Experience-Dependent Coding of Time-Dependent Frequency Trajectories by Off Responses in Secondary Auditory Cortex

Abstract

Time-dependent frequency trajectories are an inherent feature of many behaviorally relevant sounds, such as species-specific vocalizations. Dynamic frequency trajectories, even in short sounds, often convey meaningful information, which may be used to differentiate sound categories. However, it is not clear what and where neural responses in the auditory cortical pathway are critical for conveying information about behaviorally relevant frequency trajectories, and how these responses change with experience. Here, we uncover tuning to subtle variations in frequency trajectories in auditory cortex of female mice. We found that auditory cortical responses could be modulated by variations in a pure tone trajectory as small as 1/24th of an octave, comparable to what has been reported in primates. In particular, late spiking after the end of a sound stimulus was more often sensitive to the sound's subtle frequency variation compared to spiking during the sound. Such "Off" responses in the adult A2, but not those in core auditory cortex, were plastic in a way that may enhance the representation of a newly acquired, behaviorally relevant sound category. We illustrate this with the maternal mouse paradigm for natural vocalization learning. By using an ethologically inspired paradigm to drive auditory responses in higher-order neurons, our results demonstrate that mouse auditory cortex can track fine frequency changes, which allows A2 Off responses in particular to better respond to pitch trajectories that distinguish behaviorally relevant, natural sound categories.

Systematic analysis of goal‐related movement sequences during maternal behaviour in a female mouse model for Rett syndrome

“…Traditionally, these behavioural studies were quantified using qualitative “spot checks”, observations without disturbing the nest and cage (of 15 min or lesser), and later studies with short intervals of disturbances to induce pup retrieval or other maternal behaviours. These studies paved the way for more recent optogenetics experiments to perturb neural circuitry and molecular/cellular analysis to determine genes and cell types involved in maternal behaviour (Bendesky et al., 2017; Chen et al., 2019; Chong et al., 2020; Fang et al., 2018; Kohl et al., 2018; Krishnan et al., 2017; Lau, Krishnan, et al., 2020; Lau, Layo, et al., 2020; Li et al., 2019; Maynard et al., 2018; Moffitt et al., 2018; Niv et al., 2015; Tasaka et al., 2018; Wu et al., 2014). However, due to limited person power and/or due to reductionist views to focus on particular behaviours, only certain aspects of the dynamic behaviour were noted and discrete end‐point analysis (such as time to retrieve pups, nesting and errors in retrieval) performed in most studies.…”

Enhanced Discriminative Abilities of Auditory Cortex Neurons for Pup Calls Despite Reduced Evoked Responses in C57BL/6 Mother Mice

“…Among many acoustic cues, the rising slope of an acoustic stimulus can change the response strength and its latency (Heil 1997a(Heil , b, 2011. In our case, the very sharp rising slope of the adult and pup calls (1-5ms) or subtle variations in the frequency trajectory of the calls (Chong et al 2020) could promote responses even if the neuron CF is far from the spectral content of the vocalizations.…”

Emergence and function of cortical offset responses in sound termination detection

“…Another approach to understand the behavioural role of auditory offset responses could be to study where the AAF is projecting and what could be the use of offset responses in these areas. It was previously shown that offset responses in the secondary auditory cortex are plastic and able to enhance the representation of a newly acquired, behaviourally relevant sound category (Chong et al, 2020). Whether the activity of AAF neurons is crucial for this plasticity to happen remains to be elucidated.…”

“…Together, these quantifications confirm that the neuronal responses measured at sound termination are not affected by the weak and short spectral splatter caused by a fast offset ramp. In the future, the role of offset responses in detecting sound termination should be studied in natural environments, using for example vocalization calls (Chong et al, 2020). This would tell if the auditory system, and the MGB or the AAF more specifically, evolved in a way to meet the challenges of detecting naturally terminating sounds.…”