Fronto-Temporal Coupling Dynamics During Spontaneous Activity and Auditory Processing in the Bat Carollia perspicillata

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.

Echolocation reverses information flow in a cortical vocalization network

“…Directed connectivity in the FAF-AC circuit during vocal production Oscillations in FAF and AC predict ensuing vocal output with functionally opposite patterns, but how rhythms in this network interact during vocal production remains unknown. In previous work we reported low-frequency (1-12 Hz) phase coherence in the FAF-AC circuit during spontaneous activity, with emergence of -band (> 25 Hz) coherence at the onset of external acoustic stimulation (García-Rosales et al, 2020). To study FAF-AC oscillatory dynamics during vocal production, we looked beyond phase correlations and examined causal interactions in the fronto-auditory circuit based on a transfer entropy framework.…”

“…1 mm 2 ) with the aid of a scalpel blade on the first day of recordings. In the AC, recordings were made mostly in the high frequency fields (Eiermann and Esser, 2000;Esser and Eiermann, 1999;García-Rosales et al, 2020)) After surgery, animals were given no less than two days of rest before the onset of experiments. No experiments on a single animal lasted longer than 4 h per day.…”

“…Experimental evidence demonstrates that the neural activity in frontal regions relates to vocalization (Gavrilov et al, 2017; Hage and Nieder, 2013; Roy et al, 2016; Weineck et al, 2020), correlating with the acoustic and behavioural properties of produced calls (Hage and Nieder, 2013; Weineck et al, 2020). Frontal regions are also anatomically and functionally connected with the auditory cortex (AC; (García-Rosales et al, 2020; Kobler et al, 1987; Park et al, 2015; Plakke and Romanski, 2014; Winkowski et al, 2013; Winkowski et al, 2018)), a cornerstone structure for audition that exhibits suppression to self-produced sounds (Aliu et al, 2009; Baess et al, 2011; Martikainen et al, 2005; Rummell et al, 2016), including vocalizations (Eliades and Wang, 2003, 2005; Flinker et al, 2010; Tsunada and Eliades, 2020). Such auditory cortical suppression is thought to be mediated by preparatory motor signals originating in the motor system (i.e.…”

“…LFPs are an electrophysiological marker of the extracellular spiking activity and synaptic currents in local neuronal populations (Buzsaki et al, 2012). In frontal and sensory cortices, these signals participate in cognitive processes, sensory computations, and interareal communication via phase coherence (Fries, 2015; García-Rosales et al, 2018; García-Rosales et al, 2020; Helfrich and Knight, 2016; Lakatos et al, 2008; Lakatos et al, 2013). In the FAF, a richly connected auditory region of the bat frontal cortex (Eiermann and Esser, 2000; Kobler et al, 1987), LFP activity predicts vocal output while synchronizing differentially with dorso-striatal oscillations according to vocalization type (Weineck et al, 2020).…”

Systematic Review: Anesthetic Protocols and Management as Confounders in Rodent Blood Oxygen Level Dependent Functional Magnetic Resonance Imaging (BOLD fMRI)—Part B: Effects of Anesthetic Agents, Doses and Timing

“…First, anesthetics per definitionem alter brain functions as observable on a macroscopic level, and it is believed that this altered state of functionality results from reduced information integration [ 11 ]. Based on local as well as global electrophysiological measurements, different anesthetics however differently affect neuronal spontaneous and evoked activity [ 12 ].…”