Elsevier

Clinical Neurophysiology

Volume 122, Issue 9, September 2011, Pages 1755-1763
Clinical Neurophysiology

Exacerbated attention orienting to auditory stimulation in migraine patients

https://doi.org/10.1016/j.clinph.2011.02.013Get rights and content

Abstract

Objective

To investigate long-term (LTH) and short-term (STH) habituation of auditory event-related potentials (ERPs) during a migraine cycle, using a classic habituation paradigm.

Methods

In 22 patients suffering from menstrually-related migraine and in 20 age-matched control subjects, auditory ERPs were recorded in 3 sessions: in the middle of the menstrual cycle, before menses, and during menses. In 12 patients, a migraine attack occurred during one of the peri-menses sessions. In each session, 200 trains of stimuli were presented, with an average of 10 stimuli per train.

Results

In response to the first stimuli of the trains, migraineurs exhibited in all sessions a larger orienting component of N1 than matched controls and a larger P3a in the interictal session, which normalized during attacks. They also showed a residual orienting component in response to the subsequent stimuli inside the trains. In contrast, the sensory component of N1 showed no difference between the two groups, with similar STH and LTH.

Conclusions

Migraineurs show an exacerbated attention orienting to auditory stimulation, without any habituation deficit.

Significance

Previous migraine studies reported interictal habituation deficits of ERPs, but demonstrated in the auditory modality only in paradigms testing intensity dependence. Previous and current results can be interpreted as an increased attention orienting, possibly relying on an abnormal involvement of frontal cortex in auditory processing.

Highlights

► Migraineurs were tested with a classic auditory habituation paradigm and, in apparent contrast with previous results, did not exhibit any ERP habituation deficit. ► Rather, a larger N1 orienting component was observed in migraineurs relative to controls, suggesting an increased automatic attention towards incoming acoustic input. ► The increased automatic attention towards acoustic stimuli partially normalizes during migraine attacks, and could be related to a frontal dysfunction in migraine.

Introduction

Migraine is a common, but complex neurological disorder characterized by recurrent episodes of disabling headache. During attacks, many patients present hypersensitivity to light, sound, and/or odors (The International Classification of Headache Disorders, 2004). Some studies suggest that hypersensitivity to external stimuli may even persist between migraine attacks (Main et al., 1997, Vanagaite et al., 1997, Vingen et al., 1999, Mulleners et al., 2001, Demarquay et al., 2006). During the past 15 years, numerous event-related potential (ERP) studies aimed at investigating the pathophysiological basis of such hypersensitivity to environmental stimuli (for reviews, see Giffin and Kaube, 2002, Schoenen et al., 2003, Ambrosini and Schoenen, 2006, Gantenbein and Sandor, 2006). Most of these studies converged on abnormal habituation patterns in migraine patients between attacks (for a review, see Coppola et al., 2009). These habituation deficits seem to normalize immediately before and during migraine attacks (Kropp and Gerber, 1993, Kropp and Gerber, 1995, Evers et al., 1999, Judit et al., 2000). Habituation is the most elementary and ubiquitous form of behavioral plasticity consisting in a decreased responsiveness by repetition of the same stimulus, an adaptive mechanism aimed at protecting against sensory overstimulation (Groves and Thompson, 1970). Two distinct kinds of habituation of evoked potentials are described. Long-term habituation (LTH) is observed over successive blocks of trials in the course of an experimental session and seems to fit with the classic definition of habituation, i.e. an adaptation to loss of novelty (Sokolov, 1963). Short-term habituation (STH) is a rapid response decrement, whose origin would most probably be a refractory period effect (Ritter et al., 1968, Budd et al., 1998). In migraine, habituation deficits have been first reported for cognitive responses like the Contingent Negative Variation (CNV, in Kropp and Gerber, 1993, Kropp and Gerber, 1995) and the P300 (P3a and/or P3b, elicited by various paradigms, in Wang et al., 1995, Wang and Schoenen, 1998, Evers et al., 1999, Siniatchkin et al., 2003). Habituation of obligatory sensory responses has been particularly investigated in the visual modality. Numerous migraine studies showed a deficient habituation of visual evoked potentials to pattern reversals (Schoenen et al., 1995, Afra et al., 1998, Wang et al., 1999, Di Clemente et al., 2005). However, this result was not systematically observed, and a relation was demonstrated between temporal or spatial frequency of visual stimuli and habituation deficit in migraine patients (Oelkers et al., 1999, Sand and Vingen, 2000).

Despite the fact that phonophobia is a classic feature of migraine attacks, only few studies have addressed habituation of auditory responses in migraineurs. Auditory processing in migraine was initially explored through the study of intensity dependence of auditory potentials (IDAP). An augmented IDAP was reported in migraine patients (Wang et al., 1996, Wang et al., 1999, Judit et al., 2000, Siniatchkin et al., 2000c; Ambrosini et al., 2003), except in one study (Sand and Vingen, 2000). A deficit in LTH of auditory ERPs was found through IDAP paradigms in two studies (Wang et al., 1996, Ambrosini et al., 2003), but not in a third one (Sand and Vingen, 2000). Using an oddball paradigm, Wang and Schoenen did not find any habituation deficit of auditory sensory component N1-P2 (Wang and Schoenen, 1998). Short-term habituation of auditory responses in migraine patients has only been addressed through the demonstration of impaired gating of middle latency P50 in migraine patients (Ambrosini et al., 2001, Siniatchkin et al., 2003).

As the habituation of auditory responses has been rarely investigated in migraine and the results are quite controversial, the present study aimed first at investigating STH and LTH of auditory N1 and subsequent automatic orienting brain responses, in migraine patients and in control subjects, using a classic habituation paradigm (Ritter et al., 1968, Woods and Elmasian, 1986): trains of about 10 stimuli are presented with 5.5 to 8 s of inter-train silent gaps. This paradigm allows for a simultaneous study of STH (within trains) and LTH (between trains), as well as an assessment of components related to automatic attention orienting (towards the initial stimuli of the trains). In order to be able to clearly differentiate the different components, and in particular to dissociate the obligatory sensory N1 from the subsequent orienting response, we used a set of 7 scalp electrodes, including the mastoids. The second aim of this study was to investigate auditory ERPs during a migraine cycle. To optimize the chance of recording ERPs during migraine attacks, we selected female patients with menstrually-related migraine without aura. Auditory ERPs were recorded in migraineurs and control subjects on three different days: just before menses, at the beginning of menses and in the middle of the menstrual period. Based on the results of the literature, we hypothesized that migraine patients would show a deficit in habituation of the sensory and orienting components in the migraine-free period but a normalization before and during migraine attacks.

Section snippets

Patients and healthy subjects

Twenty-five female migraine patients were included in the study. Patients fulfilled International Headache Society (IHS) criteria for menstrually-related migraine without aura (The International Classification of Headache Disorders, 2004). The recordings of two patients were discarded for technical reasons, and one patient was excluded from analyses because she had been taking paroxetine for 2 months. The final group thus included 22 patients. Their mean age was 27 years ± 7. Duration of the

Results

Fig. 1 displays the grand average ERPs to the first three stimuli of the trains and to generic standards, averaged over the 3 sessions for 20 healthy subjects and for 22 migraine patients.

Discussion

We investigated auditory processing using a classic auditory ERP habituation paradigm in migraine patients and in female controls. This paradigm consisted in presenting short trains of auditory stimuli, separated by silent gaps. On the one hand, this paradigm basically allows investigating short-term habituation (along trains) and long-term habituation (along the whole recording session) of obligatory sensory ERPs to repetitive auditory stimuli. As expected (Woods and Elmasian, 1986), healthy

Acknowledgements

We wish to thank the control subjects and the patients who participated in this experiment. We are also grateful to the technicians of the Functional Neurology Department for their help in recordings ERPs. The authors have no conflict of interest.

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