulus-driven attention) or to-be ignored (non focused attention). We calculated the percentage PPI for the N100 and P200 components of the AEP and determined cortical generators by standardized weighted low resolution tomography. Results: At 400 ms, the PPI of the N100 was greater after an unexpected prepulse than after a to-beattended prepulse, the PPI of the P200 was greater after a to-be-attended prepulse than after a to-be ignored prepulse. At 1000 ms, to-be-attended and unexpected prepulses had similar effects. Cortical sources were modulated in areas involved in both types of attention. Conclusions: Stimulus-driven attention and goal-directed attention each have specific effects on the attentional modulation of PPI. Significance: By using a new PPI paradigm that specifically controls attention, we demonstrated that the early stages of the gating process (as evidenced by N100) are influenced by stimulus-driven attention and that the late stages (as evidenced by P200) are influenced by goal-directed attention. Ó 2013 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.

1. Introduction Filtering out irrelevant information is a crucial way of protecting the cognitive resources required for goal-directed activities. One of the physiological indices of these protective neural ⇑ Corresponding author. Address: Department of Clinical Neurophysiology, Roger Salengro Hospital, F-59037 Lille cedex, France. Tel.: +33 320 446 461; fax: +33 320 446 355. E-mail addresses: [email protected], [email protected] (A. Annic).

processes is referred to as prepulse inhibition (PPI), an index of sensorimotor gating. It corresponds to the attenuation of the startle reflex amplitude to an intense tactile, visual or acoustic stimulus (called the pulse) when a weaker, non-startling stimulus (the prepulse) precedes the pulse by approximately 30–500 ms. The prepulse attenuates not only motor responses (e.g., the eye-blink reflex) but also cortical responses to a sound pulse, such as the N100 and P200 components of the auditory evoked potential (AEP) (Perlstein et al., 1993, 2001) or the auditory evoked theta,

1388-2457/$36.00 Ó 2013 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.clinph.2013.12.002

Please cite this article in press as: Annic A et al. Effects of stimulus-driven and goal-directed attention on prepulse inhibition of the cortical responses to an auditory pulse. Clin Neurophysiol (2014), http://dx.doi.org/10.1016/j.clinph.2013.12.002

2

A. Annic et al. / Clinical Neurophysiology xxx (2014) xxx–xxx

alpha and gamma oscillations (Kedzior et al., 2006, 2007). The N100 component of the AEP is thought to represent the processing of the auditory stimulus’s physical attributes, e.g., its intensity (Davis and Zerlin, 1966), and is thus a measure of the initial registration, processing and attribute selection of an auditory stimulus (Hillyard and Picton, 1979). The P200 component of the AEP reflects a later stage of stimulus processing and is viewed as an index of some aspects of the stimulus classification process (Garcia-Larrea et al., 1992). Therefore, PPI of these AEP components could be a marker of sensory and cognitive gating. According to Inui et al. (2012), PPI of cortical responses could be a valuable tool for understanding the mechanisms of sensory gating and the impairments of these mechanisms in disease. Perriol et al. (2005) used PPI of cortical responses to a pulse to compare attention disorders in patients with Lewy body dementia, Parkinson’s disease dementia and Alzheimer’s disease. They observed disruption of PPI of the N100 and P200 components of the AEP in patients with Lewy body dementia and Parkinson’s disease dementia but not in patients with Alzheimer’s disease, this suggested the involvement of dopaminergic subcorticothalamocortical networks in PPI regulation. Data from animal studies have suggested that sensorimotor gating is mediated by the corticostriatal and pallidothalamic circuitry, which includes the prefrontal cortex, thalamus, amygdala, hippocampus, nucleus accumbens, striatum, ventral pallidum, and globus pallidum (Swerdlow et al., 2001). In a functional magnetic resonance imaging (fMRI) study, Campbell et al. (2007) described a primary pontine circuitry for sensorimotor gating that interconnects with inferior parietal, superior temporal, frontal and prefrontal cortices via the thalamus and striatum. Hence, PPI is mediated by a broad network that includes cortical regions known to be involved in cognitive processes (namely attention). Moreover, although the magnitude of PPI is influenced by the prepulse-pulse lead interval (Filion et al., 1998), the PPI can also be modulated by attention processes. Several researchers have reported that in an active PPI paradigm (when participants are explicitly asked to attend to the prepulse), PPI is greater after a to-be-attended prepulse than after a to-be-ignored prepulse (Dawson et al., 1993; Filion et al., 1993). Rissling et al. (2007) combined an active PPI paradigm with a continuous performance test (CPT) involving rapid perceptual discrimination and working-memory processes. In Rissling et al.’s experiment, participants were presented a series of single digits (from 0 to 9) and were instructed to (i) press a response button after they saw a 0–0 sequence and (ii) refrain from pressing the button at any other time. The auditory pulses were presented just after the visual stimuli, which were used as a prepulse. Hence, the ‘‘0’’ was the to-be-attended visual prepulse and the other digits served as to-be-ignored visual prepulses. With a lead interval of 240 ms, startle eye-blink inhibition was greater after the to-be-attended prepulse than after the to-be-ignored prepulse. However, the attentional modulation of PPI has only been investigated for the eye-blink reflex. Furthermore, only passive PPI paradigms (i.e., with no tasks to be performed and no instructions concerning the prepulse) have been used to modulate the amplitude of the N100 and P200 components of the AEP (Abduljawad et al., 2001; Perriol et al., 2005; Inui et al., 2012; De Pascalis et al., 2013). The effect of attention on these markers of sensory and cognitive gating has not previously been investigated. Moreover, attention is a complex neurocognitive process. It can be either goal-directed (i.e., focused on relevant signals derived from task demands) or stimulus-driven (i.e., captured by salient properties of stimuli that are sometimes irrelevant for the task) (Desimone and Duncan, 1995; Kastner and Ungerleider, 2000). To the best of our knowledge, it has not been established whether goal-directed attention and stimulus-driven attention differ in their modulation of PPI.

Given that (i) PPI of the N100 and P200 components of the AEP is a marker of sensory and cognitive gating and (ii) the effect of attention on these cortical indexes had not previously been investigated (especially in terms of their differential modulation by stimulus-driven and goal directed attention), the main objective of the present study was to evaluate the effect of stimulus-driven and goal-directed attention on PPI of the AEP N100 and P200 components. Moreover, modulation of the anatomical sources of these AEP components by a prepulse had never previously been investigated. Anatomical sources of potentials recorded on the surface of the scalp can be studied with source reconstruction methods. Of the various methods, standardized low-resolution electromagnetic tomography (sLORETA), introduced by Pascual-Marqui (2002) is an interesting tool for modeling spatially distinct source activities in the absence of prior knowledge of the generators’ anatomical location. Standardized weighted low-resolution electromagnetic tomography (swLORETA) is a recent modification of sLORETA, which compensates for variations in the sensors’ sensitivity to current sources at different depths (Palmero-Soler et al., 2007). Hence, our secondary objective was to use swLORETA to determine how the cortical generators of N100 and P200 components of the AEP were modulated by the nature type of attention paid to the prepulse. To this end, we combined an active acoustic PPI paradigm with a visual CPT as in Rissling et al. (2007) and studied inhibition of the cortical responses by recording the N100 and P200 components of the AEP. In contrast to previous studies using active PPI paradigms, we used three types of prepulse in the present work: one on which the subject’s attention was voluntary focused (to-be-attended), one on which the subject’s attention has not to be focused (to-be-ignored) and a third one that involuntarily captured the subject’s attention (unexpected). To control for the attentional resources allocated to each type of prepulse, the event-related potential P300 component was recorded. It has been demonstrated that the amplitude of P300 varies according to the amount of attentional resources allocated to the task (Donchin et al., 1986). In the present study, we expected that the to-be-attended prepulse (involved in goal-directed attention) would be associated with the late, centroparietal P300 component which is observed when an infrequent, task-relevant stimulus is presented, whereas the unexpected prepulse (involved in stimulus-driven attention) would be associated with the early, frontocentral P300 which occurs when the subject is presented with an unexpected stimulus in the absence of any instructions (Squires et al., 1975). We hypothesized that the degree of inhibition of cortical responses to the pulse would depend on the prepulse type, with (i) greater inhibition after a to-be-attended prepulse or an unexpected prepulse than after a to-be-ignored prepulse and (ii) greater inhibition after a to-beattended prepulse than after an unexpected prepulse. We also assumed that each type of prepulse would differentially modulate the N100 and P200 components and the latter’s generators.

2. Methods 2.1. Participants The study populations comprised 26 right-handed, healthy volunteers (10 female, 16 male; mean (SD) age: 22.4 (2.7) years). According to self-reports, none of the participants had a history of neurological or psychiatric disorders. None was taking psychoactive drugs, including tobacco or cannabis. Subjects with a history of visual or auditory impairments were excluded from the study. All participants gave their informed consent to participation in the study. The study protocol was approved by the local institutional review board (‘‘Comité de Protection des Personnes NordOuest IV’’, reference 2008-006842-25).

Please cite this article in press as: Annic A et al. Effects of stimulus-driven and goal-directed attention on prepulse inhibition of the cortical responses to an auditory pulse. Clin Neurophysiol (2014), http://dx.doi.org/10.1016/j.clinph.2013.12.002

A. Annic et al. / Clinical Neurophysiology xxx (2014) xxx–xxx

2.2. Task Subjects were comfortably seated and watched a 17-inch monitor placed 150 cm away. They performed a startle-CPT session similar to that used by Rissling et al. (2007). The startling acoustic stimulus (the pulse) was a 110 dB, 40 ms burst of white noise (measured with a sound level meter) with a near instantaneous rise/fall time. It was presented binaurally through headphones (TDH39). Each session included a control task and a startle-CPT task. During the control task, participants were presented a series of 140 ‘‘O’’ letters (4 cm high and 3.5 cm wide). The presentation time was 29 ms and the interstimulus interval varied from 1300 to 1500 ms (mean: 1400 ms). Participants only had to watch to the monitor. They were instructed that they would occasionally hear a brief burst of noise through the headphones but did not need to pay attention to it. Ten pulses were randomly delivered, with an inter-pulse interval ranging from 18 to 30 s (mean = 24 s). None of the pulses were temporally related to visual stimuli. The aim of this control task was to record responses to ‘‘pulse only’’ stimuli in a perceptual context that was as similar as possible to the startleCPT task.

3

During the startle-CPT task (Fig. 1), the participants were presented a series of 360 visual stimuli (presentation time: 29 ms; interstimulus interval from 1300 to 1500 ms (mean: 1400 ms), as in the control task). The stimuli were the letters ‘‘O’’, ‘‘X’’ and ‘‘A’’ (4 cm high and 3.5 cm wide) and meaningless symbols (filling the whole screen). Participants were instructed to press a response button as quickly as possible with the right index finger only when the probe letter X occurred immediately after the cue letter A. The following trial frequencies were used: target A–X: 11%; A–O: 11%; no A–X: 17%; no A–O: 61%. ‘‘No A’’ trials included sequences with the letter ‘‘O’’ or symbols; however, participants were not informed of the possible occurrence of symbols. During this CPT task, 30 auditory pulses were delivered: 10 after the letter ‘‘A’’ (the to-beattended prepulse), 10 after a non-A letter (the to-be-ignored prepulse) and 10 after a symbol (the unexpected prepulse, capturing involuntarily attention). Fifteen of the 30 sounds were delivered 400 ms after the visual stimulus (i.e., with a short-lead interval) and fifteen were delivered 1000 ms after (i.e., with a long-lead interval). To limit anticipation and habituation, the pulses were delivered at variable intervals and with at least fourteen seconds between two pulses. Two blocks of the startle-CPT task were administered. They were preceded by a practice CPT-only block

Fig. 1. Schematic representation of the continuous performance test (CPT)-startle task. ISI: interstimulus interval.

Please cite this article in press as: Annic A et al. Effects of stimulus-driven and goal-directed attention on prepulse inhibition of the cortical responses to an auditory pulse. Clin Neurophysiol (2014), http://dx.doi.org/10.1016/j.clinph.2013.12.002

4

A. Annic et al. / Clinical Neurophysiology xxx (2014) xxx–xxx

during which 20 visual stimuli (the letters ‘‘O’’, ‘‘X’’ and ‘‘A’’) were presented to the participants, along with one example of an A-X sequence. In both conditions, a central fixation cross was continuously presented during interstimulus intervals. The mean response time, the number of hits and the number of false alarms were recorded. 2.3. Electroencephalographic recording An electroencephalogram (EEG) was recorded continuously from 128 scalp locations, using a DC amplifier (ANT Software BV, Enschede, The Netherlands) and a Quick-capÒ 128 AgCl electrode cap (ANT Software BV) placed according to the 10/05 international system (Oostenveld and Praamstra, 2001) with a linked mastoid reference. A vertical electro-oculogram (EOG) was recorded using two electrodes placed 1.5 cm above and below the axis of the right pupil, in order to detect artifacts related to eye movements. We used Advanced Source AnalysisÒ (ASA) software (ANT Software BV, Enschede, the Netherlands) for data acquisition. The EEG and EOG signals were digitized with a sampling rate of 1024 Hz. Electrode impedances were kept below 5 kOhms. 2.4. EEG analysis The EEG data were analyzed with ASAÒ software. The EEG signal was band-pass filtered between 0.1 and 30 Hz and ocular artifacts were detected and removed off-line. During the control task, AEPs were averaged over a 500 ms epoch starting 100 ms before the pulse. During the startle-CPT task, AEPs were averaged separately for each type of prepulse and each lead interval (400 and 1000 ms) over a 500 ms epoch starting 100 ms before the pulse. For each epoch, a baseline correction was performed using data from 100 ms prior to the stimulus. P300 potentials were averaged over a 900 ms epoch starting 100 ms before the (visual) stimulus onset. For each epoch, a baseline correction was performed using data from 100 ms prior to the stimulus. The N100 component of the AEP was defined as the largest negative peak from baseline in a 75–150 ms window following presentation of the pulse. The P200 component of the AEP was defined as the largest positive peak from baseline in a 130–300 ms window following presentation of the pulse. The N100 and P200 baselineto-peak amplitude values were measured at Cz. Lastly, the P300 potential was defined as the largest positive peak in a 250– 600 ms window following presentation of the visual stimulus. Baseline-to-peak amplitude was measured at each of the three midline electrodes (Fz, Cz and Pz). Given that the positive P300 potential occurred during the AEP, the N100 and P200 components of the AEP after each type of prepulse (‘‘A’’, ‘‘noA’’ and symbol) with a 400 ms interval were better identified by subtracting the visual P300 components respectively associated with presentation of the letter ‘‘A’’, ‘‘noA’’ and the symbol. The percentage PPI of N100 and P200 was calculated according to the equation: 100 

ðresponse amplitude in the control session  response amplitude in the test sessionÞ response amplitude in the control session

2.5. swLORETA and AEP source localization SwLORETA was performed with ASAÒ software. The swLORETA solution was computed using a standard set of electrodes and a standard MRI dataset (Evans and Collins, 1993) within which a three-dimensional grid of 1056 points (grid spacing: 5 mm) restricted to the grey matter represents the possible signal sources.

The boundary element model was used to compute the lead field matrix and model the mechanism by which the original current sources are superimposed on each other to yield the measured voltage fields at each detector. This constitutes the first step in any attempt to compute an inverse solution (Geselowitz, 1967). We calculated the mean current density of the swLORETA analysis for all time-points within a 30 ms time window around the N100 and P200 peaks (the ‘‘peak window’’) in the control task and for each type of prepulse (‘‘A’’, ‘‘noA’’ and symbol) in the startle-CPT task. The same calculation was performed for a 30 ms time window within the baseline period (65 to 35 ms before pulse presentation – hereafter referred to as the ‘‘baseline window’’). 2.6. Statistical analysis The Kolmogorov–Smirnov test was used to check for normal data distributions. 2.6.1. PPI of the N100 and P200 components of the AEP One-factor repeated-measures analyses of variance (ANOVAs) were performed separately for each lead interval, with prepulse (‘‘A’’, ‘‘noA’’ or symbol) as within-subject factor. When required, post hoc analyses with a Bonferroni correction were performed. The significance threshold was set to p < 0.05 for all analyses. 2.6.2. P300 Two-factor repeated-measures analyses of variance (ANOVAs) were performed, with the prepulse (‘‘A’’, ‘‘noA’’ or symbol) and location (Fz, Cz, Pz) as within-subject factors. When required, post hoc analyses with a Bonferroni correction were performed. The significance threshold was set to p < 0.05 for all the latter analyses. 2.7. Source localization for AEP data 2.7.1. Generators of the N100 and P200 components of the AEP Comparisons were performed by applying a non-parametric permutation procedure (Nichols and Holmes, 2002), with a null hypothesis H0: R (swLORETA peak–swLORETA baseline) = 0. To identify cortical generators of the N100 and P200 components of the AEP, we used the control dataset and performed a [peak–baseline] contrast. 2.7.2. Attentional modulation of generators To identify how each prepulse modulated the cortical generators of the N100 and P200 components, we performed [peak–baseline] contrasts for the startle-CPT task. 2.7.2.1. The control task versus startle-CPT task. We performed a [control–startle-CPT task] contrast, with a null hypothesis H0: R (swLORETA peak control–swLORETA peak startle-CPT task) = 0 and by using swLORETA solutions for N100 and P200 generators. These comparisons allowed us to identify N100 and P200 generators for which the current source density was significantly higher when the pulse occurred alone (P) than when the pulse was preceded by a prepulse, namely:  a [P–A] contrast: the pulse alone was compared with the pulse preceded by an ‘‘A’’ prepulse.  a [P–noA] contrast: the pulse alone was compared with the pulse preceded by ‘‘noA’’ prepulse.  a [P–S] contrast: the pulse alone was compared with the pulse preceded by a symbol prepulse.

2.7.2.2. The startle-CPT task: comparisons between conditions. To establish more precisely how the N100 and P200 generators were

Please cite this article in press as: Annic A et al. Effects of stimulus-driven and goal-directed attention on prepulse inhibition of the cortical responses to an auditory pulse. Clin Neurophysiol (2014), http://dx.doi.org/10.1016/j.clinph.2013.12.002

5

A. Annic et al. / Clinical Neurophysiology xxx (2014) xxx–xxx

modulated by attention, we performed a series of comparisons between the various startle-CPT task conditions:  an [S–A] contrast, to identify generators for which the current source density was significantly higher when the pulse was preceded by a symbol prepulse than when the pulse was preceded by an ‘‘A’’ prepulse.  an [A–S] contrast, to identify generators for which the current source density was significantly higher when the pulse was preceded by an ‘‘A’’ prepulse than when the pulse was preceded by a symbol prepulse.  an [S–noA] contrast, to identify generators for which the current source density was significantly higher when the pulse was preceded by a symbol prepulse than when the pulse was preceded by a ‘‘noA’’ prepulse.  a [noA–S] contrast, to identify generators for which the current source density was significantly higher when the pulse was preceded by a ‘‘noA’’ prepulse than when the pulse was preceded by a symbol prepulse.  an [A–noA] contrast to identify generators for which the current source density was significantly higher when the pulse was preceded by an ‘‘A’’ prepulse than when the pulse was preceded by a ‘‘noA’’ prepulse.  a [noA–A] contrast, to identify generators for which the current source density was significantly higher when the pulse was preceded by ‘‘noA’’ prepulse compared with an ‘‘A’’ prepulse. In order to avoid false positives in these tests (while not compromising our ability to evaluate the functional networks), the threshold for statistical significance was set to p < 0.001 for all the above analyses. Talairach Daemon software was used to determine the Talairach coordinates (x, y, z) of the cortical areas involved (Lancaster et al., 1997, 2000). 3. Results All data were normally distributed and are presented as the mean and standard deviation (SD). 3.1. Behavioral performance The mean time reaction was 369 (43) ms, the mean percentage of correct answers was 99% (2.5) and the mean number of false alarms was 0.15 (0.37). 3.2. The AEP in the control task Fig. 2A shows the grand average AEP in the control task. The mean amplitude of the N100 component was 30.7 (20.8) lV, with a latency of 101.9 (10.5) ms. The mean amplitude of the P200 component was 23.7 (12.7) lV, with a latency of 215.3 (36.9) ms. 3.3. PPI of AEP components 3.3.1. The N100 component Fig. 3A shows the mean (SD) percentage PPI of the N100 component of the AEP at each lead interval. With a lead interval of 400 ms, an ANOVA revealed a significant main effect of the prepulse type (F(2,50) = 3.3, p = 0.045). Further comparisons revealed greater PPI after a symbol than after an ‘‘A’’ (t25 = 2, p = 0.04) or a ‘‘noA’’ prepulse (t25 = 2.1, p = 0.03). The difference in PPI between the ‘‘A’’ prepulse and the ‘‘noA’’ prepulse was not significant (t25 = 0.045, p = 0.96). With a lead interval of 1000 ms, there was no effect of the prepulse type.

µV

-30 N100 component

-25 -20 -15 -10 -100

-5

0

100

200

300

0

400 ms

5 10 15 20 µV

-100

-6

-2

A

P200 component

Cz 100

300

500

700 ms

2

6 A prepulse

10

noA prepulse Symbol prepulse

14

B

Fig. 2. Grand averages of AEPs in the control condition (pulse only) at the Cz location (2A) and grand averages of the P300 waveforms at Cz location for each type of prepulse (2B).

3.3.2. The P200 component Fig. 3B shows the mean (SD) percentage PPI of the P200 component of the AEP at each lead interval. With a lead interval of 400 ms, an ANOVA revealed a significant main effect of prepulse type (F(2,50) = 4.5, p = 0.017). Further comparisons revealed greater PPI after an ‘‘A’’ prepulse than after a ‘‘noA’’ prepulse (t25 = 2.7, p = 0.01). There were no significant differences between the ‘‘A’’ prepulse and the symbol prepulse (t25 = 1.4, p = 0.15) or between the ‘‘noA’’ prepulse and the symbol prepulse (t25 = 1.7, p = 0.09). With a lead interval of 1000 ms, the type of prepulse did not have a specific effect. 3.4. The P300 component Grand averages of P300 waveforms on Cz for each type of prepulse are shown in Fig. 2B. The ‘‘A’’ prepulse was associated with a centroparietal P300 with a mean (SD) latency of 420 (35) ms and mean (SD) amplitudes of 0.42 (0.9), 6.45 (4) and 9.73 (4.6) lV at Fz, Cz and Pz, respectively. The symbol prepulse was associated with an earlier P300, with a mean (SD) latency of 386 (28) ms and mean (SD) amplitudes of 2.05 (2.8), 12.22 (6.8) and 13.8 (6.7) lV at Fz, Cz and Pz, respectively. 3.5. AEP source localization data Given that there was no effect of the type of prepulse on PPI of the AEP with a lead interval of 1000 ms, source analyses were only performed on the AEP recorded with a 400 ms lead interval. 3.5.1. The N100 component 3.5.1.1. Generators of N100, as a function of the type of prepulse. As we had observed greater PPI with the symbol prepulse than with

Please cite this article in press as: Annic A et al. Effects of stimulus-driven and goal-directed attention on prepulse inhibition of the cortical responses to an auditory pulse. Clin Neurophysiol (2014), http://dx.doi.org/10.1016/j.clinph.2013.12.002

A. Annic et al. / Clinical Neurophysiology xxx (2014) xxx–xxx

% change from baseline

6

*

60

sublobar areas were either inhibited or had lower current densities. During the startle-CPT task, generators not observed in the control condition were observed (i) in the temporal and sub-lobar regions when an ‘‘A’’ prepulse preceded the pulse, (ii) in the occipital and limbic lobes when a ‘‘noA’’ prepulse preceded the pulse and (iii) in the temporal, parietal and limbic lobes when a symbol prepulse preceded the pulse. Table 1 presents these effects of attention on N100 generators. To evaluate attentional modulation more precisely, we performed [S–A], [A–S], [S–noA] and [noA–S] contrasts (Table 2). Fig. 4 depicts the swLORETA t-test maps for theses contrasts. Since there was no significant difference between the data for ‘‘A’’ and ‘‘noA’’ prepulses, we did not perform [A–noA] or [noA–A] contrasts.

*

50 40 30 20 10 0 400

1000

% change from baseline

A 60

noA

A

symbol

*

50 40

3.5.2. The P200 component of the AEP 3.5.2.1. Generators of P200 as a function of the type of prepulse. We performed the same analysis for P200 as for N100. Given that we found greater PPI for an ‘‘A’’ prepulse than for an ‘‘noA’’ prepulse and the absence of a significant difference between a symbol prepulse and both ‘‘A’’ and ‘‘noA’’ prepulses, only the results obtained with A and ‘‘noA’’ prepulses are presented here. The cortical areas involved are listed in Table 3. Our data showed that several areas in the temporal, frontal, parietal, occipital and limbic lobes and in the sublobar regions were activated during the control and the startle-CPT tasks.

30 20 10 0

400

1000 A

noA

symbol

B

Fig. 3. Mean inhibition of the N100 component (3A) and the P200 component (3B) of the AEP at 400 and 1000 ms lead intervals for ‘‘A’’, ‘‘noA’’ and symbol prepulses. Asterisks indicate significant differences (p < 0.05). Standard error bars are included.

the ‘‘A’’ and ‘‘noA’’ prepulses, we performed a [peak–baseline] contrast in order to identify cortical generators of the responses to pulses preceded by ‘‘A’’, ‘‘noA’’ and symbol prepulses. The cortical areas involved are listed in Table 1: several areas in the temporal, frontal, parietal, occipital and limbic lobes and in the sublobar regions were activated during the control task and the startle-CPT tasks. 3.5.1.2. Modulation of N100 generators by attention. In order to study the attentional modulation of current densities, we first compared the localizations of the N100 generators in the control and startle-CPT tasks by performing [control–startle-CPT task] contrasts. The results of these comparisons are presented in the Table 1. There were three types of effects: (i) inhibition of the generator (when significant swLORETA activation was found in the control condition but no more in the startle-CPT condition). (ii) reduction in current density (i.e., a lower current density in the startle-CPT condition than in the control condition). (iii) lack of an effect (i.e., no difference between the startle-CPT task and the control condition). When the pulse was preceded by a prepulse, most of the sources in the temporal, frontal, parietal, occipital, limbic and

3.5.2.2. Attentional modulation of P200 generators. In order to study the attentional modulation of current densities, we first compared the localization of the P200 generators in the control and startleCPT tasks by performing a [control–startle-CPT task] contrast (Table 3). When the pulse was preceded by a prepulse, most sources in the temporal, frontal, parietal, occipital, limbic and sublobar areas were either inhibited or had a lower current density. The various effects of attention on P200 generators (namely inhibition, lower current density or the lack of an effect) are summarized in Table 3. To evaluate modulation by focused attention more precisely, we performed [A–noA] and [noA–A] contrasts (Table 4). Fig. 5 depicts the swLORETA t-test maps for these contrasts.

4. Discussion 4.1. Inhibition of cortical responses In the present study, we sought to determine the role of attention in the sensory gating process. By studying changes in the cortical responses to a pulse (which corresponds to irrelevant information) preceded by a prepulse on which attention was focused, we were able to monitor the inhibition of irrelevant information. Firstly, our data showed that with a lead interval of 400 ms, greater inhibition of cortical responses to the pulse was observed following the to-be-attended prepulse (the ‘‘A’’ prepulse) and the unexpected prepulse (the symbol prepulse) than following the to-be-ignored prepulse (the ‘‘noA’’ prepulse). Secondly, the effects of attention on PPI differed as a function of the AEP component: the N100 component was inhibited more by an unexpected prepulse than by a to-be-attended prepulse, whereas the P200 component was inhibited more by a to-be-attended prepulse than by a to-be ignored prepulse. Thirdly, with a lead interval of 1000 ms, the type of prepulse did not have a specific effect on inhibition of cortical responses to the pulse. As expected, the allocation of attentional resources (as evidenced by the characteristics of P300) depended on the type of prepulse.

Please cite this article in press as: Annic A et al. Effects of stimulus-driven and goal-directed attention on prepulse inhibition of the cortical responses to an auditory pulse. Clin Neurophysiol (2014), http://dx.doi.org/10.1016/j.clinph.2013.12.002

A. Annic et al. / Clinical Neurophysiology xxx (2014) xxx–xxx

7

Table 1 Cortical generators of the N100 component in control and startle-CPT tasks and significant swLORETA activation for the N100 component when comparing control and startle CPT-tasks. For each column describing a type of prepulse, subcolumn 1 represents the localization of generators within a timeframe around the N100 peak for the control AEP (pulse alone: P), with the corresponding Brodmann area (BA); subcolumn 2 represents the localization when the pulse is preceded by an ‘‘A’’ prepulse (A), a ‘‘noA’’ prepulse (noA) or a symbol prepulse (S) with a [peak–baseline] contrast, with ‘‘N’’ indicating significant swLORETA activation (p < 0.001); subcolumn 3 represents significant swLORETA activation (‘X’) when comparing control and startle CPT-tasks (p < 0.001); subcolumn 4: a color code indicates how the current density changed at each localization during the startle-CPT task. Grey indicates there was no change, compared with the control condition (pulse alone: P); orange indicates that the current density was significantly lower in the prepulse condition than in the control condition; green indicates that generators not observed in the control condition became significant; red indicates that all the generators observed in the control condition were no more observed when a prepulse was present. The prepulse–pulse interval was 400 ms.

We showed that the inhibition of cortical responses produced by a stimulus that is irrelevant (with respect to the ongoing task) is modulated by attention. Our results demonstrate that

goal-directed and stimulus-driven attention have specific effects on PPI. Our original experimental approach enabled us to distinguish between these two effects. In fact, we monitored the

Please cite this article in press as: Annic A et al. Effects of stimulus-driven and goal-directed attention on prepulse inhibition of the cortical responses to an auditory pulse. Clin Neurophysiol (2014), http://dx.doi.org/10.1016/j.clinph.2013.12.002

8

A. Annic et al. / Clinical Neurophysiology xxx (2014) xxx–xxx

Table 2 Effects of focused attention on the N100 generators during a startle-CPT task. We performed [S–A], [A–S], [S–noA] and [noA–S] contrast analyses. S: the pulse was preceded by a symbol prepulse; A: the pulse was preceded by an ‘‘A’’ prepulse; noA: the pulse was preceded by a ‘‘noA’’ prepulse. The prepulse–pulse interval was 400 ms. Each ‘X’ indicates significant swLORETA activation (p < 0.001). Brain regions

[S–A]

Temporal lobe Middle temporal gyrus Superior temporal gyrus

X X

Frontal lobe Medial frontal gyrus Precentral gyrus Inferior frontal gyrus Superior frontal gyrus Middle frontal gyrus

[A–S]

[S–noA] X X

X X X X

X X X X

Parietal lobe Precuneus Superior parietal lobule Inferior parietal lobule Postcentral gyrus

X X

X

Occipital lobe Middle occipital gyrus Cuneus Lingual gyrus

X X X

X X

Limbic lobe Cingulate gyrus Parahippocampal gyrus Uncus

[noA–S]

X

X X

X

X X

Sublobar regions Thalamus Lentiform nucleus Insula Caudate body

attentional resources allocated to each type of prepulse by recording the P300 component of the event-related potential; this contrasts with previous studies involving an active PPI paradigm but in which attention was monitored through behavioral parameters only (Hazlett et al., 2001; Rissling et al., 2005, 2007; Hazlett et al., 2008b) and/or in which stimulus-driven attention was not investigated (Dawson et al., 1993; Hazlett et al., 2001; Rissling et al., 2005, 2007). With a lead interval of 400 ms, inhibition of the AEP’s N100 component was greater after an unexpected prepulse than after a to-be-attended or a to-be-ignored prepulse, whereas inhibition of the AEP’s P200 component was greater after a to-be-attended prepulse than after a to-be-ignored prepulse. Our first hypothesis (i.e., inhibition of cortical responses to the pulse is dependent on the type of prepulse, with a greater inhibition following a prepulse on which attention was focused than following a to-be-ignored prepulse) was thus confirmed. In contrast, our second hypothesis (i.e., PPI of cortical responses would be greater following a to-be-attended than following an unexpected prepulse) was only partially confirmed. We found that the effects of goal-directed attention and stimulus-driven attention on PPI differed for the P200 and N100 component of the AEP. Inhibition of the P200 component was greater after a to-be-attended prepulse than after a to-be ignored prepulse, whereas inhibition of the N100 component was greater after an unexpected prepulse than after a to-be attended prepulse. This suggests that stimulus-driven attention influences sensory gating earlier in the process (in the time window around N100) than goal-directed attention does. In fact, N100 is primarily an exogenous component of the AEP and is sensitive to the physical characteristics of the auditory stimulus. The amplitude of N100 is strongly dependent on the stimulus’s rise time, intensity and duration (Rosburg et al., 2008). We can therefore assume that stimulus-driven attention specifically influences PPI by modulating the irrelevant stimulus’s characteristics.

Goal-directed attention had an influence on PPI later in the process (in the time window around P200). Several studies have shown that P200 and N100 are independent, distinct components (Crowley and Colrain, 2004). In terms of its functional significance, the P200 component evoked by passive listening may reflect allocation of attention and the initial conscious experience of a stimulus (Näätänen, 1992). Garcia-Larrea et al. (1992) suggested that P200 is required (but not sufficient) for generation of a P300 component. In other words, a P300 could only be evoked if the cognitive processes reflected by P200 leads to the identification of the stimulus as a target. If not, cognitive evaluation of the stimulus is terminated and no P300 is elicited. Schirmer and Kotz (2006) considered that the P200 component reflects the integration of complex acoustic cues and enables the subject to gauge the significance of stimuli. Taken as a whole, these observations suggest that P200 reflects cognitive or high-level processes leading to sensory integration of auditory stimulus. We can therefore assume that goal-directed attention specifically modulates the cognitive evaluation of an irrelevant stimulus and thus influences PPI. With a lead time of 1000 ms, PPI of the AEP was also observed but the type of attention did not have a specific influence on cortical responses. This observation agrees with previous studies showing that at long lead intervals, sensorimotor gating is not modulated by controlled attentional processes. Indeed, Hazlett et al. (2001) and Rissling et al. (2007) reported that during a startle-CPT task with a lead interval of 1200 ms, there were no differences in eye-blink PPI when comparing a to-be-attended visual prepulse with a to-be-ignored visual prepulse. We observed this same phenomenon (the absence of a differential effect of attention with a long lead interval) for cortical responses. 4.2. Attentional modulation of cortical generators of the AEP 4.2.1. N100 sources Previous fMRI and sLORETA (standardized low resolution tomography) studies have suggested that the N100 generators are located in auditory cortical areas (i.e., the temporal lobe) and in other regions (namely the limbic, frontal, occipital and parietal lobes and the thalamus (Mayhew et al., 2010; Zhang et al., 2011)). In the control task, our results are consistent with these previous reports – even though a contribution by the lentiform nucleus has never previously been observed. This is probably due to our use of swLORETA technique, which provides an accurate reconstruction of deep current sources (Palmero-Soler et al., 2007). During the startle-CPT task (and regardless of the type of prepulse) a significant lower current density (relative to the control task) was observed at almost all source localizations. This finding is consistent with a lower AEP amplitude when the startling stimulus was preceded by a prepulse. However, the magnitude of the reduction in current density for N100 generators differed from one cortical area to another. Our data suggest that stimulus-driven attention and goal-directed attention have different effects on the current density. When stimulus-driven attention was engaged, PPI of the N100 was greater than when goal-directed attention was engaged. Our current density analysis revealed greater activation of the temporal and occipital areas and the inferior parietal lobule in this condition. It has been shown that the temporoparietal junction (which includes the superior temporal gyrus and the inferior parietal lobule) mediates stimulus-driven attention (Shomstein et al., 2010). Our results suggest that these areas influence the N100 generators. The involvement of the occipital cortex is probably related to visual processing of the unexpected visual prepulse (due to its salience). When an unexpected prepulse preceded the pulse, we observed generators in areas that lacked them in the control task: the post-

Please cite this article in press as: Annic A et al. Effects of stimulus-driven and goal-directed attention on prepulse inhibition of the cortical responses to an auditory pulse. Clin Neurophysiol (2014), http://dx.doi.org/10.1016/j.clinph.2013.12.002

A. Annic et al. / Clinical Neurophysiology xxx (2014) xxx–xxx

central gyrus, fusiform gyrus, parahippocampal gyrus and uncus. Bocquillon et al. (2011) have shown that the postcentral gyrus is involved in stimulus-driven attention. We observed a higher current density in the frontal lobe and the precuneus when goal-directed attention was engaged than in the other conditions. Relative to the control task, additional generators were found in the fusiform gyrus and the caudate nucleus. Goal-directed attention involves a dorsal frontoparietal network, the core regions of which comprise the dorsal parietal cortex (namely the intraparietal sulcus and the superior parietal lobule) and the dorsal frontal cortex (along the precentral sulcus, near or at the frontal eye field) (Corbetta and Shulman, 2002). Use of LORETA and swLORETA techniques for P300 source localization of P300 has demonstrated that goal-directed attention involves the superior parietal lobule, the prefrontal cortex (medial and inferior gyri), the premotor cortex (precentral gyrus) (Bocquillon et al., 2011) and the precuneus (Volpe et al., 2007). These areas influence the N100 generators. Moreover, we found additional generators (namely in the fusiform gyrus and the body of the caudate nucleus). Activation of the fusiform gyrus has already been observed in response to a stimulus requiring goal-directed attention (Volpe et al., 2007). In an fMRI study with an active auditory PPI paradigm, Hazlett et al. (2008a) reported that greater PPI of the startle eye-blink during an attended PPI condition was associated with a greater activation in the caudate and prefrontal cortex. Although our experimental conditions

9

differed (since Hazlett et al. studied the role of the frontostriatal and thalamic circuitry in the modulation of PPI with a 120 ms lead interval, rather than cortical generators), the two sets of results both reveal a role of the frontal lobe and caudate in attentional modulation of PPI – essentially when attention is goal-directed. 4.2.2. P200 sources There are fewer literature data on P200 generators than on N100 generators. Most studies indicate that the P200 is generated in temporal associative auditory regions (Hari et al., 1980; Perrault and Picton, 1984; Godey et al., 2001), although the involvement of non-temporal regions (such as the frontal cortex (McCarley et al., 1991) and the inferior parietal lobe (Knight et al., 1988)) has been suggested in lesion studies. Using sLORETA, Jung et al. (2010) tried to localize the sources of auditory N100 and P200 components by using a 32-channel recording in epileptic patients by comparing the source localization data before and after treatment with an antiepileptic. Following treatment, the current density for P200 was significantly lower in the parieto-occipital, orbitofrontal and prefrontal regions. More recently, De Pascalis et al. (2013) used sLORETA to identify P200 sources in the superior parietal lobule and the precuneus. However, the fact that only 22 channels were recorded limited the accuracy of spatial localization. In summary, we consider that the P200 generators are located in auditory areas in the cortex (i.e. the temporal lobe) and frontal, parietal and

Fig. 4. Comparisons of N100 generators with swLORETA t-test maps (horizontal, sagittal and coronal plane images) according conditions: [A–S] contrast (4A), [S–A] contrast (4B), [noA–S] contrast (4C) and [S–noA] contrast (4D) (p < 0.001). Significant generators are displayed in green for the [A–S] contrast, in red for the [S–A] contrast, in violet for the [noA–S] contrast and in blue for the [S–noA] contrast. In the A condition, the pulse is preceded by an ‘‘A’’ prepulse. In the S condition, the pulse is preceded by a symbol prepulse. In the noA condition, the pulse is preceded by a ‘‘noA’’ prepulse.

Please cite this article in press as: Annic A et al. Effects of stimulus-driven and goal-directed attention on prepulse inhibition of the cortical responses to an auditory pulse. Clin Neurophysiol (2014), http://dx.doi.org/10.1016/j.clinph.2013.12.002

10

A. Annic et al. / Clinical Neurophysiology xxx (2014) xxx–xxx

Table 3 Cortical generators of the P200 component in control and startle-CPT tasks and significant swLORETA activation for P200 component between control and startle CPT-tasks. For each column describing a type of prepulse, subcolumn 1 represents the localization of generators within a timeframe around the P200 peak for the control AEP (pulse alone: P), with the corresponding Brodmann area (BA); subcolumn 2 represents the localization when the pulse is preceded by an ‘‘A’’ prepulse (A) or a ‘‘noA’’ prepulse (noA) with a [peak– baseline] contrast, with ‘‘N’’ indicating significant swLORETA activation (p < 0.001); subcolumn 3 represents significant swLORETA activation (‘X’) when comparing control and startle CPT-tasks (p < 0.001); subcolumn 4: a color code indicates how the current density changed at each localization during the startle-CPT task. Grey indicates there was no change, compared with the control condition (pulse alone: P); orange indicates that the current density was significantly lower in the prepulse condition than in the control condition; red indicates that all the generators observed in the control condition were no more observed when a prepulse was present. The prepulse–pulse interval was 400 ms.

Please cite this article in press as: Annic A et al. Effects of stimulus-driven and goal-directed attention on prepulse inhibition of the cortical responses to an auditory pulse. Clin Neurophysiol (2014), http://dx.doi.org/10.1016/j.clinph.2013.12.002

A. Annic et al. / Clinical Neurophysiology xxx (2014) xxx–xxx

occipital regions. In our control task, we found sources not only in these same areas but also in the cingulate and parahippocampal gyri, the thalamus, the insula and the body of the caudate nucleus. Hence, we confirmed the existence of previously described sources and also found additional, deeper generators – probably because our EEG was recorded at 128 scalp sites and swLORETA enabled us to reconstruct deep current sources more accurately (PalmeroSoler et al., 2007). Moreover, the stimulation conditions in our control task slightly differed from those in previous studies, since visual stimuli that did not require any particular processing were also presented. During the startle-CPT task, we observed a significant lower current density at almost all source locations (relative to the Table 4 Effects of focused attention on the P200 generators during startle-CPT task. We performed [A–noA] and [noA–A] contrast analyses. A: the pulse was preceded by an ‘‘A’’ prepulse; noA: the pulse was preceded by a ‘‘noA’’ prepulse. The prepulse–pulse interval was 400 ms. Each ‘X’ indicates significant swLORETA activation (p < 0.001). Brain regions

[A–noA]

Temporal lobe Middle temporal gyrus Superior temporal gyrus

X

Frontal lobe Medial frontal gyrus Precentral gyrus Inferior frontal gyrus Superior frontal gyrus Middle frontal gyrus

X

X

X X

Parietal lobe Precuneus Superior parietal lobule Inferior parietal lobule Postcentral gyrus Supramarginal gyrus

X X

Occipital lobe Inferior occipital gyrus Cuneus Lingual gyrus Limbic lobe Cingulate gyrus Parahippocampal gyrus Sublobar regions Thalamus Lentiform nucleus Insula Caudate body

[noA–A]

X X X

X

X X

11

control task). Below, we only discuss the influence of goal-directed attention on P200 generators because stimulus-driven attention did not have any effect on PPI of this component. The effects of goal-directed attention on modulation of P200 component were less clear than those seen for the N100 component – probably because P200 occurs later after the visual stimulus occurrence (at least 600 ms). As described for modulation of N100 generator, we found less current density in occipital regions when attention was goal-directed. The current density was lower in the caudate body for P200 component in the startle-CPT task than in the control task. We found that when attention was goal-directed, the caudate body is involved in modulation of N100 generator but not in modulation of the P200 generator given the reduced current density in this area. This suggests that the caudate’s influence on modulation of PPI by goal-directed attention occurs early – within the first 100 ms after the stimulus. In contrast to the data on modulation of the N100 generator, we observed a higher current density in the parahippocampal gyrus when attention was goal-directed. This region is known to be involved in goal-directed attention. Volpe et al. (2007) and Ota et al. (2013) have used a passive acoustic PPI paradigm to demonstrate the parahippocampal region’s involvement in sensorimotor gating. Our results revealed an influence of this area on the modulation of PPI of cortical responses by goal-directed attention. The influence occurred at about 200 ms post-stimulus. Our study had several limitations. Although our study population comprised both men and women, we lacked data on the latter’s hormonal status. In fact, Jovanovic et al. (2004) have shown that PPI varies according to the phase of the menstrual cycle. However, most studies of PPI do not exclude women and have either failed to evaluate a gender effect (Rissling et al., 2005; Kedzior et al., 2006; Molina et al., 2009; Scholes and Martin-Iverson, 2009; Larrauri et al., 2012) or found that a gender effect was not present (Stojanov et al., 2003; Ashare et al., 2007; Kedzior et al., 2007; Kedzior and Martin-Iverson, 2007; Rissling et al., 2007). Secondly, we did not check on the self-reported absence of nicotine and cannabis use by assaying urine or blood samples. However, self-reporting of cannabis use is a validated way of evaluating actual consumption (Martin et al., 1988) and nicotine can be detected in the urine samples of most of non-smokers (Matsukura et al., 1979; Baselt, 2000). Thirdly, we used the same MRI template (Colin27) (rather than individual MRI data) for swLORETA source localization in all participants. However, the use of a standard MRI template increases the signal-to-noise ratio

Fig. 5. Comparisons of P200 generators with swLORETA t-test maps (horizontal, sagittal and coronal plane images) according conditions: [A–noA] contrast (5A) and [noA–A] contrast (5B) (p < 0.001). Significant generators are displayed in yellow for the [A–noA] contrast and in cyan for the [noA–A] contrast. In the A condition, the pulse is preceded by an ‘‘A’’ prepulse. In the noA condition, the pulse is preceded by a ‘‘noA’’ prepulse.

Please cite this article in press as: Annic A et al. Effects of stimulus-driven and goal-directed attention on prepulse inhibition of the cortical responses to an auditory pulse. Clin Neurophysiol (2014), http://dx.doi.org/10.1016/j.clinph.2013.12.002

12

A. Annic et al. / Clinical Neurophysiology xxx (2014) xxx–xxx

(Holmes et al., 1998) and means that brain normalization for transforming individual brain images into a standard anatomical space is not necessary. Indeed, normalization would have distorted the images and made the results less precise. Moreover, our participants were young healthy subjects who were very unlikely to be suffering from brain atrophy or morphological abnormalities. 5. Conclusion In conclusion, the modulation of PPI by attention is influenced by both stimulus-driven and goal-directed attention. By studying the PPI of N100 and P200 cortical components generated by an irrelevant stimulus (the pulse), we found that stimulus-driven and goal-directed attention have specific effects on the inhibition process. Stimulus-driven attention and goal-directed attention influenced PPI through modulation of the irrelevant stimulus’s sensory characteristics and cognitive evaluation, respectively. Our results highlighted brain areas involved in the stimulus-driven and goal-directed attentional modulation of N100 and P200 sources. For N100 sources in particular, we observed an influence of the fusiform gyrus, parahippocampal gyrus and uncus when stimulus-driven attention was engaged and an influence of the caudate body when goal-directed attention was engaged. As PPI has been shown to be a useful index of sensory gating impairments in basal ganglia disorders (e.g., schizophrenia and Parkinson’s disease (Perriol et al., 2005; Hazlett et al., 2008a,b)), our active paradigm may be of great value for more precise investigations of the role of attention in these impairments. Moreover, studying PPI of auditory cortical responses seems particularly relevant in conditions in which the amplitude of the startle reflex decreases (as in the elderly (Ellwanger et al., 2003) and patients with basal ganglia disorders). Financial interests None. Acknowledgment The authors wish to thank David Fraser for helpful comments on the manuscript’s English. References Abduljawad KA, Langley RW, Bradshaw CM, Szabadi E. Effects of clonidine and diazepam on prepulse inhibition of the acoustic startle response and the N1/P2 auditory evoked potential in man. J Psychopharmacol 2001;15:237–42. Ashare RL, Hawk Jr LW, Mazzullo RJ. Motivated attention: incentive effects on attentional modification of prepulse inhibition. Psychophysiology 2007;44: 839–45. Baselt RC. Disposition of toxic drugs and chemicals in man. 5th ed. Foster city, California: Chemical Toxicology Institute; 2000. Bocquillon P, Bourriez JL, Palmero-Soler E, Betrouni N, Houdayer E, Derambure P, et al. Use of swLORETA to localize the cortical sources of target- and distracterelicited P300 components. Clin Neurophysiol 2011;122:1991–2002. Campbell LE, Hughes M, Budd TW, Cooper G, Fulham WR, Karayanidis F, et al. Primary and secondary neural networks of auditory prepulse inhibition: a functional magnetic resonance imaging study of sensorimotor gating of the human acoustic startle response. Eur J Neurosci 2007;26:2327–33. Corbetta M, Shulman GL. Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 2002;3:201–15. Crowley KE, Colrain IM. A review of the evidence for P2 being an independent component process: age, sleep and modality. Clin Neurophysiol 2004;115: 732–44. Davis H, Zerlin S. Acoustic relations of the human vertex potential. J Acoust Soc Am 1966;39:109–16. Dawson ME, Hazlett EA, Filion DL, Nuechterlein KH, Schell AM. Attention and schizophrenia: impaired modulation of the startle reflex. J Abnorm Psychol 1993;102:633–41.

De Pascalis V, Cozzuto G, Russo E. Effects of personality trait emotionality on acoustic startle response and prepulse inhibition including N100 and P200 event-related potential. Clin Neurophysiol 2013;124:292–305. Desimone R, Duncan J. Neural mechanisms of selective visual attention. Annu Rev Neurosci 1995;18:193–222. Donchin E, Miller GA, Farwell LA. The endogenous components of the event-related potential–a diagnostic tool? Prog Brain Res 1986;70:87–102. Ellwanger J, Geyer MA, Braff DL. The relationship of age to prepulse inhibition and habituation of the acoustic startle response. Biol Psychol 2003;62:175–95. Evans AC, Collins DL. 3D statistical neuroanatomical models from 305 MRI volumes. In: Proceedings of IEEE-nuclear science symposium and medical imaging conference. 1993. p.1813–1817.. Filion DL, Dawson ME, Schell AM. Modification of the acoustic startle-reflex eyeblink: a tool for investigating early and late attentional processes. Biol Psychol 1993;35:185–200. Filion DL, Dawson ME, Schell AM. The psychological significance of human startle eyeblink modification: a review. Biol Psychol 1998;47:1–43. Garcia-Larrea L, Lukaszewicz AC, Mauguiere F. Revisiting the oddball paradigm. Non-target vs neutral stimuli and the evaluation of ERP attentional effects. Neuropsychologia 1992;30:723–41. Geselowitz DB. On bioelectric potentials in an inhomogeneous volume conductor. Biophys J 1967;7:1–11. Godey B, Schwartz D, de Graaf JB, Chauvel P, Liegeois-Chauvel C. Neuromagnetic source localization of auditory evoked fields and intracerebral evoked potentials: a comparison of data in the same patients. Clin Neurophysiol 2001;112:1850–9. Hari R, Aittoniemi K, Jarvinen ML, Katila T, Varpula T. Auditory evoked transient and sustained magnetic fields of the human brain. Localization of neural generators. Exp Brain Res 1980;40:237–40. Hazlett EA, Dawson ME, Schell AM, Nuechterlein KH. Attentional stages of information processing during a continuous performance test: a startle modification analysis. Psychophysiology 2001;38:669–77. Hazlett EA, Buchsbaum MS, Zhang J, Newmark RE, Glanton CF, Zelmanova Y, et al. Frontal–striatal–thalamic mediodorsal nucleus dysfunction in schizophreniaspectrum patients during sensorimotor gating. Neuroimage 2008a;42: 1164–77. Hazlett EA, Dawson ME, Schell AM, Nuechterlein KH. Probing attentional dysfunctions in schizophrenia: startle modification during a continuous performance test. Psychophysiology 2008b;45:632–42. Hillyard SA, Picton TW. Event-related potentials and selective information processing in man. In: Desmedt J, editor. Prog Clin Neurophys. Basel: Karger; 1979. Holmes CJ, Hoge R, Collins L, Woods R, Toga AW, Evans AC. Enhancement of MR images using registration for signal averaging. J Comput Assist Tomogr 1998; 22:324–33. Inui K, Tsuruhara A, Kodaira M, Motomura E, Tanii H, Nishihara M, et al. Prepulse inhibition of auditory change-related cortical responses. BMC Neurosci 2012; 13:135. Jovanovic T, Szilagyi S, Chakravorty S, Fiallos AM, Lewison BJ, Parwani A, et al. Menstrual cycle phase effects on prepulse inhibition of acoustic startle. Psychophysiology 2004;41:401–6. Jung KY, Cho JW, Joo EY, Kim SH, Choi KM, Chin J, et al. Cognitive effects of topiramate revealed by standardised low-resolution brain electromagnetic tomography (sLORETA) of event-related potentials. Clin Neurophysiol 2010; 121:1494–501. Kastner S, Ungerleider LG. Mechanisms of visual attention in the human cortex. Annu Rev Neurosci 2000;23:315–41. Kedzior KK, Martin-Iverson MT. Attention-dependent reduction in prepulse inhibition of the startle reflex in cannabis users and schizophrenia patients–a pilot study. Eur J Pharmacol 2007;560:176–82. Kedzior KK, Koch M, Basar-Eroglu C. Prepulse inhibition (PPI) of auditory startle reflex is associated with PPI of auditory-evoked theta oscillations in healthy humans. Neurosci Lett 2006;400:246–51. Kedzior KK, Koch M, Basar-Eroglu C. Auditory-evoked EEG oscillations associated with prepulse inhibition (PPI) of auditory startle reflex in healthy humans. Brain Res 2007;1163:111–8. Knight RT, Scabini D, Woods DL, Clayworth C. The effects of lesions of superior temporal gyrus and inferior parietal lobe on temporal and vertex components of the human AEP. Electroencephalogr Clin Neurophysiol 1988;70:499–509. Lancaster JL, Rainey LH, Summerlin JL, Freitas CS, Fox PT, Evans AC, et al. Automated labeling of the human brain: a preliminary report on the development and evaluation of a forward-transform method. Hum Brain Mapp 1997;5: 238–42. Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas CS, Rainey L, et al. Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp 2000;10:120–31. Larrauri JA, Rosenthal MZ, Levin ED, McClernon FJ, Schmajuk NA. Effects of unexpected changes in visual scenes on the human acoustic startle response and prepulse inhibition. Behav Processes 2012;89:1–7. Martin GW, Wilkinson DA, Kapur BM. Validation of self-reported cannabis use by urine analysis. Addict Behav 1988;13:147–50. Matsukura S, Sakamoto N, Seino Y, Tamada T, Matsuyama H, Muranaka H. Cotinine excretion and daily cigarette smoking in habituated smokers. Clin Pharmacol Ther 1979;25:555–61. Mayhew SD, Dirckx SG, Niazy RK, Iannetti GD, Wise RG. EEG signatures of auditory activity correlate with simultaneously recorded fMRI responses in humans. Neuroimage 2010;49:849–64.

Please cite this article in press as: Annic A et al. Effects of stimulus-driven and goal-directed attention on prepulse inhibition of the cortical responses to an auditory pulse. Clin Neurophysiol (2014), http://dx.doi.org/10.1016/j.clinph.2013.12.002

A. Annic et al. / Clinical Neurophysiology xxx (2014) xxx–xxx McCarley RW, Faux SF, Shenton ME, Nestor PG, Adams J. Event-related potentials in schizophrenia: their biological and clinical correlates and a new model of schizophrenic pathophysiology. Schizophr Res 1991;4:209–31. Molina V, Montes C, Tamayo P, Villa R, Osuna MI, Perez J, et al. Correlation between prepulse inhibition and cortical perfusion during an attentional test in schizophrenia. A pilot study. Prog Neuropsychopharmacol Biol Psychiatry 2009;33:53–61. Näätänen R. Attention and brain function. Hillsdale, NJ: Erlbaum; 1992. Nichols TE, Holmes AP. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 2002;15:1–25. Oostenveld R, Praamstra P. The five percent electrode system for high-resolution EEG and ERP measurements. Clin Neurophysiol 2001;112:713–9. Ota M, Sato N, Matsuo J, Kinoshita Y, Kawamoto Y, Hori H, et al. Multimodal image analysis of sensorimotor gating in healthy women. Brain Res 2013; 1499:61–8. Palmero-Soler E, Dolan K, Hadamschek V, Tass PA. SwLORETA: a novel approach to robust source localization and synchronization tomography. Phys Med Biol 2007;52:1783–800. Pascual-Marqui RD. Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 2002;2:5–12. Perlstein WM, Fiorito E, Simons RF, Graham FK. Lead stimulation effects on reflex blink, exogenous brain potentials, and loudness judgments. Psychophysiology 1993;30:347–58. Perlstein WM, Simons RF, Graham FK. Prepulse effects as a function of cortical projection system. Biol Psychol 2001;56:83–111. Perrault N, Picton TW. Event-related potentials recorded from the scalp and nasopharynx. I. N1 and P2. Electroencephalogr Clin Neurophysiol 1984;59: 177–94. Perriol MP, Dujardin K, Derambure P, Marcq A, Bourriez JL, Laureau E, et al. Disturbance of sensory filtering in dementia with Lewy bodies: comparison

13

with Parkinson’s disease dementia and Alzheimer’s disease. J Neurol Neurosurg Psychiatry 2005;76:106–8. Rissling AJ, Dawson ME, Schell AM, Nuechterlein KH. Effects of perceptual processing demands on startle eyeblink modification. Psychophysiology 2005;42:440–6. Rissling AJ, Dawson ME, Schell AM, Nuechterlein KH. Effects of cigarette smoking on prepulse inhibition, its attentional modulation, and vigilance performance. Psychophysiology 2007;44:627–34. Rosburg T, Boutros NN, Ford JM. Reduced auditory evoked potential component N100 in schizophrenia–a critical review. Psychiatry Res 2008;161:259–74. Schirmer A, Kotz SA. Beyond the right hemisphere: brain mechanisms mediating vocal emotional processing. Trends Cogn Sci 2006;10:24–30. Scholes KE, Martin-Iverson MT. Relationships between prepulse inhibition and cognition are mediated by attentional processes. Behav Brain Res 2009;205:456–67. Shomstein S, Lee J, Behrmann M. Top-down and bottom-up attentional guidance: investigating the role of the dorsal and ventral parietal cortices. Exp Brain Res 2010;206:197–208. Squires NK, Squires KC, Hillyard SA. Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. Electroencephalogr Clin Neurophysiol 1975;38:387–401. Stojanov W, Karayanidis F, Johnston P, Bailey A, Carr V, Schall U. Disrupted sensory gating in pathological gambling. Biol Psychiatry 2003;54:474–84. Swerdlow NR, Geyer MA, Braff DL. Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology (Berl) 2001;156:194–215. Volpe U, Mucci A, Bucci P, Merlotti E, Galderisi S, Maj M. The cortical generators of P3a and P3b: a LORETA study. Brain Res Bull 2007;73:220–30. Zhang F, Deshpande A, Benson C, Smith M, Eliassen J, Fu QJ. The adaptive pattern of the auditory N1 peak revealed by standardized low-resolution brain electromagnetic tomography. Brain Res 2011;1400:42–52.

Please cite this article in press as: Annic A et al. Effects of stimulus-driven and goal-directed attention on prepulse inhibition of the cortical responses to an auditory pulse. Clin Neurophysiol (2014), http://dx.doi.org/10.1016/j.clinph.2013.12.002

Effects of stimulus-driven and goal-directed attention on prepulse inhibition of the cortical responses to an auditory pulse.

Inhibition by a prepulse (prepulse inhibition, PPI) of the response to a startling acoustic pulse is modulated by attention. We sought to determine wh...
2MB Sizes 0 Downloads 0 Views