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.