Attentional influence on the P50 component of the auditory event-related brain potential

doi:10.1016/0167-8760(92)90011-Y

International Journal of Psychophysiology

Volume 12, Issue 2, March 1992, Pages 197-209

https://doi.org/10.1016/0167-8760(92)90011-Y Get rights and content

Abstract

To determine if attentional factors influence the suppression of the auditory P50 in a conditioning-testing paradigm, known as the ‘sensory gating’ effect, we tested 10 healthy young adults in four experimental conditions. The first condition was the traditional passive conditioning-testing paradigm in which a pair of identical auditory clicks is administered at an interstimulus interval fixed at 500 ms. The effect of interest is a reduction of P50 amplitude in response to the second stimulus. In the next condition, the second stimulus could be one of two possible frequencies and subjects were required to count one and to ignore the other. The third and fourth experimental conditions involved a motor response. In the third condition, subjects were required to make a unimanual button press to the occurrence of the second stimulus. In the fourth condition, subjects were required to discriminate among two possible second stimuli, and make a unimanual button press to the occurrence of the designated stimulus. Subjects also completed four matched blocks of single stimulus (i.e., unpaired) presentations to provide a baseline for assessing the effect of the warning stimulus on the evoked response. We found, in agreement with previous results, that passive exposure to the paired stimuli produced a suppression of P50 amplitude to the second stimulus. However, we also found that suppression of P50 amplitude was not evident when subjects selectively counted the designated stimuli, and was reduced in magnitude when a simple motor response was required and when a selective motor response was based on stimulus discrimination. In addition, we observed that the amplitude of the P50 was larger with unpaired single stimuli than it was either with the first or second stimulus of a pair, regardless of processing demands. Furthermore, variations in processing demands did not affect P50 amplitude when a single stimulus was presented. This pattern of results suggests that the ‘sensory gating’ effect is not a simple ‘hard-wired’ inhibitory phenomenon. Rather, it may be one manifestation of an attention regulation process that is activated by a warning stimulus and has either inhibitory or excitatory effects on neural transmission, determined by variations in processing demands. Presentation of a warning stimulus may have an additional, unselective suppressing effect, operating independently of this attention regulating process.

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Citation Excerpt :
In non-invasive, scalp EEG/MEG recordings, the most reliable finding has been that the N100 − an auditory ERP component that peaks at about 100 msec from stimulus onset (Näätänen & Picton, 1987; Pratt, 2011) and likely has its primary source generator in the auditory cortex (Giard et al., 2000; Godey et al., 2001; Näätänen & Picton, 1987; Neelon et al., 2006; Vaughan & Ritter, 1970) − might be enhanced by attentional focus (Hackley et al., 1990; Hansen and Hillyard, 1980, 1983; Hillyard et al., 1973; Luck & Kappenman, 2012; Näätänen et al., 1981; Rosburg et al., 2009; Woldorff et al., 1993; Woldorff & Hillyard, 1991). In addition to N100, there were some reports that attention-driven enhancement can already be found for the P50 auditory ERP component (Guterman et al., 1992; Wan et al., 2008; Woldorff et al., 1993; Woldorff & Hillyard, 1991; Zabelina et al., 2015) − the component that peaks at about 50 msec from stimulus onset (for review: Pratt, 2011) and also likely originates in the auditory cortex (Huotilainen et al., 1998; Liegeois-Chauvel et al., 1994; Ponton et al., 2002; Pratt, 2011). Finally, several intracranial local field potential (LFP) studies reported enhancement in the auditory cortex as a result of selective attention (Bidet-Caulet et al., 2007; Mesgarani & Chang, 2012; Zion Golumbic et al., 2013).
Brain sensory processing is not passive, but is rather modulated by our internal state. Different research methods such as non-invasive imaging methods and intracranial recording of the local field potential (LFP) have been used to study to what extent sensory processing and the auditory cortex in particular are modulated by selective attention. However, at the level of the single- or multi-units the selective attention in humans has not been tested. In addition, most previous research on selective attention has explored externally-oriented attention, but attention can be also directed inward (i.e., internal attention), like spontaneous self-generated thoughts and mind-wandering. In the present study we had a rare opportunity to record multi-unit activity (MUA) in the auditory cortex of a patient. To complement, we also analyzed the LFP signal of the macro-contact in the auditory cortex. Our experiment consisted of two conditions with periodic beeping sounds. The participants were asked either to count the beeps (i.e., an “external attention” condition) or to recall the events of the previous day (i.e., an “internal attention” condition). We found that the four out of seven recorded units in the auditory cortex showed increased firing rates in “external attention” compared to “internal attention” condition. The beginning of this attentional modulation varied across multi-units between 30–50 msec and 130–150 msec from stimulus onset, a result that is compatible with an early selection view. The LFP evoked potential and induced high gamma activity both showed attentional modulation starting at about 70–80 msec. As the control, for the same experiment we recorded MUA activity in the amygdala and hippocampus of two additional patients. No major attentional modulation was found in the control regions. Overall, we believe that our results provide new empirical information and support for existing theoretical views on selective attention and spontaneous self-generated cognition.
Auditory evoked brain potentials as markers of chronic effects of mild traumatic brain injury in mid-life
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Citation Excerpt :
MCI/AD does not affect this region: Changes to auditory cortical potentials observed for this condition are thought to be mediated by disinhibition of sensory cortex resulting from frontal dysfunction (Golob et al., 2002). Additionally, mechanisms of auditory gating known to affect P50 amplitude are affected by fronto-parietally-mediated processes of attention (Guterman et al., 1992) and the P50 has a prominent frontal contributing source (Knott et al., 2009). However, other neural contributors to auditory sensory potentials may be impacted by mTBI including temporal, limbic, thalamic and midbrain areas.
Auditory event-related potential (ERP) correlates of pre-dementia in late-life may also be sensitive to chronic effects of mild traumatic brain injury (mTBI) in mid-life. In addition to mTBI history, other clinical factors may also influence ERP measures of brain function. This study’s objective was to evaluate the relationship between mTBI history, auditory ERP metrics, and common comorbidities.
ERPs elicited during an auditory target detection task, psychological symptoms, and hearing sensitivity were collected in 152 combat-exposed veterans and service members, as part of a prospective observational cohort study. Participants, with an average age of 43.6 years, were grouped according to positive (n = 110) or negative (n = 42) mTBI history. Positive histories were subcategorized into repetitive mTBI (3 + ) (n = 40) or non-repetitive (1–2) (n = 70).
Positive history of mTBI was associated with reduced N200 amplitude to targets and novel distractors. In participants with repetitive mTBI compared to non-repetitive and no mTBI, P50 was larger in response to nontargets and N100 was smaller in response to nontargets and targets. Changes in N200 were mediated by depression and anxiety symptoms and hearing loss, with no evidence of a supplementary direct mTBI pathway.
Auditory brain function differed between the positive and negative mTBI groups, especially for repetitive injury, which implicated more basic, early auditory processing than did any mTBI exposure. Symptoms of internalizing psychopathology (depression and anxiety) and hearing loss are implicated in mTBI’s diminished brain responses to behaviorally relevant and novel stimuli.
A mid-life neurologic vulnerability conferred by mTBI, particularly repetitive mTBI, may be detectable using auditory brain potentials, and so auditory ERPs are a target for study of dementia risk in this population.
Impaired conscious access and abnormal attentional amplification in schizophrenia
2018, NeuroImage: Clinical
Previous research suggests that the conscious perception of a masked stimulus is impaired in schizophrenia, while unconscious bottom-up processing of the same stimulus, as assessed by subliminal priming, can be preserved. Here, we test this postulated dissociation between intact bottom-up and impaired top-down processing and evaluate its brain mechanisms using high-density recordings of event-related potentials. Sixteen patients with schizophrenia and sixteen controls were exposed to peripheral digits with various degrees of visibility, under conditions of either focused attention or distraction by another task. In the distraction condition, the brain activity evoked by masked digits was drastically reduced in both groups, but early bottom-up visual activation could still be detected and did not differ between patients and controls. By contrast, under focused top-down attention, a major impairment was observed: in patients, contrary to controls, the late non-linear ignition associated with the P3 component was reduced. Interestingly, the patients showed an essentially normal attentional amplification of the P1 and N2 components. These results suggest that some but not all top-down attentional amplification processes are impaired in schizophrenia, while bottom-up processing seems to be preserved.
Disruption of Conscious Access in Schizophrenia
2017, Trends in Cognitive Sciences
Schizophrenia is a severe and complex psychiatric disorder resulting in delusions, hallucinations, and cognitive impairments. Across a variety of paradigms, an elevated threshold for conscious perception has been repeatedly observed in persons with schizophrenia. Remarkably, even subtle measures of subliminal processing appear to be preserved. We argue here that the dissociation between impaired conscious access and intact unconscious processing may be due to a specific disruption of top-down attentional amplification. This proposal is compatible with the neurophysiological disturbances observed in schizophrenia, including dysconnectivity, abnormal neural oscillations, and glutamatergic and cholinergic dysregulation. Therefore, placing impaired conscious access as a central feature of schizophrenia can help researchers develop a coherent and parsimonious pathophysiological framework of the disease.
The relevance of attention in schizophrenia P50 paired stimulus studies
2016, Clinical Neurophysiology
P50 suppression refers to the P50 ERP amplitude-reduction to the second (S2) relative to the first (S1) of identical brief auditory stimuli (SOA = 500 ms). Its reduction in schizophrenia is argued to represent impaired inhibitory input (II) mechanisms. Enhancing attention enhances II functionality (reducing S2P50 amplitude and increasing P50 difference) in healthy subjects. We determined whether the effect of attention on P50 suppression differs between schizophrenia patients (SCZ) and controls (CON) and thus is a confound in P50 schizophrenia research.
We manipulated the direction of attention (attention, non-attention) in 21 SCZ and 18 CON in the P50 suppression task.
Directing attention towards stimulus pairs (versus non-attention) increased P50 suppression (P50 difference). This effect differed between groups, with attention increasing S1P50, reducing S2P50 and increasing P50 suppression (P50 difference and reducing P50 ratio) in CON only. No group differences were found for P50 difference or ratio.
Attention is a confound in schizophrenia P50 research and thus should be carefully controlled. When attention was controlled, P50 group differences were not found.
The SCZ–CON P50 difference reported in the literature may be related to uncontrolled attention (and not impaired P50 suppression per se).
Detecting tones in complex auditory scenes
2015, NeuroImage
In everyday life, our auditory system is bombarded with many signals in complex auditory scenes. Limited processing capacities allow only a fraction of these signals to enter perceptual awareness. This magnetoencephalography (MEG) study used informational masking to identify the neural mechanisms that enable auditory awareness. On each trial, participants indicated whether they detected a pair of sequentially presented tones (i.e., the target) that were embedded within a multi-tone background.
We analysed MEG activity for ‘hits’ and ‘misses’, separately for the first and second tones within a target pair. Comparing physically identical stimuli that were detected or missed provided insights into the neural processes underlying auditory awareness. While the first tone within a target elicited a stronger early P50m on hit trials, only the second tone evoked a negativity at 150 ms, which may index segregation of the tone pair from the multi-tone background. Notably, a later sustained deflection peaking around 300 and 500 ms (P300m) was the only component that was significantly amplified for both tones, when they were detected pointing towards its key role in perceptual awareness.
Additional Dynamic Causal Modelling analyses indicated that the negativity at 150 ms underlying auditory stream segregation is mediated predominantly via changes in intrinsic connectivity within auditory cortices. By contrast, the later P300m response as a signature of perceptual awareness relies on interactions between parietal and auditory cortices.
In conclusion, our results suggest that successful detection and hence auditory awareness of a two-tone pair within complex auditory scenes relies on recurrent processing between auditory and higher-order parietal cortices.

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Attentional influence on the P50 component of the auditory event-related brain potential

Abstract

Psych. Res.

Biol. Psychiatry

Electroencephalogr. Clin. Neurophysiol.

Physiol. Psychol.

Electroencephalogr. Clin. Neurophysiol.

Neurophysiological evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia

Biol. Psychiatry

The maltese cross: A new simplistic model for memory

Behav. Brain Sci.

Perception and Communication

On the speed of mental processes

Attention and Performance

Acta Psychol.

Neurobiological studies of sensory gating in schizophrenia

Schizophr. Bull.

Neurophysiological evidence for a defect in inhibitory pathways in schizophrenia: Comparison of medicated and drug free patients

Biol. Psychiatry

A new method for off-line removal of ocular artifact

Electroencephalogr. Clin. Neurophysiol.

Pearl II: Portable laboratory computer system for psychophysiological assessment using event related brain potentials

Neurobehav. Toxicol. Teratol.