Research ReportPrefrontal gamma-band activity distinguishes between sound durations
Introduction
Studies using intracortical recordings in animals have proposed oscillatory synchronization in the gamma-band range (∼ 30–100 Hz) as a mechanism underlying perceptual binding (Fries et al., 1997, Gray et al., 1989, Singer et al., 1997). Early electroencephalography (EEG) work in humans has supported this notion by showing increased gamma-band activity (GBA) during the perception of regularly moving bars (Lutzenberger et al., 1995, Müller et al., 1996) and gestalt-like (Kaiser et al., 2004, Tallon-Baudry et al., 1996) or meaningful objects (Keil et al., 1999, Pulvermüller et al., 1996, Rodriguez et al., 1999). Moreover, recent research has implicated fast oscillatory signals in a variety of cognitive processes including selective attention (Bauer et al., 2006, Fries et al., 2001, Gruber et al., 1999, Herrmann et al., 1999, Müller and Keil, 2004), memory (Axmacher et al., 2006, Gruber et al., 2004b, Herrmann et al., 2004c, Osipova et al., 2006), and decision-making (Jung-Beeman et al., 2004). These findings suggest a more general role of oscillatory synchronization for cognitive processes (Kaiser and Lutzenberger, 2005a, Kaiser and Lutzenberger, 2005b, Keil et al., 2001). Most of these functions have been related to induced, nonphase-locked GBA with typical peak latencies of ∼ 200–300 ms post stimulus onset (Tallon-Baudry and Bertrand, 1999), whereas evoked, phase-locked gamma responses may reflect both sensory processing (Busch et al., 2004, Karaka° and Ba°ar, 1998) and fast memory matches (Herrmann et al., 2004a). An overview of different types of gamma responses has been provided by Başar-Eroğlu et al. (1996).
At present, most researchers would agree that human GBA recorded with EEG or magnetoencephalography (MEG) may be interpreted as a correlate of the activation of cortical object representations. Evidence for GBA during the internal maintenance of an object representation in the absence of external stimulation has been yielded first in visual delayed matching-to-sample tasks where 25–45 Hz activity was increased at occipital and bilateral temporal electrodes compared with a nonmemory control condition (Tallon-Baudry et al., 1998, Tallon-Baudry et al., 1999). Furthermore, familiar pictures gave rise to stronger gamma responses than novel images, probably reflecting the activation of an existing memory trace (Gruber and Müller, 2005, Herrmann et al., 2004c). This gamma response is diminished to repeated presentations, suggesting a “sharpening” of the activated network (Gruber et al., 2004a, Gruber and Müller, 2002). Conversely, increased GBA with stimulus repetition of nonfamiliar objects may reflect the formation of new cortical representations (Fiebach et al., 2005, Gruber and Müller, 2005, Gruber and Müller, 2006). These EEG studies have usually yielded topographically widespread activations across a wide frequency range which may be attributable to the fact that averages across numerous stimuli were calculated, possibly resulting in the activation of a large number of different networks. However, so far there exists little evidence for GBA enhancements reflecting the activation of networks representing individual stimuli.
Here we used MEG with its high sensitivity to local activations to identify stimulus-specific oscillatory signals. Previous MEG studies using a statistical probability mapping have revealed highly local and spectrally narrow GBA enhancements in frequencies between ∼ 50 and 90 Hz exhibiting clear topographical differences, e.g., between auditory spatial versus nonspatial processing during passive change detection paradigms (Kaiser et al., 2000a, Kaiser et al., 2002a, Kaiser et al., 2002b). During delayed matching-to-sample tasks requiring the memorization of auditory spatial versus pattern-related information, enhanced GBA during the delay phase was found over regions of the putative auditory dorsal and ventral processing streams, respectively (Lutzenberger et al., 2002, Kaiser et al., 2003). This suggested that not the sounds as such were maintained, but their task-relevant acoustic features. GBA in response to the probe sound S2 was dependent on whether S1 and S2 were identical or not: a nonmatching S2 elicited an additional gamma response, possibly reflecting the activation of a further network in addition to the representation of S1 (Leiberg et al., 2006a). The present study used a short-term memory task where subjects had to memorize the duration of brief noise stimuli. Unlike previous studies where we averaged the responses across several different stimuli, here we employed only two S1 sounds to enable the direct comparison of oscillatory activity between two individual stimuli based on a sufficient number of trials. On the basis of previous work both in animals (Genovesio et al., 2006, Sakurai et al., 2004) and humans (Belin et al., 2002, Coull et al., 2004, Macar et al., 2002, Rao et al., 2001, Smith et al., 2003) we expected that representations of sound duration would involve premotor/prefrontal cortex. The present task required the maintenance of separate representations of the two durations of S1. We expected that different durations would be represented by different local networks which would be characterized by GBA enhancements at different frequencies and, possibly, with different topographies. The time courses of oscillatory activity in these local networks should reflect their involvement in the different stages of the working memory task, like stimulus encoding and maintenance and the comparison of sample and probe sounds.
Section snippets
Behavioral data
Subjects showed an overall performance of 76.5% hits (SD = 4.2) and 81.8% correct rejections (SD = 3.6). While correct response rates did not differ between short and long S2 stimuli, short S2 sounds elicited longer reaction times than longer stimuli (reaction time for short S2: 518.5 ms (SD = 36.3 ms) after the offset of S2; reaction time for long S2: 386.0 ms (SD = 39.6 ms)), F(1,11) = 5.7, p = 0.036. Hit rate and correct rejection rate for the matching trials were 82.5% (SD = 6.3) and 78.0% (SD = 5.2),
Discussion
The active memorization of brief sound durations and the subsequent comparison of sample and probe stimuli in a working memory task were associated with magnetoencephalographic GBA increases over frontal cortical areas. The comparison of shorter with longer sounds (100 versus 200 ms, respectively) yielded four GBA components with distinct spectral and temporal characteristics. During the encoding of S1, oscillatory activity at ∼ 40 Hz over the left fronto-temporal cortex differentiated longer
Subjects
Twelve healthy adults (seven females, five males, mean age 23.8 (SD = 0.4) years) gave their informed and written consent to participate in the study. The study was conducted in accordance with the Declaration of Helsinki.
Experimental procedure and stimulus materials
Subjects were seated upright in a magnetically shielded room (Vakuum-Schmelze, Hanau, Germany). They were instructed to sit still and keep their eyes open, looking at a fixation cross in the center of their visual field ∼2 m in front of them. Auditory stimuli were presented
Acknowledgment
This study was supported by Deutsche Forschungsgemeinschaft (DFG) grant SFB 550/C1.
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