Sound Classification and Call Discrimination Are Decoded in Order as Revealed by Event-Related Potential Components in Frogs

Abstract

Species that use communication sounds to coordinate social and reproductive behavior must be able to distinguish vocalizations from nonvocal sounds as well as to identify individual vocalization types. In this study we sought to identify the neural localization of the processes involved and the temporal order in which they occur in an anuran species, the music frog Babina daunchina. To do this we measured telencephalic and mesencephalic event-related potentials (ERPs) elicited by synthesized white noise (WN), highly sexually attractive (HSA) calls produced by males from inside nests and male calls of low sexual attractiveness (LSA) produced outside of nests. Each stimulus possessed similar temporal structures. The results showed the following: (1) the amplitudes of the first negative ERP component (N1) at ∼100 ms differed significantly between WN and conspecific calls but not between HSA and LSA calls, indicating that discrimination between conspecific calls and nonvocal sounds occurs in ∼100 ms, (2) the amplitudes of the second positive ERP component (P2) at ∼200 ms in the difference waves between HSA calls and WN were significantly higher than between LSA calls and WN in the right telencephalon, implying that call characteristic identification occurs in ∼200 ms and (3) WN evoked a larger third positive ERP component (P3) at ∼300 ms than conspecific calls, suggesting the frogs had classified the conspecific calls into one category and perceived WN as novel. Thus, both the detection of sounds and the identification of call characteristics are accomplished quickly in a specific temporal order, as reflected by ERP components. In addition, the most dynamic ERP patterns appeared in the left mesencephalon and the right telencephalon, indicating the two brain regions might play key roles in anuran vocal communication.

Auditory neural networks for attention prefer biologically significant sounds and exhibit sexual dimorphism in anurans

“…In particular, the strengths of GC causal brain network connections in music frogs within the time window of the N1, P2 and P3 ERP components varied with the acoustic stimulus type and were sexually dimorphic. The results of the present study also show that the factor 'reproductive status' has neither main effects nor interactions with other factors, consistent with previous studies revealing that reproductive status does not affect the amplitude and latency of auditory ERP components elicited by male advertisement calls and white noise (Fang et al, 2015). The GC connections therefore represent relatively stable network properties not readily susceptible to seasonal hormonal influences.…”

“…Electrophysiological studies have shown that call playback stimuli elicit N1 ERP components significantly different from those elicited by white noise (WN) (Fang et al, 2015), consistent with the idea that music frogs allocate attention on the basis of the biological significance of sounds insofar as N1 is not solely determined by sensory processing but is modulated by attention (Gazzaniga et al, 2014). Moreover, both resting-state brain networks (Xue et al, 2016b) and functional brain networks associated with auditory perception (Xue et al, 2016a) have been identified in the music frog, suggesting that brain functions such as attention are mediated by specific brain networks.…”

“…Three stimuli of different biological significance were used: HSA calls, LSA calls and WN ( Fig. 2) (Fang et al, 2015). HSA and LSA calls that contained five notes recorded from the same individual were chosen randomly from the data set of our laboratory.…”

“…Specifically, each stimulus was presented a total of 100 times to each animal for a total of 300 stimulus presentations for each subject. Stimuli were presented from the two speakers simultaneously and broadcast in a random order within three blocks (100 stimulus presentations each), with a 1.5 s inter-stimulus interval between each stimulus presentation (Fang et al, 2015). Each stimulation block was followed by a 5 min silent period.…”

“…EEG signals were then divided into epochs with a duration of 1700 ms, including a pre-stimulus baseline of 200 ms. All epochs were inspected visually and those with artifacts and electrode drifts were removed from any further processing. The EEG signal within three 100 ms time windows corresponding to three previously identified auditory ERP components in this species (Fang et al, 2015) was analyzed further: the time window of 30-130 ms after stimulus onset was defined as ERP component N1, the 150-250 ms window was defined as P2 and the 290-390 ms window was defined as P3. The epochs of a given ERP component from an individual were then extracted and concatenated sequentially to build a new data set.…”