Encoding of frequency-modulation (FM) rates in human auditory cortex

Abstract

Frequency-modulated sounds play an important role in our daily social life. However, it currently remains unclear whether frequency modulation rates affect neural activity in the human auditory cortex. In the present study, using magnetoencephalography, we investigated the auditory evoked N1m and sustained field responses elicited by temporally repeated and superimposed frequency-modulated sweeps that were matched in the spectral domain, but differed in frequency modulation rates (1, 4, 16, and 64 octaves per sec). The results obtained demonstrated that the higher rate frequency-modulated sweeps elicited the smaller N1m and the larger sustained field responses. Frequency modulation rate had a significant impact on the human brain responses, thereby providing a key for disentangling a series of natural frequency-modulated sounds such as speech and music.

Modulation of Auditory Evoked Magnetic Fields Elicited by Successive Frequency-Modulated (FM) Sweeps

“…Positron emission tomography (Zatorre and Belin, 2001 ) and functional MRI (Jamison et al, 2006 ) studies demonstrated that the right hemisphere plays a dominant role in spectral processing. Previous MEG studies (Heinemann et al, 2011 ; Okamoto and Kakigi, 2015 ) also revealed that the N1m responses elicited by FM sweeps were larger in the right than in the left hemisphere. The right hemispheric dominance for FM sweep processing observed in the present study is also consistent with previous findings demonstrating that auditory cortex lesions in the right hemisphere caused severe impairments in detecting the frequency modulation of test sounds, whereas lesions in the left did not cause such an impairment in animals (Wetzel et al, 1998 ; Rybalko et al, 2006 ) or humans (Johnsrude et al, 2000 ).…”

“…The results obtained appear to be contradictory to previous findings showing that the N1/ N1m responses elicited by repetitive identical pure tones were smaller than those elicited by successive distinct pure tones (Butler, 1968 ; Sams et al, 1985 ; Lagemann et al, 2012 ). Previous studies showed that neurons in the auditory cortex are sensitive to the rate and/or direction of FM sweeps in animals (Mendelson and Cynader, 1985 ; Heil and Scheich, 1992 ; Heil et al, 1992 ; Mendelson et al, 1993 ; Nelken and Versnel, 2000 ; Tian and Rauschecker, 2004 ; Godey et al, 2005 ; Atencio et al, 2007 ; Brown and Harrison, 2009 ; Trujillo et al, 2011 ) and humans (Hall et al, 2000 , 2002 ; Hsieh et al, 2012 ; Joanisse and Desouza, 2014 ; Okamoto and Kakigi, 2015 ). The neural processing of repetitive FM sweeps in the human auditory cortex appears to differ from that of repetitive pure tones.…”

“…AS and TS had a duration of 0.25 s with 0.01-s linear onset and offset ramps (sampling rate: 48,000 Hz). They were temporally repeated and superimposed FM sweeps similar to those used in our previous study (Okamoto and Kakigi, 2015 ). They consisted of six FM tones that traversed an upward or downward direction within the 500–2000 Hz frequency range with a modulation rate of 4 or 16 octaves per sec , resulting in four FM sweeps (FM_up_04, FM_up_16, FM_down_04, and FM_down_16).…”

“…Previous studies showed that FM sweeps caused stronger neural activity than pure tones in the primary auditory cortex of marmosets (Liang et al, 2002 ) as well as stronger non-primary auditory area activity than that in the primary auditory cortex in cats (Tian and Rauschecker, 1994 , 1998 ; Heil and Irvine, 1998 ). Moreover, a recent MEG study measuring the neural activity elicited by temporally repeated and superimposed FM sweeps revealed that lower-rate FM sweeps (1 and 4 octaves per sec ) elicited larger N1m source strengths and shorter N1m latencies than higher-rate FM sweeps (16 and 64 octaves per sec ; Okamoto and Kakigi, 2015 ). FM sweeps in human speech play an essential role in verbal communications.…”

A Minimum Temporal Window for Direction Detection of Frequency-Modulated Sweeps: A Magnetoencephalography Study

“…Overall, previous studies employing the MMNm paradigm to examine the brain's pre-attentive processing of FM features at an automatic preconscious encoding level have mostly focused on detecting changes in the directionality of frequency contours. In general, the frequency sweep durations examined in these MMNm studies were relatively long (i.e., slow rates), ranging from approximately 100 -250 ms (Pardo and Sams, 1993) to 1000 ms (Okamoto and Kakigi, 2015). It has been suggested that the duration limit or "temporal window" of the frequency contour, at which the auditory cortex is able to reliably detect direction, can critically affect how speech sounds are perceived (Hickok and Poeppel, 2000).…”