Abstract
Most mammals rely on the extraction of acoustic information from the environment in order to survive. However, the mechanisms that support sound representation in auditory neural networks involving sensory and association brain areas remain underexplored. In this study, we address the functional connectivity between an auditory region in frontal cortex (the frontal auditory field, FAF) and the auditory cortex (AC) in the bat Carollia perspicillata. The AC is a classic sensory area central for the processing of acoustic information. On the other hand, the FAF belongs to the frontal lobe, a brain region involved in the integration of sensory inputs, modulation of cognitive states, and in the coordination of behavioural outputs. The FAF-AC network was examined in terms of oscillatory coherence (local-field potentials, LFPs), and within an information theoretical framework linking FAF and AC spiking activity. We show that in the absence of acoustic stimulation, simultaneously recorded LFPs from FAF and AC are coherent in low frequencies (1-12 Hz). This “default” coupling was strongest in deep AC layers and was unaltered by acoustic stimulation. However, presenting auditory stimuli did trigger the emergence of coherent auditory-evoked gamma-band activity (>25 Hz) between the FAF and AC. In terms of spiking, our results suggest that FAF and AC engage in distinct coding strategies for representing artificial and natural sounds. Taken together, our findings shed light onto the neuronal coding strategies and functional coupling mechanisms that enable sound representation at the network level in the mammalian brain.
Footnotes
In this revision we delved deeper into the nature of gamma activity in the AC and FAF of Carollia perspicillata. Very weak correlations in the trial-by-trial power of low-frequency and gamma-band activities suggest that gamma in the AC-FAF circuit may not be wholly accounted for by a broadband increase of LFP onset-related power. This is further supported by a lack of correlation between the energy of the evoked response and the increase of gamma coherence in the FAF-AC network. Although this does not constitute conclusive evidence demonstrating that the reported gamma is indeed a separable phenomenon from the evoked response, the results hint towards the possibility of evoked gamma activity being an important component for audition. We propose that gamma rhythms in onset-related responses of auditory areas should be addressed carefully and thoroughly in future research.