Changes in Electroencephalogram Approximate Entropy Reflect Auditory Processing and Functional Complexity in Frogs

Brain systems engage in what are generally considered to be among the most complex forms of information processing. In the present study, we investigated the functional complexity of anuran auditory processing using the approximate entropy(Ap En) protocol for electroencephalogram(EEG) recordings from the forebrain and midbrain while male and female music frogs(Babina daunchina) listened to acoustic stimuli whose biological significance varied. The stimuli used were synthesized white noise(reflecting a novel signal), conspecific male advertisement calls with either high or low sexual attractiveness(reflecting sexual selection) and silence(reflecting a baseline). The results showed that 1) Ap En evoked by conspecific calls exceeded Ap En evoked by synthesized white noise in the left mesencephalon indicating this structure plays a critical role in processing acoustic signals with biological significance; 2) Ap En in the mesencephalon was significantly higher than for the telencephalon, consistent with the fact that the anuran midbrain contains a large well-organized auditory nucleus(torus semicircularis) while the forebrain does not; 3) for females Ap En in the mesencephalon was significantly different than that of males, suggesting that males and females process biological stimuli related to mate choice differently.     

仙琴蛙对不同类型声音的感知差异研究

既往研究发现听觉感知包括对声音信号的觉察、感觉、注意和知觉等多个认知过程,但依然不清楚大脑如何对不同类型的复杂声音信号(如同种鸣声和其他声音)进行解码和处理,以及在感知不同类型声音信号时大脑活动的动态特征.本研究记录了在随机播放白噪声和洞内鸣叫声音刺激时仙琴蛙Nidirana daunchina的左右端脑、间脑和中脑的...     

Integration of sensory and motor processing underlying social behaviour in túngara frogs

Social decision making involves the perception and processing of social stimuli, the subsequent evaluation of that information in the context of the individual's internal and external milieus to produce a decision, and then culminates in behavioural output informed by that decision. We examined brain networks in an anuran communication system that relies on acoustic signals to guide simple, stereotyped motor output. We used egr-1 mRNA expression to measure neural activation in male túngara frogs, Physalaemus pustulosus, following exposure to conspecific and heterospecific calls that evoke competitive or aggressive behaviour. We found that acoustically driven activation in auditory brainstem nuclei is transformed into activation related to sensory-motor interactions in the diencephalon, followed by motor-related activation in the telencephalon. Furthermore, under baseline conditions, brain nuclei typically have correlated egr-1 mRNA levels within brain divisions. Hearing conspecific advertisement calls increases correlations between anatomically distant brain divisions; no such effect was observed in response to calls that elicit aggressive behaviour. Neural correlates of social decision making thus take multiple forms: (i) a progressive shift from sensory to motor encoding from lower to higher stages of neural processing and (ii) the emergence of correlated activation patterns among sensory and motor regions in response to behaviourally relevant social cues.     

Effects of Caller Characteristics on Auditory Laterality in an Early Primate (Microcebus murinus)

Background

Auditory laterality is suggested to be characterized by a left hemisphere dominance for the processing of conspecific communication. Nevertheless, there are indications that auditory laterality can also be affected by communicative significance, emotional valence and social recognition.

Methodology/Principal Findings

In order to gain insight into the effects of caller characteristics on auditory laterality in the early primate brain, 17 gray mouse lemurs were tested in a head turn paradigm. The head turn paradigm was established to examine potential functional hemispheric asymmetries on the behavioral level. Subjects were presented with playbacks of two conspecific call types (tsak calls and trill calls) from senders differing in familiarity (unfamiliar vs. familiar) and sex (same sex vs. other sex). Based on the head turn direction towards these calls, evidence was found for a right ear/left hemisphere dominance for the processing of calls of the other sex (Binomial test: p = 0.021, N = 10). Familiarity had no effect on the orientation biases.

Conclusions/Significance

The findings in this study support the growing consensus that auditory laterality is not only determined by the acoustic processing of conspecific communication, but also by other factors like the sex of the sender.     

The recovery functions of auditory event-related potentials during split-second discriminations

We examined the recovery cycles of auditory event-related potentials (ERPs) in a high-speed auditory discrimination task and in passive conditions. Each trial contained 3 tones cued by a warning flash. In passive conditions, auditory ERPs consisted mainly of N1 (108 msec) and P2 (213 msec) components superimposed on a small CNV. The N1 and P2 were comparable in amplitude and both had prolonged refractory periods. In discriminative reaction time (DRT) conditions the same tones cued or inhibited press responses and elicited additional endogenous components (principally the Nd and P3). ERPs in DRT conditions were superimposed upon a prominent CNV that began after the warning cue and lasted throughout the signal delivery period.The N1 was larger in active than passive conditions and showed less marked refractory effects, while the P2 was smaller and showed more marked refractoriness. Differences between active and passive conditions could be explained by the presence of an endogenous negative potential (the Nd) with a short refractory period that was superimposed upon the N1 and P2.The P3 was recorded only in active conditions. At short ISIs (0.5 sec), P3 amplitudes were reduced and P3 latencies lengthened in parallel with prolongations in reaction time due to so-called psychological refractory period (PRP) effects. Both P3 recovery and the PRP reflected central mechanisms since they were observed at short ISIs when stimuli cueing different responses succeeded one another.N1 and P3 amplitudes diminished over the course of the experiment in both active and passive conditions. The decrease (amounting to about 30% of initial amplitudes) did not appear due to reductions in vigilance, since it was not accompanied by changes in reaction time or response accuracy, or by changes in other endogenous components (CNV or Nd). Short-term N1 habituation was unaffected by long-term amplitude reductions suggesting that independent mechanisms were responsible for the two phenomena.     

Representation of complex vocalizations in the Lusitanian toadfish auditory system: evidence of fine temporal,frequency and amplitude discrimination

Many fishes rely on their auditory skills to interpret crucial information about predators and prey, and to communicate intraspecifically. Few studies, however, have examined how complex natural sounds are perceived in fishes. We investigated the representation of conspecific mating and agonistic calls in the auditory system of the Lusitanian toadfish Halobatrachus didactylus, and analysed auditory responses to heterospecific signals from ecologically relevant species: a sympatric vocal fish (meagre Argyrosomus regius) and a potential predator (dolphin Tursiops truncatus). Using auditory evoked potential (AEP) recordings, we showed that both sexes can resolve fine features of conspecific calls. The toadfish auditory system was most sensitive to frequencies well represented in the conspecific vocalizations (namely the mating boatwhistle), and revealed a fine representation of duration and pulsed structure of agonistic and mating calls. Stimuli and corresponding AEP amplitudes were highly correlated, indicating an accurate encoding of amplitude modulation. Moreover, Lusitanian toadfish were able to detect T. truncatus foraging sounds and A. regius calls, although at higher amplitudes. We provide strong evidence that the auditory system of a vocal fish, lacking accessory hearing structures, is capable of resolving fine features of complex vocalizations that are probably important for intraspecific communication and other relevant stimuli from the auditory scene.     

Processing of global and local properties——An analysis with event-related brain potentials

The different processing of global and local properties of compound visual stimuli was studied with event-related brain potentials (ERPs) in the present experiment. It was found that, compared with the identification of global properties, the discrimination of local properties elicited longer RTs, lower accuracies, increased amplitudes of P1, decreased amplitudes of N1, and longer latencies of N2 and P3. The conflict of global and local properties increased the amplitudes of P2, decreased the amplitudes of P3, and prolonged latencies of N2 and P3. These results indicated that the advantage of global processing occurs at an early perceptual stage, and the attentional mechanisms for global and local processing may be different.     

A lateralized functional auditory network is involved in anuran sexual selection

Right ear advantage (REA) exists in many land vertebrates in which the right ear and left hemisphere preferentially process conspecific acoustic stimuli such as those related to sexual selection. Although ecological and neural mechanisms for sexual selection have been widely studied, the brain networks involved are still poorly understood. In this study we used multi-channel electroencephalographic data in combination with Granger causal connectivity analysis to demonstrate, for the first time, that auditory neural network interconnecting the left and right midbrain and forebrain function asymmetrically in the Emei music frog (Babina daunchina), an anuran species which exhibits REA. The results showed the network was lateralized. Ascending connections between the mesencephalon and telencephalon were stronger in the left side while descending ones were stronger in the right, which matched with the REA in this species and implied that inhibition from the forebrain may induce REA partly. Connections from the telencephalon to ipsilateral mesencephalon in response to white noise were the highest in the non-reproductive stage while those to advertisement calls were the highest in reproductive stage, implying the attention resources and living strategy shift when entered the reproductive season. Finally, these connection changes were sexually dimorphic, revealing sex differences in reproductive roles.     

P300 in young and elderly subjects: Auditory frequency and intensity effects

Auditory event-related potentials (ERPs) were assessed in young and elderly subjects when stimulus intensity (40 vs. 60 dB SL) and standard/target tone frequency (250/500 Hz and 1000/2000 Hz) were manipulated to study the effects of these variables on the P3(00) and N1, P2 and N2 components. Auditory thresholds for each stimulus type were obtained, and the stimulus intensity was adjusted to effect perceptually equal intensities across conditions for each subject. Younger subjects demonstrated larger P3 amplitudes and shorter latencies than elderly subjects. The low frequency stimuli produced larger P3 amplitude and shorter latencies than the high frequency stimuli. Low intensity stimuli yielded somewhat smaller P3 amplitudes and longer peak latencies than high intensity stimulus tones. Although additional stimulus intensity and frequency effects were obtained for the N1, P2 and N2 components, these generally differed relatively little with subject age. The findings suggest that auditory stimulus parameters contribute to P3 measures, which are different for young compared to elderly subjects.     

Evoked activity of the cat hypothalamus and amygdala under food motivation and in emotional stress

Amplitude-latency characteristics of auditory evoked potentials (EPs) recorded in bilateral points of the lateral hypothalamus and amygdala were studied under food motivation, in emotional stress (presentation of dogs) and tentative reactions. In the state of hunger, as compared with safety, the latencies of P1, N2 components of EP in hypothalamus, and P1, N2, N3 in amygdala were decreased and their amplitudes were changed. Changes in the left side of both structures were more pronounced. During presentation of dogs, decreases of latencies of all EP components including N1 occurred in hypothalamus and amygdala, changes in hypothalamic potentials were more pronounced on the right side, whereas in the amygdala--on the left side. During tentative responses to emotional-neutral stimuli, the latency of EP increased. It was concluded that sensory reactivity of hypothalamus and amygdala increased in motivational-emotional states. It was supposed that the side of dominance of structure may be related both to the factors of active or passive behavior during fear and the genesis of emotion (motivational or informational).     

Reflection of Anxiety in the Characteristics of Evoked EEG Potentials in 10- to 11-Year-Old Children

We studied the peculiarities of the amplitude/time parameters of evoked EEG potentials (EPs) and event-related potentials (ERPs) in 10- to 11-year-old children characterized by low and high anxiety levels. The latter levels were estimated using the scale of the manifest anxiety test of Prikhozhan and projective techniques (“House–Tree–Person,” HTP, and the Lüscher color test). For children with a high anxiety level, the amplitudes of the following EP components and ERPs were lower than those in low-anxiety children of the same age: P1 (predominantly in the occipital region of the left hemisphere), P2 (in the right occipital region), and Р300 wave (in different loci of both hemispheres). In high-anxiety children, we also more frequently observed increased amplitudes of the N2 component in the left parietal and right occipital regions. High-anxiety individuals were characterized by longer latencies of component P1 (mostly in the right frontal and left central regions) and, at the same time, shorter latencies of component N1 (in the parietal and occipital regions of the left hemisphere and also in the right temporal region). Thus, we found that the amplitude/time characteristics of a few EP components and ERPs in children with high anxiety levels differ statistically significantly from the parameters of corresponding EPs/ERPs in individuals of the same age but with low anxiety levels.     

Auditory stimulus-induced changes in immediate-early gene expression related to an inborn perceptual predisposition

Auditory-induced expression of the immediate-early gene ZENK was examined in 18 brain areas of domestic chicken and Japanese quail subjects with no previous exposure to parental vocalizations. After one 30-min exposure (approximately 120 calls) within 24 h of hatching to either the chicken or quail maternal call, paired subjects from each species showed significantly more intense levels of ZENK staining to conspecific (own species) calls. Single brain areas did not show consistent, large differences in ZENK expression across all subject pairs. Instead, a majority of brain areas exhibited a small conspecific stimulus-induced staining advantage in each species. The species differed in the quantitative distribution of ZENK responses among brain areas; qualitative patterns of call-induced staining exhibited both similarities and differences. The results suggest shared neural correlates and potential developmental/evolutionary differences in congenital brain responses to biologically significant auditory stimuli in na?ve individuals of the two species.     

Auditory selective attention in middle-aged and elderly subjects: an event-related brain potential study

Reaction times (RTs) and event-related brain potentials (ERPs) were recorded in middle-aged (MA) and elderly (ELD) subjects performing an auditory selective attention task. Subjets attended to tone bursts of a specified pitch and ear of delivery and responded to occasional longer duration target tones (75 vs. 25 msec). Infrequent novel stimuli (computer synthesized sounds and digitized environmental noises) were also included in the stimulus sequence.No significant age-related differences were found in the speed or accuracy of target detection. However, in both groups, RTs were delayed (by more than 300 msec) to targets that followed novel sounds. The prolongation was greater following novel sounds in the attended ear, particularly in the ELD group.The effects of selective attention on ERPs to standard tones were isolated as negative difference waves (Nds) by subtracting ERPs to non-attended stimuli from ERPs to the same signals when attended. Nds had similar amplitudes, latencies of onset (60 msec), and distributions in ELD and MA groups. In both groups, Nd waves were more prominent following right ear stimulation, reflecting possible hemispheric asymmetries of generators in posterior temporal regions.The mismatch negativity (MMN) was isolated by subtracting ERPs to standard tones from ERPs to deviant stimuli. MMN amplitudes were reduced in the ELD group. There was also a significant change in MMN distribution with age: the MMN was larger over the right hemisphere for MA subjects but larger over the left for ELD subjects. Elderly subjects showed a trend toward smaller P3 amplitudes and delayed P3 latencies, but group differences did not reach statistical significance. ERPs to novel sounds were characterized by centrally distributed N2 and P3a components. Although the novel P3a was enhanced with attention, no novel Nd waves could be isolated. This suggests that novel sounds fell outside the focus of attention.     

Heritable features of the auditory oddball event-related potential: peaks,latencies, morphology and topography

Baseline auditory ERP data from a larger study of the genetic determinants of the response to alcohol were collected from 59 monozygotic (MZ) twin pairs and from 39 same-sex dizygotic (DZ) twin pairs who drank socially. Three methods for measuring genetic influence on the ERPs were applied. First, based on maximum-likelihood estimates, the heritability of conventional peak amplitude and latency of N1 and P3 components was computed for each of 16 lead locations using tests of the significance of heritability based on intraclass correlations. P3 amplitude provided the strongest results, distributed symmetrically over caudal leads, and implied gene dominance as the mode of genetic transmission for the P3 component. A substantial genetic influence on N1 latency suggested a mixture of additive and dominance effects in the left fronto-temporal region. N1 amplitude measures trended towards significant heritability, but none was observed for P3 latency. The second method used the maximum of the cross-correlation function to compare wave form shape in a lead-by-lead analysis of data from cotwins. Genetic influence was apparent in both target and non-target ERP responses, with a fronto-central topography of significant results. The third method reduced all spatial and temporal ERP differences from a pair of twins to a single scalar number for each response. Distributions of this global measure revealed significant genetic influence on both non-target and target ERPs. A post hoc analysis of the effect of gender on the heritability of N1 or P3 peaks and latencies revealed no statistically significant observations in this sample of young adult twins.     

Auditory event-related potentials to the apparent auditory image motion

Auditory event-related potentials (ERP) were registered to the dichotically presented white noise stimuli (duration 1500 ms, band 150-1200 Hz). Abrupt or gradual change ofinteraural time difference in the middle of stimuli (750 ms after sound offset) was perceived as an apparent auditory image (AI) instant relocation or motion from the midline to one of the ears. In responses these stimuli two ERPs were observed: one to the sound onset, and second--to the onset of motion or AI relocation. ERPs to AI relocation differed from those to sound onset in longer components latencies (123 ms versus 105 ms for N 1,227 ms versus 190 ms for P2). In responses to AI motion component latencies were even longer (N1: 137 ms, P2: 240 ms); N1 amplitude was greater at sites contralateral to the AI motion direction.     

A test of the matched filter hypothesis in two sympatric frogs,Chiromantis doriae and Feihyla vittata

The matched filter hypothesis proposes that the auditory sensitivity of receivers should match the spectral energy distribution of the senders’ signals. If so, receivers should be able to distinguish between species-specific and hetero-specific signals. We tested the matched filter hypothesis in two sympatric species, Chiromantis doriae and Feihyla vittata, whose calls exhibit similar frequency characters and that overlap in the breeding season and microenvironment. For both species, we recorded male calls and measured the auditory sensitivity of both sexes using the auditory brainstem response (ABR). We compared the auditory sensitivity with the spectral energy distribution of the calls of each species and found that (1) auditory sensitivity matched the signal spectrogram in C. doriae and F. vittata; (2) the concordance conformed better to the conspecific signal versus the hetero-specific signal. In addition, our results show that species differences are larger than sex differences for ABR audiograms.     

Age differences of event-related potentials in the perception of successive and spatial components of auditory information

The perception of spatial and successive contexts of auditory information develops during child ontogeny. We compared event-related potentials (ERPs) recorded in 5- to 6-year-old children (N = 15) and adults (N = 15) in response to a digital series with omitted digits to explore age differences in the perception of successive auditory information. In addition, ERPs in response to the sound of a falling drop presented binaurally were obtained to examine the spatial content of auditory information. The ERPs obtained from the omitted digits significantly differed in the amplitude and latency of the N200 and P300 components between adults and children, which supports the hypothesis that the perception of a successive auditory structure is less automatic in children compared to adults. Although no significant differences were found in adults, the sound of a falling drop presented to the left ears of children elicited ERPs with earlier latencies and higher amplitudes of the P300 and N400 components in the right temporal area. Stimulation of the right ear caused an increasing amplitude of the N100 component in children. Thus, the observed differences in the auditory ERPs of children and adults reflect developmental changes in the perception of spatial and successive auditory information.     

Neural Activity Patterns in Response to Interspecific and Intraspecific Variation in Mating Calls in the Túngara Frog

Background

During mate choice, individuals must classify potential mates according to species identity and relative attractiveness. In many species, females do so by evaluating variation in the signals produced by males. Male túngara frogs (Physalaemus pustulosus) can produce single note calls (whines) and multi-note calls (whine-chucks). While the whine alone is sufficient for species recognition, females greatly prefer the whine-chuck when given a choice.

Methodology/Principal Findings

To better understand how the brain responds to variation in male mating signals, we mapped neural activity patterns evoked by interspecific and intraspecific variation in mating calls in túngara frogs by measuring expression of egr-1. We predicted that egr-1 responses to conspecific calls would identify brain regions that are potentially important for species recognition and that at least some of those brain regions would vary in their egr-1 responses to mating calls that vary in attractiveness. We measured egr-1 in the auditory brainstem and its forebrain targets and found that conspecific whine-chucks elicited greater egr-1 expression than heterospecific whines in all but three regions. We found no evidence that preferred whine-chuck calls elicited greater egr-1 expression than conspecific whines in any of eleven brain regions examined, in contrast to predictions that mating preferences in túngara frogs emerge from greater responses in the auditory system.

Conclusions

Although selectivity for species-specific signals is apparent throughout the túngara frog brain, further studies are necessary to elucidate how neural activity patterns vary with the attractiveness of conspecific mating calls.     

The P300 event-related potentials in dementia of the Alzheimer type. Correlations between P300 and monoamine metabolites

We studied auditory event-related potentials (ERPs) in 40 patients with dementia of the Alzheimer type (DAT). Peak latencies and amplitudes of N100, P200 and P300 components were measured. To study the possible relationships between the ERPs and monoaminergic neurotransmitter functions, CSF neurotransmitter metabolites were also analyzed. In patients with DAT, the P300 amplitude was significantly reduced and the P300 latency was prolonged. CSF concentrations of 5-hydroxyindoleacetic acid (5-HIAA) and homovanillic acid (HVA) were decreased. The P300 amplitude was significantly correlated with the 5-HIAA concentration. There were no correlations between the P300 components and the HVA concentration. These findings suggest that the serotonergic system modulates the P300 component of ERPs in patients with DAT.     

Effects of Auditory Attention Training with the Dichotic Listening Task: Behavioural and Neurophysiological Evidence

Facilitation of general cognitive capacities such as executive functions through training has stirred considerable research interest during the last decade. Recently we demonstrated that training of auditory attention with forced attention dichotic listening not only facilitated that performance but also generalized to an untrained attentional task. In the present study, 13 participants underwent a 4-week dichotic listening training programme with instructions to report syllables presented to the left ear (FL training group). Another group (n = 13) was trained using the non-forced instruction, asked to report whichever syllable they heard the best (NF training group). The study aimed to replicate our previous behavioural results, and to explore the neurophysiological correlates of training through event-related brain potentials (ERPs). We partially replicated our previous behavioural training effects, as the FL training group tended to show more allocation of auditory spatial attention to the left ear in a standard dichotic listening task. ERP measures showed diminished N1 and enhanced P2 responses to dichotic stimuli after training in both groups, interpreted as improvement in early perceptual processing of the stimuli. Additionally, enhanced anterior N2 amplitudes were found after training, with relatively larger changes in the FL training group in the forced-left condition, suggesting improved top-down control on the trained task. These results show that top-down cognitive training can modulate the left-right allocation of auditory spatial attention, accompanied by a change in an evoked brain potential related to cognitive control.