Experience-dependent coding of frequency-modulated trajectories by offsets in auditory cortex

Abstract

Frequency modulations are an inherent feature of many behaviorally relevant sounds, including vocalizations and music. Changing trajectories in a sound's frequency often conveys meaningful information, which can be used to differentiate sound categories, as in the case of intonations in tonal languages. However, it is not clear what features of the neural responses in what parts of the auditory cortical pathway might be more important for conveying information about behaviorally relevant frequency modulations, and how these responses change with experience. Here we uncover tuning to subtle variations in frequency trajectories in mouse auditory cortex. Surprisingly, we found that auditory cortical responses could be modulated by variations in a pure tone trajectory as small as 1/24th of an octave. Offset spiking accounted for a significant portion of tuned responses to subtle frequency modulation. Offset responses that were present in the adult A2, but not those in Core auditory cortex, were plastic in a way that enhanced the representation of an acquired behaviorally relevant sound category, which we illustrate with the maternal mouse paradigm for natural communication sound learning. By using this ethologically inspired sound-feature tuning paradigm to drive auditory responses in higher-order neurons, our results demonstrate that auditory cortex can track much finer frequency modulations than previously appreciated, which allows A2 offset responses in particular to attune to the pitch trajectories that distinguish behaviorally relevant, natural sound categories. Frequency trajectory conveys meaning across many sounds, from environmental noises to vocalizations and music. In human speech, pitch modulation conveys expressive and linguistic meaning, especially in tonal languages [1][2][3][4]. In music, emotional meaning can be conveyed through pitch modulation [5]. In many species, such as birds, rodents, monkeys, dogs, and even some marine animals, the temporal features of a vocalization, including its pitch trajectory, vary by context, and can express the intention as well as identity of a vocalizer [6][7][8][9][10]. Intonation-sensitive brain areas have been reported in the human auditory cortex using subdural electrophysiology [11], and the ability to process and recognize pitch trajectory in vocalizations can be shaped by experience [12][13][14]. However, the temporal or spatial resolution of methods used in human studies are coarse compared to the rate at which neurons in the auditory system respond, as well as to the time scale of many intonations, leaving still unclear the neural mechanisms for tuning to the frequency modulations in natural sounds.Frequency modulation encoding at the single neuron level in Core auditory cortex has been studied with directional sweeps or long duration sinusoidal modulations [15][16][17][18][19][20]. Offset responses are particularly selective for linear sweep direction [21], while entrained periodic firing can encode the onsets of the multiple cycles in up to 20 Hz sinusoida...

Maternal Experience-Dependent Cortical Plasticity in Mice Is Circuit- and Stimulus-Specific and Requires MECP2

“…We also found that some aspects of the surrogacy-induced plasticity that we observed here were most prominent in the late phase of the response to calls. Interestingly, this observation bears similarity to a recent report that secondary auditory cortex (A2) neurons show maternal plasticity in offset responses to frequencymodulated stimuli (Chong et al, 2019). Nevertheless, we are confident that this effect does not bear on our data because our recordings were made in more dorsal thalamo-recipient auditory cortical areas, not in A2.…”