Serial and parallel processing in the human auditory cortex: A magnetoencephalographic study

Department of Integrative Physiology, National Institute for Physiological Sciences, Okazaki 444-8585, Japan.
Cerebral Cortex (Impact Factor: 8.67). 02/2006; 16(1):18-30. DOI: 10.1093/cercor/bhi080
Source: PubMed


Although anatomical, histochemical and electrophysiological findings in both animals and humans have suggested a parallel and serial mode of auditory processing, precise activation timings of each cortical area are not well known, especially in humans. We investigated the timing of arrival of signals to multiple cortical areas using magnetoencephalography in humans. Following click stimuli applied to the left ear, activations were found in six cortical areas in the right hemisphere: the posteromedial part of Heschl's gyrus (HG) corresponding to the primary auditory cortex (PAC), the anterolateral part of the HG region on or posterior to the transverse sulcus, the posterior parietal cortex (PPC), posterior and anterior parts of the superior temporal gyrus (STG), and the planum temporale (PT). The mean onset latencies of each cortical activity were 17.1, 21.2, 25.3, 26.2, 30.9 and 47.6 ms respectively. These results suggested a serial model of auditory processing along the medio-lateral axis of the supratemporal plane and, in addition, implied the existence of several parallel streams running postero-superiorly (from the PAC to the belt region and then to the posterior STG, PPC or PT) and anteriorly (PAC-belt-anterior STG).

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Available from: Atsuko Gunji, Oct 13, 2014
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    • "More specifically, assuming a 10-ms signal delay from cochlea to cortex (Liegeois Chauvel et al., 1991), the earliest onset latencies in the core, belt and parabelt were 17, 33 and 51 ms, respectively. These agree well with non-invasive results from the human auditory cortex , where corresponding serial activation occurs in the 17–48 ms range (Inui et al., 2006). The mean delay between response onset and maximum firing rate was 32 ms. "
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    ABSTRACT: Incoming sounds are represented in the context of preceding events, and this requires a memory mechanism that integrates information over time. Here, it was demonstrated that response adaptation, the suppression of neural responses due to stimulus repetition, might reflect a computational solution that auditory cortex uses for temporal integration. Adaptation is observed in single-unit measurements as two-tone forward masking effects and as stimulus-specific adaptation (SSA). In non-invasive observations, the amplitude of the auditory N1m response adapts strongly with stimulus repetition, and it is followed by response recovery (the so-called mismatch response) to rare deviant events. The current computational simulations described the serial core-belt-parabelt structure of auditory cortex, and included synaptic adaptation, the short-term, activity-dependent depression of excitatory corticocortical connections. It was found that synaptic adaptation is sufficient for columns to respond selectively to tone pairs and complex tone sequences. These responses were defined as combination sensitive, thus reflecting temporal integration, when a strong response to a stimulus sequence was coupled with weaker responses both to the time-reversed sequence and to the isolated sequence elements. The temporal complexity of the stimulus seemed to be reflected in the proportion of combination-sensitive columns across the different regions of the model. Our results suggest that while synaptic adaptation produces facilitation and suppression effects, including SSA and the modulation of the N1m response, its functional significance may actually be in its contribution to temporal integration. This integration seems to benefit from the serial structure of auditory cortex. © 2015 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.
    European Journal of Neuroscience 03/2015; 41(5):615-30. DOI:10.1111/ejn.12820 · 3.18 Impact Factor
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    • "Dotted lines on sagittal views indicate the height of the axial slice. [Doeller et al., 2003; Inui et al., 2006; Opitz et al., 1999; Sch€ onwiesner et al., 2007; Yvert et al., 2001]. Consistent with sensor-level data and previous findings, MMNm was larger on the right hemisphere [Paavilainen et al., 1991; Recasens et al., 2014]. "
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    ABSTRACT: Our auditory system is able to encode acoustic regularity of growing levels of complexity to model and predict incoming events. Recent evidence suggests that early indices of deviance detection in the time range of the middle-latency responses (MLR) precede the mismatch negativity (MMN), a well-established error response associated with deviance detection. While studies suggest that only the MMN, but not early deviance-related MLR, underlie complex regularity levels, it is not clear whether these two mechanisms interplay during scene analysis by encoding nested levels of acoustic regularity, and whether neuronal sources underlying local and global deviations are hierarchically organized. We registered magnetoencephalographic evoked fields to rapidly presented four-tone local sequences containing a frequency change. Temporally integrated local events, in turn, defined global regularities, which were infrequently violated by a tone repetition. A global magnetic mismatch negativity (MMNm) was obtained at 140-220 ms when breaking the global regularity, but no deviance-related effects were shown in early latencies. Conversely, Nbm (45-55 ms) and Pbm (60-75 ms) deflections of the MLR, and an earlier MMNm response at 120-160 ms, responded to local violations. Distinct neuronal generators in the auditory cortex underlay the processing of local and global regularity violations, suggesting that nested levels of complexity of auditory object representations are represented in separated cortical areas. Our results suggest that the different processing stages and anatomical areas involved in the encoding of auditory representations, and the subsequent detection of its violations, are hierarchically organized in the human auditory cortex. Hum Brain Mapp, 2014. © 2014 Wiley Periodicals, Inc.
    Human Brain Mapping 11/2014; 35(11). DOI:10.1002/hbm.22582 · 5.97 Impact Factor
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    • "We cannot elucidate the involvement of other brain regions such as the hippocampus or frontal cortex. However, peak latency at approximately 60 ms of Off-P50m suggested that it originating in the early stage of the auditory feedforward pathway [27]. In support this finding, the present results showed that Off-P50m arose from the auditory cortex. "
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    ABSTRACT: Previous studies showed that the amplitude and latency of the auditory offset cortical response depended on the history of the sound, which implicated the involvement of echoic memory in shaping a response. When a brief sound was repeated, the latency of the offset response depended precisely on the frequency of the repeat, indicating that the brain recognized the timing of the offset by using information on the repeat frequency stored in memory. In the present study, we investigated the temporal resolution of sensory storage by measuring auditory offset responses with magnetoencephalography (MEG). The offset of a train of clicks for 1 s elicited a clear magnetic response at approximately 60 ms (Off-P50m). The latency of Off-P50m depended on the inter-stimulus interval (ISI) of the click train, which was the longest at 40 ms (25 Hz) and became shorter with shorter ISIs (2.5∼20 ms). The correlation coefficient r2 for the peak latency and ISI was as high as 0.99, which suggested that sensory storage for the stimulation frequency accurately determined the Off-P50m latency. Statistical analysis revealed that the latency of all pairs, except for that between 200 and 400 Hz, was significantly different, indicating the very high temporal resolution of sensory storage at approximately 5 ms.
    PLoS ONE 08/2014; 9(8):e106553. DOI:10.1371/journal.pone.0106553 · 3.23 Impact Factor
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