Consonance and dissonance of musical chords: neural correlates in auditory cortex of monkeys and humans.

Some musical chords sound pleasant, or consonant, while others sound unpleasant, or dissonant. Helmholtz's psychoacoustic theory of consonance and dissonance attributes the perception of dissonance to the sensation of "beats" and "roughness" caused by interactions in the auditory periphery between adjacent partials of complex tones comprising a musical chord. Conversely, consonance is characterized by the relative absence of beats and roughness. Physiological studies in monkeys suggest that roughness may be represented in primary auditory cortex (A1) by oscillatory neuronal ensemble responses phase-locked to the amplitude-modulated temporal envelope of complex sounds. However, it remains unknown whether phase-locked responses also underlie the representation of dissonance in auditory cortex. In the present study, responses evoked by musical chords with varying degrees of consonance and dissonance were recorded in A1 of awake macaques and evaluated using auditory-evoked potential (AEP), multiunit activity (MUA), and current-source density (CSD) techniques. In parallel studies, intracranial AEPs evoked by the same musical chords were recorded directly from the auditory cortex of two human subjects undergoing surgical evaluation for medically intractable epilepsy. Chords were composed of two simultaneous harmonic complex tones. The magnitude of oscillatory phase-locked activity in A1 of the monkey correlates with the perceived dissonance of the musical chords. Responses evoked by dissonant chords, such as minor and major seconds, display oscillations phase-locked to the predicted difference frequencies, whereas responses evoked by consonant chords, such as octaves and perfect fifths, display little or no phase-locked activity. AEPs recorded in Heschl's gyrus display strikingly similar oscillatory patterns to those observed in monkey A1, with dissonant chords eliciting greater phase-locked activity than consonant chords. In contrast to recordings in Heschl's gyrus, AEPs recorded in the planum temporale do not display significant phase-locked activity, suggesting functional differentiation of auditory cortical regions in humans. These findings support the relevance of synchronous phase-locked neural ensemble activity in A1 for the physiological representation of sensory dissonance in humans and highlight the merits of complementary monkey/human studies in the investigation of neural substrates underlying auditory perception.

Neural correlates of auditory stream segregation in primary auditory cortex of the awake monkey.

An important feature of auditory scene analysis is the perceptual organization of sequential sound components, or 'auditory stream segregation'. Auditory stream segregation can be demonstrated by presenting a sequence of high and low frequency tones in an alternating pattern, ABAB. When the tone presentation rate (PR) is slow or the frequency separation (DeltaF) between the tones is small (<10%), a connected alternating sequence ABAB is perceived. When the PR is fast or the DeltaF is large, however, the alternating sequence perceptually splits into two parallel auditory streams, one composed of interrupted 'A' tones, and the other of interrupted 'B' tones. The neurophysiological basis of this perceptual phenomenon is unknown. Neural correlates of auditory stream segregation were examined in A1 of the awake monkey using neuronal ensemble techniques (multiunit activity and current source density). Responses evoked by alternating frequency sequences of tones, ABAB, were studied as a function of PR (5, 10, 20 and 40 Hz). 'A' tones corresponded to the best frequency (BF) of the cortical site, while 'B' tones were situated away from the BF by an amount DeltaF. At slow PRs, 'A' and 'B' tones evoked responses that generated an overall pattern of activity at the stimulus PR. In contrast, at fast PRs, 'B' tone responses were differentially suppressed, resulting in a pattern of activity consisting predominantly of 'A' tone responses at half the PR. The magnitude of 'B' tone response suppression increased with DeltaF. Differential suppression of BF and non-BF tone responses at high PRs can be explained by physiological principles of forward masking. The effect of DeltaF is explained by the hypothesis that responses to tones distant from the BF are more susceptible to suppression by BF tones than responses to tones near the BF. These results parallel human psychoacoustics of auditory stream segregation and suggest a cortical basis for the perceptual phenomenon.

Complex tone processing in primary auditory cortex of the awake monkey. I. Neural ensemble correlates of roughness.

Previous physiological studies [e.g., Bieser and Muller-Preuss, Exp. Brain Res. 108, 273-284 (1996); Schulze and Langner, J. Comp. Physiol. A 181, 651-663 (1997); Steinschneider et al., J. Acoust. Soc. Am. 104, 2935-2955 (1998)] have suggested that neural activity in primary auditory cortex (A1) phase-locked to the waveform envelope of complex sounds with low (<300 Hz) periodicities may represent a neural correlate of roughness perception. However, a correspondence between these temporal response patterns and human psychophysical boundaries of roughness has not yet been demonstrated. The present study examined whether the degree of synchronized phase-locked activity of neuronal ensembles in A1 of the awake monkey evoked by complex tones parallels human psychoacoustic data defining the existence region and frequency dependence of roughness. Stimuli consisted of three consecutive harmonics of fundamental frequencies (f(0)s) ranging from 25 to 4000 Hz. The center frequency of the complex tones was fixed at the best frequency (BF) of the cortical sites, which ranged from 0.3 to 10 kHz. Neural ensemble activity in the thalamorecipient zone (lower lamina III) and supragranular cortical laminae (upper lamina III and lamina II) was measured using multiunit activity and current source density techniques and the degree of phase-locking to the f0 was quantified by spectral analysis. In the thalamorecipient zone, the stimulus f0 at which phase-locking was maximal increased with BF and reached an upper limit between 75 and 150 Hz for BFs greater than about 3 kHz. Estimates of limiting phase-locking rates also increased with BF and approximated psychoacoustic values for the disappearance of roughness. These physiological relationships parallel human perceptual data and therefore support the relevance of phase-locked activity of neuronal ensembles in A1 for the physiological representation of roughness.

Complex tone processing in primary auditory cortex of the awake monkey. II. Pitch versus critical band representation.

Noninvasive neurophysiological studies in humans support the existence of an orthogonal spatial representation of pure tone frequency and complex tone pitch in auditory cortex [Langner et al., J. Comp. Physiol. A 181, 665-676 (1997)]. However, since this topographic organization is based on neuromagnetic responses evoked by wideband harmonic complexes (HCs) of variable fundamental frequency (f0), and thus interharmonic frequency separation (deltaF), critical band filtering effects due to differential resolvability of harmonics may have contributed to shaping these responses. To test this hypothesis, the present study examined responses evoked by three-component HCs of variable f0 in primary auditory cortex (A1) of the awake monkey. The center frequency of the HCs was fixed at the best frequency (BF) of the cortical site. Auditory evoked potential (AEP), multiunit activity, and current source density techniques were used to evaluate A1 responses as a function of f0 (=deltaF). Generally, amplitudes of nearly all response components increased with f0, such that maximal responses were evoked by HCs comprised of low-order resolved harmonics. Statistically significant increases in response amplitude typically occurred at deltaFs between 10% and 20% of center frequency, suggestive of critical bandlike behavior. Complex tone response amplitudes also reflected nonlinear summation in that they could not be predicted by the pure tone frequency sensitivity curves of the cortical sites. A mechanism accounting for the observed results is proposed which involves mutual lateral inhibitory interactions between responses evoked by stimulus components lying within the same critical band. As intracortical AEP components likely to be propagated to the scalp were also strongly modulated by deltaF, these findings indicate that noninvasive recordings of responses to complex sounds may require a consideration of critical band effects in their interpretation.

Binaural interactions in primary auditory cortex of the awake macaque.

The functional organization of primary auditory cortex in non-primates is generally modeled as a tonotopic gradient with an orthogonal representation of independently mapped binaural interaction columns along the isofrequency contours. Little information is available regarding the validity of this model in the primate brain, despite the importance of binaural cues for sound localization and auditory scene analysis. Binaural and monaural responses of A1 to pure tone stimulation were studied using auditory evoked potentials, current source density and multiunit activity. Key findings include: (i) differential distribution of binaural responses with respect to best frequency, such that 74% of the sites exhibiting binaural summation had best frequencies below 2000 Hz; (ii) the pattern of binaural responses was variable with respect to cortical depth, with binaural summation often observed in the supragranular laminae of sites showing binaural suppression in thalamorecipient laminae; and (iii) dissociation of binaural responses between the initial and sustained action potential firing of neuronal ensembles in A1. These data support earlier findings regarding the temporal and spatial complexity of responses in A1 in the awake state, and are inconsistent with a simple orthogonal arrangement of binaural interaction columns and best frequency in A1 of the awake primate.

Click train encoding in primary auditory cortex of the awake monkey: evidence for two mechanisms subserving pitch perception.

Multiunit activity (MUA) and current source density (CSD) patterns evoked by click trains are examined in primary auditory cortex (A1) of three awake monkeys. Temporal and spectral features of click trains are differentially encoded in A1. Encoding of temporal features occurs at rates of 100-200 Hz through phase-locked activity in the MUA and CSD, is independent of pulse polarity pattern, and occurs in high best frequency (BF) regions of A1. The upper limit of ensemble-wide phase-locking is about 400 Hz in the input to A1, as manifested in the cortical middle laminae CSD and MUA of thalamocortical fibers. In contrast, encoding of spectral features occurs in low BF regions, and resolves both the f0 and harmonics of the stimuli through local maxima of activity determined by the tonotopic organization of the recording sites. High-pass filtered click trains decrease spectral encoding in low BF regions without modifying phase-locked responses in high BF regions. These physiological responses parallel features of human pitch perception for click trains, and support the existence of two distinct physiological mechanisms involved in pitch perception: the first using resolved harmonic components and the second utilizing unresolved harmonics that is based on encoding stimulus waveform periodicity.

Pitch vs. spectral encoding of harmonic complex tones in primary auditory cortex of the awake monkey.

Neuromagnetic studies in humans and single-unit studies in monkeys have provided conflicting views regarding the role of primary auditory cortex (A1) in pitch encoding. While the former support a topographic organization based on the pitch of complex tones, single-unit studies support the classical tonotopic organization of A1 defined by the spectral composition of the stimulus. It is unclear whether the incongruity of these findings is due to limitations of noninvasive recordings or whether the discrepancy genuinely reflects pitch representation based on population encoding. To bridge these experimental approaches, we examined neuronal ensemble responses in A1 of the awake monkey using auditory evoked potential (AEP), multiple-unit activity (MUA) and current source density (CSD) techniques. Macaque monkeys can perceive the missing fundamental of harmonic complex tones and therefore serve as suitable animal models for studying neural encoding of pitch. Pure tones and harmonic complex tones missing the fundamental frequency (f0) were presented at 60 dB SPL to the ear contralateral to the hemisphere from which recordings were obtained. Laminar response profiles in A1 reflected the spectral content rather than the pitch (missing f0) of the compound stimuli. These findings are consistent with single-unit data and indicate that the cochleotopic organization is preserved at the level of A1. Thus, it appears that pitch encoding of multi-component sounds is more complex than suggested by noninvasive studies, which are based on the assumption of a single dipole generator within the superior temporal gyrus. These results support a pattern recognition mechanism of pitch encoding based on a topographic representation of stimulus spectral composition at the level of A1.