Encoding of nested levels of acoustic regularity in hierarchically organized areas of the human auditory cortex

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.

Empirical evaluation of fused EEG-MEG source reconstruction. Application to auditory mismatch generators

“…This is totally consistent with MLR findings from intracranial recordings studies (Liégeois-Chauvel et al, 1994;Pantev et al, 1995;Yvert et al, 2002). Recent MEG findings also reported temporal contributions including HG, in the right hemisphere (Recasens et al, 2014a) and bilaterally (Recasens et al, 2014b).…”

“…Beside, recent findings of earlier mismatch responses than the MMN encourage to develop a comprehensive analysis of auditory responses to improve our understanding of auditory (deviance) processing. To date, only a few MEG studies addressed the localization of early deviance components (Recasens et al, 2014a;2014b;Ruhnau et al, 2013), with activity circumscribed in the primary auditory cortex. Taken together, these recent findings indicate that it is time to combine high temporal and spatial information for an in-depth characterization of auditory processing.…”

“…To our knowledge no study has been conducted using fused inversion (simultaneous recordings but separate source modeling were conducted in Huotilainen et al, 1998;Kuuluvainen et al, 2014;Rinne et al, 2000). Taken together, fMRI (see for review Deouell, 2007) and electrophysiological studies (Fulham et al, 2014;Giard et al, 1995;Lappe et al, 2013a;Marco-Pallarés et al, 2005;Recasens et al, 2014b;Ruhnau et al, 2013;Waberski et al, 2001) suggested that the most prominent sources are located in temporal and frontal areas. However, there is a large and acknowledged variability across findings that prevents from a reliable and detailed description of the MMN network.…”

Mismatch negativity to pitch pattern deviants in schizophrenia

“…The peak amplitude of all three MMNs was maximal over frontocentral areas and exhibited CSDs consistent with bilateral sources from temporal lobe, although source modelling was not performed. The complex MMN tasks generated both an early (~ 125 ms) and a late MMN (~ 500 ms), while the simple pitch MMN task only generated an early MMN (~ 125 ms), consistent with previous studies (Korpilahti et al ., ; Zachau et al ., ; Recasens et al ., ; Haigh et al ., ; Korpilahti et al ., ). The results shown here demonstrate that while the early MMN responses on complex pattern tasks appear to be within normal limits in Sz, the later (and in HC, the most prominent) MMN is deficient in Sz.…”

“…() reported an early MMN at 146 ms after deviant descending pairs of tones, and a second MMN around 340 ms. Recasens et al . () measured MMN to a deviant additional tone and detected an early MMN around 150–200 ms and a later MMN around 250 ms, each arising from separate generator locations. The appearance of multiple MMNs may represent deviance detection at different levels of the auditory hierarchy (Grimm & Escera, ; Escera & Malmierca, ), with the early MMN being more sensory‐related (more in line with May & Tiitinen, , ), and the late MMN being more cognitive‐related (Näätänen, ; Winkler, ; Winkler et al ., ).…”