Abstract
Experimental evidence supports that cortical oscillations represent multiscale temporal modulations existent in natural stimuli, yet little is known about the processing of these multiple timescales at a neuronal level. Here, using extracellular recordings from the auditory cortex (AC) of awake bats (Carollia perspicillata), we show the existence of three neuronal types which represent different levels of the temporal structure of conspecific vocalizations, and therefore constitute direct evidence of multiscale temporal processing of naturalistic stimuli by neurons in the AC. These neuronal subpopulations synchronize differently to local-field potentials, particularly in theta- and high frequency bands, and are informative to a different degree in terms of their spike rate. Interestingly, we also observed that both low and high frequency cortical oscillations can be highly informative about the listened calls. Our results suggest that multiscale neuronal processing allows for the precise and non-redundant representation of natural vocalizations in the AC.
Highlights
Experimental evidence supports that cortical oscillations represent multiscale temporal modulations existent in natural stimuli, yet little is known about the processing of these multiple timescales at a neuronal level
Is the multiscale temporal structure of distress vocalizations represented by cortical neurons, or are phenomena such as neuronal suppression or phase-locking limitations hindering it? These two phenomena affect neuronal responses by preventing activation to sounds presented at fast rates (> 10–30 Hz)[25,26]
We report five main findings: (i) different units in the auditory cortex (AC) represent different levels of the temporal structure of natural calls; (ii) neuronal spiking synchronizes differently to ongoing local-field potentials (LFPs), depending on which temporal features of the natural sequences the units are able to encode; (iii) the information content in spiking rate depends on which timescale of the sequences is encoded by the units; (iv) the phase of low and high frequency LFPs is informative about the perceived acoustic streams; and (v) paired neuronal responses in the AC convey independent information, in consonance with the observed functional segregation
Summary
Experimental evidence supports that cortical oscillations represent multiscale temporal modulations existent in natural stimuli, yet little is known about the processing of these multiple timescales at a neuronal level. Experimental evidence indicates that electrophysiological oscillations in the human AC can represent different timescales existing in speech sounds, allowing the simultaneous processing of the syllabic rate (at rhythms of 4–8 Hz, consistent with theta-band oscillations), and the phonemic rate (rhythms of >30 Hz, consistent with gamma-band fluctuations)[19,20,21] Such multiscale processing at distinct frequencies is well explored in humans, little is known regarding the representation of different vocalization timescales in other mammals, especially at a neuronal level in the cortex. We aimed to bridge this gap by recording electrophysiological activity from the AC of the bat Carollia perspicillata in response to natural distress sequences, comprising at least two different timescales: the syllabic rate and the bout rate Both the AC and the distress communication repertoire of this species have been well investigated[3,4,22,23,24], making it a suitable model for studying the specifics of auditory temporal processing in the brain. Spike–LFP coupling has been extensively studied in the visual and somatosensory systems[31,32,33,34], the interactions between these signals in the auditory modality during communication call processing is less clear
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