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 behavioral 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.
Highlights
Many animals rely on the processing of acoustic information for survival
We found that the frontal auditory field (FAF)-auditory cortex (AC) network is synchronized by default in low-frequencies, and that coherence with the FAF is strongest in deep laminae of the AC
Auditory stimuli consisted of artificially constructed syllabic trains with repetition rates of 5.28 and 97 Hz in order to test for slow and fast periodicities in acoustic streams, plus another syllabic train that had no clear rhythmicity as syllables were presented in a Poisson-like sequence with 70 Hz average rate
Summary
Many animals rely on the processing of acoustic information for survival. the mechanisms by which sounds are represented in neural networks involving distant areas in the brain remain obscure. PFC is thought to engage in cognitive processes ranging from attention, learning, and memory formation/retrieval, to decision making (Miller, 2000; Floresco and Ghods-Sharifi, 2007; St Onge et al, 2011; Gourley et al, 2013; Gilmartin et al, 2014; Pezze et al, 2014; Helfrich and Knight, 2016; Kim et al, 2016; Werchan et al, 2016; Helfrich et al, 2017) This area could be a fundamental node for sound evaluation in auditory networks, and even for the implementation of acoustically guided behaviors
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