Comparison of non-invasive, scalp-recorded auditory steady-state responses in humans, rhesus monkeys, and common marmosets.

Auditory steady-state responses (ASSRs) are basic neural responses used to probe the ability of auditory circuits to produce synchronous activity to repetitive external stimulation. Reduced ASSR has been observed in patients with schizophrenia, especially at 40 Hz. Although ASSR is a translatable biomarker with a potential both in animal models and patients with schizophrenia, little is known about the features of ASSR in monkeys. Herein, we recorded the ASSR from humans, rhesus monkeys, and marmosets using the same method to directly compare the characteristics of ASSRs among the species. We used auditory trains on a wide range of frequencies to investigate the suitable frequency for ASSRs induction, because monkeys usually use stimulus frequency ranges different from humans for vocalization. We found that monkeys and marmosets also show auditory event-related potentials and phase-locking activity in gamma-frequency trains, although the optimal frequency with the best synchronization differed among these species. These results suggest that the ASSR could be a useful translational, cross-species biomarker to examine the generation of gamma-band synchronization in nonhuman primate models of schizophrenia.

Cerebral cortical processing time is elongated in human brain evolution.

An increase in number of neurons is presumed to underlie the enhancement of cognitive abilities in brain evolution. The evolution of human cognition is then expected to have accompanied a prolongation of net neural-processing time due to the accumulation of processing time of individual neurons over an expanded number of neurons. Here, we confirmed this prediction and quantified the amount of prolongation in vivo, using noninvasive measurements of brain responses to sounds in unanesthetized human and nonhuman primates. Latencies of the N1 component of auditory-evoked potentials recorded from the scalp were approximately 40, 50, 60, and 100 ms for the common marmoset, rhesus monkey, chimpanzee, and human, respectively. Importantly, the prominent increase in human N1 latency could not be explained by the physical lengthening of the auditory pathway, and therefore reflected an extended dwell time for auditory cortical processing. A longer time window for auditory cortical processing is advantageous for analyzing time-varying acoustic stimuli, such as those important for speech perception. A novel hypothesis concerning human brain evolution then emerges: the increase in cortical neuronal number widened the timescale of sensory cortical processing, the benefits of which outweighed the disadvantage of slow cognition and reaction.

Noninvasive scalp recording of the middle latency responses and cortical auditory evoked potentials in the alert common marmoset.

The common marmoset (Callithrix jacchus), a New World monkey, serves as a useful animal model in clinical and basic neuroscience. The present study recorded scalp auditory evoked potentials (AEP) in non-sedated common marmoset monkeys (n = 4) using a noninvasive method similar to that used in humans, and aimed to identify nonhuman primate correlates of the human AEP components. A pure tone stimulus was presented while electroencephalograms were recorded using up to 16 disk electrodes placed on the scalp and earlobes. Candidate homologues of two categories of the human AEP, namely, the middle latency responses (MLR; Na, Pa, Nb, and Pb) and the cortical auditory evoked potentials (CAEP; P1, N1, P2, N2, and the sustained potential, SP) were identified in the marmoset. These waves were labeled as CjNa, CjPa, CjNb, CjPb, CjP1, CjN1, CjP2, CjN2, and CjSP, where Cj stands for Callithrix jacchus. The last MLR component, CjPb, was identical to the first CAEP component, CjP1, similar to the relationship between Pb and P1 in humans. The peak latencies of the marmoset MLR and CAEP were generally shorter than in humans, which suggests a shorter integration time in neural processing. To our knowledge, the present study represents the first scalp recorded MLR and CAEP in the alert common marmoset. Further use of these recording methods would enable valid species comparisons of homologous brain indices between humans and animals.

Noninvasive scalp recording of cortical auditory evoked potentials in the alert macaque monkey.

Scalp-recorded evoked potentials (EP) provide researchers and clinicians with irreplaceable means for recording stimulus-related neural activities in the human brain, due to its high temporal resolution, handiness, and, perhaps more importantly, non-invasiveness. This work recorded the scalp cortical auditory EP (CAEP) in unanesthetized monkeys by using methods that are essentially identical to those applied to humans. Young adult rhesus monkeys (Macaca mulatta, 5-7 years old) were seated in a monkey chair, and their head movements were partially restricted by polystyrene blocks and tension poles placed around their head. Individual electrodes were fixated on their scalp using collodion according to the 10-20 system. Pure tone stimuli were presented while electroencephalograms were recorded from up to nineteen channels, including an electrooculogram channel. In all monkeys (n = 3), the recorded CAEP comprised a series of positive and negative deflections, labeled here as macaque P1 (mP1), macaque N1 (mN1), macaque P2 (mP2), and macaque N2 (mN2), and these transient responses to sound onset were followed by a sustained potential that continued for the duration of the sound, labeled the macaque sustained potential (mSP). mP1, mN2 and mSP were the prominent responses, and they had maximal amplitudes over frontal/central midline electrode sites, consistent with generators in auditory cortices. The study represents the first noninvasive scalp recording of CAEP in alert rhesus monkeys, to our knowledge.

Neural mechanisms underlying the orienting response to subject's own name: an event-related potential study.

Neural processes underlying the orienting response (OR) to subject's own name (SON) were investigated using the oddball paradigm. Subjects were presented with SON, subject's parent's name, and unfamiliar persons' names while they played a video game and ignored the auditory stimuli. A P3a-like frontal positivity (P440, 440 ms) indexing OR was elicited by SON only when it was the rare stimulus and its amplitude decreased with the repeated presentation of SON. Preceding the P440, SON consistently elicited an early frontal negativity (SON negativity, 170-270 ms), including when SON was the high-probability stimulus, and unlike the P440, this negativity did not habituate. These results conform to the hypothesis that early preattentive processing of speech sounds distinguishes SON from other names irrespective of short-term stimulus context, and that this culminates in an OR only when SON is evaluated as being contextually meaningful.

Functional asymmetry in primary auditory cortex for processing musical sounds: temporal pattern analysis of fMRI time series.

Hemispheric differences in the temporal processing of musical sounds within the primary auditory cortex were investigated using functional magnetic resonance imaging (fMRI) time series analysis on a 3.0 T system in right-handed individuals who had no formal training in music. The two hemispheres exhibited a clear-cut asymmetry in the time pattern of fMRI signals. A large transient signal component was observed in the left primary auditory cortex immediately after the onset of musical sounds, while only sustained activation, without an initial transient component, was seen in the right primary auditory cortex. The observed difference was believed to reflect differential segmentation in primary auditory cortical sound processing. Although the left primary auditory cortex processed the entire 30-s musical sound stimulus as a single event, the right primary auditory cortex had low-level processing of sounds with multiple segmentations of shorter time scales. The study indicated that musical sounds are processed as 'sounds with contents', similar to how language is processed in the left primary auditory cortex.

Central auditory processing of noncontextual consonance in music: an evoked potential study.

The consonance of individual chords presented out of musical context, or the noncontextual consonance of chords, is usually defined as the absence of roughness, which is a sensation perceived when slightly mistuned frequencies are not clearly resolved in the cochlea. The present work uses evoked potentials to demonstrate that the absence of roughness is not sufficient to explain the entirety of noncontextual consonance perception. Presented with a random sequence of various pure-tone intervals (0-13 semitones), listeners' cerebral cortical activities distinguished these stimuli according to their noncontextual consonance in a manner consistent with standard musical practice, even when the intervals exceeded the critical bandwidth (approximately three semitones). The roughness-based model of noncontextual consonance could not account for this result because these wide intervals had indistinguishably low levels of roughness. Further, this effect was evident only in musicians, indicating plasticity in the underlying neural mechanisms. The results are consistent with the hypothesis that, although the absence of roughness may represent an important aspect of noncontextual consonance, properties of intervals other than those related to roughness also contribute to this perception, underpinned by neural activity in the central auditory system that can be plastically modified by experience.

Electrophysiological correlates of absolute pitch and relative pitch.

The temporal and spatial characteristics of the cortical processes responsible for absolute pitch (AP) and relative pitch (RP) were investigated by multi-channel event-related potentials (ERPs). Compared to listening, pitch-naming of tones in non-possessors of AP elicited three ERP components (P3b, parietal positive slow wave, frontal negative slow wave) over parietal and frontal scalp between 300 and 900 ms in latency, representing the cortical processes for RP. Possessors of AP elicited a unique left posterior-temporal negativity ('AP negativity') at 150 ms in both listening and pitch-naming conditions, representing the cortical processes for AP that were triggered by pitch input irrespective of the task the subjects were asked to perform. Congruency of auditory Stroop stimuli modulated the amplitudes of parietal positive slow wave (non-possessors of AP) and 'AP negativity' (possessors of AP), confirming that these components reflect the verbal labeling or pitch-to-pitch-name associative transformation that is central to pitch-naming. These results are consistent with the hypothesis that AP is subserved by neuronal processes in the left auditory association cortex that occur earlier and more automatically than the processes for RP, which involve broader areas of the cortex over longer periods of time.

Cortical processing of musical consonance: an evoked potential study.

Cortical processes underlying perception of musical consonance were investigated by long-latency auditory evoked potentials (EPs). Subjects listened to a random sequence of dyadic pure tones paired at various pitch intervals (1, 4, 6, 7, or 9 semitones). Amplitudes of P2 and N2 components of auditory EPs were significantly modulated by pitch interval of the dyads, being most negative for 1 semitone (minor second) and least negative or most positive for 7 semitones (perfect fifth). The results indicate that neural processing of consonance depend not only on peripheral mechanisms in the inner ear but also on higher associative processing of pitch relationships in the cerebral cortex.