Context-dependent processing of natural sounds in the bat cortex
Authors:   , Lopez Jury Luciana 
Published: September 2023

Bats use sounds for echolocation and communication. In the bat auditory cortex there are neurons that process species-specific calls associated to both behaviours (Kanwal, 1999). Although several studies have shown neural specializations coding for echolocation and communication calls separately, how these multifunctional neurons respond to combinations of both type of vocalizations remains unknown. In natural soundscapes of bats, silence is rare; each vocalization is likely to be heard in a context of several other conspecifics calls. In the first part of this thesis, I show that two neuronal populations of multifunctional neurons coexist in the bat cortex, including neurons that discriminate social from echolocation sounds well (selective) and neurons that are equally driven by these two ethologically different calls (non-selective). The selectivity of these neurons was highly affected by the preceding acoustic context in which the calls were heard. Non-selective neurons become selective specially to the transitions between sound categories and selective neurons turn into non-selective ones in acoustic contexts. In general, the presence of contexts leads to an overall response suppression, but the strength of this suppression is stimulus-specific. Suppression is strongest when context and target sounds belong to the same category. This special sensitivity for sounds that differ from the preceding stimulus statistics resembles a conspicuous phenomenon called stimulus-specific adaptation (SSA) (Nelken, 2014). I show that a computational model similar to those used for explaining SSA in rodents can account for the responses observed in the bat cortex to natural sounds. The model depends on segregated feedforward inputs, synaptic depression, and postsynaptic neuronal adaptation. All of these results were obtained from awake animals. However, substantial knowledge in auditory information processing in bats has been, and still is, obtained from anaesthetized preparations. Therefore, a question of paramount importance emerges: how can we relate results from recordings in anaesthetized animals to those obtained in wakefulness. In the second part of this thesis, I modify the available awake model inspired in known effects of anaesthesia on auditory processing. To test the predictions of the model, I performed in vivo experiments under anaesthesia replicating the paradigm of stimulation used in awake bats. In combination with the model, the experimental results suggest that the known effects of anaesthesia on cortical responses to sounds are not enough to explain my experimental results. The effect of anaesthesia on context-dependent processing of vocalizations turns to be asymmetric between echolocation and communication. Anaesthesia affects mostly context-dependent effects related to communication signals. A model that reproduces the data proposes that anaesthesia does not affect uniformly the neurons’ responsiveness but has frequency-specific effects in the feedforward pathway to auditory cortex. Anaesthesia decreases activity of cortical inputs tuned to high-frequency sounds, increases synaptic depression in the respective cortical synapses and “slows down” the adaptation to constant stimulation of cortical neurons. In the last part of this thesis, I change the focus towards higher-order areas of the cortex: the frontal auditory field (FAF). The FAF is an auditory region of the frontal lobe of the cortex of bats much less explored than the auditory cortex. It has been discussed a possible role of the FAF in novelty detection, sensorimotor integration and vocal production (Esser & Eiermann, 2004; Garcia-Rosales et al., 2022). Although it has been shown that this field in the frontal lobe receives the major input from the auditory cortex (Kobler et al., 1987), a description of the synaptic properties between these two auditory regions is absent. To answer this, I characterized quantitatively the response properties of auditory neurons found in the bat FAF and auditory cortex to simple sounds (pure tones). The results show that frontal neurons are responsive to sounds, and compared to auditory cortex neurons, they present sparser, less precise spiking and longer-lasting responses. By means of computational modelling, I show that slow and subthreshold synaptic dynamics can reproduce the activity pattern of neurons in the FAF. To further explore the role of the FAF in novelty detection, I incorporate frontal neurons into the previous model of cortical multifunctional neurons. Simulations show that deviance detection is transferred from auditory cortex to frontal neurons with changes in the spiking pattern. Stronger responses to deviants last longer in frontal neurons suggesting that these neurons could integrate arriving inputs at longer latencies together with the deviants in the acoustic stream. These properties resonate well with the general function of the frontal cortex of integrating over long time windows.