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Combined behavioral and neural investigations of pup retrieval. a neural code for pup call representations in the mouse auditory cortex
Combined behavioral and neural investigations of pup retrieval. a neural code for pup call representations in the mouse auditory cortex
The ability to adequately adapt to a dramatically changing environment is crucial for an animal’s survival. When female mice give birth to their offspring, their environment changes drastically and they immediately need to care for the offspring, thereby ensuring the offspring’s wellbeing. Pups completely transform the environment around the mouse, triggering a number of new behaviors, as they provide a slew of new sensory inputs, including tactile and olfactory, but also auditory. Pups emit ultrasonic vocalizations (USVs) when isolated outside the nest, triggering retrieval behavior in mothers (MTs). After pups have returned to the nest and are cared for, the USV emission ceases. Interestingly, not only MTs but also virgin mice can perform pup retrieval, provided that they either have experience with pups in their home cage or are repeatedly exposed to pups in a pup retrieval task. Those two animal groups are referred to as experienced (EVs) and naive virgins (NVs). Studies have shown that excitatory neurons in the auditory cortex of MTs and EVs respond more strongly to pup calls over time. However, these studies have been performed under head-restrained unnatural conditions. Here, we provide a framework in which MTs, EVs and NVs retrieve pups in a semi-natural, freely behaving setting. During the experiment, they carry a head-mounted miniscope that allows for imaging neural activity in multiple neurons in the auditory cortex. The entire multisensory scenery is therefore accessible to mice, which was shown to impact auditory responses to pup calls. In our study, we show differences in behavioral performances of these three groups, with MTs displaying the most skilled and fine-tuned pup retrieval behavior, already highly effective during the final pregnancy stage. EVs show slightly reduced pup retrieval abilities, but superior to NVs, which retrieve pups effectively only after a few days. Additionally, we discovered that not only pups emitted USVs, but also adult mice vocalized. Intriguingly, they vocalized significantly more when pups were present in the behavioral arena, as compared to when they were alone. Clear pup call responsive neurons in the auditory cortex of all groups were scarce. Nevertheless, the overall neuronal population showed significant responses to pup calls at least in MTs, less so in EVs and least pronounced in NVs. Strikingly, other more global and behaviorally relevant events, such as pup retrievals and nest entries and exits, showed a distinct neural signature. Despite the scarcity of clear single cell responses to pup calls, the population of auditory cortex neurons carried information about pup call presence throughout all sessions in all groups, measured by a decoding analysis. This population code could be described as a sparse and dynamic code containing a few highly informative neurons, i.e. high weight neurons, that carried most of the decoding weight in a given session. This sparsity was most pronounced in MTs and least so in NVs. Besides, these high weight neurons were largely non-overlapping with high weight neurons for other non-pup call related event types. When relating single trial pup call decoding accuracies with the associated behavioral performance in a given trial, we could identify a significant relationship in EVs that was absent in MTs and NVs, suggesting that improved single trial decoding accuracies were linked to improved pup retrieval abilities. Altogether, this study shows how different pup exposure regimes can affect the learning of an essential offspring caring behavior and, that these different learning types differently enhance the neural representations of associated sensory cues.
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Gross, Isa-Maria
2021
English
Universitätsbibliothek der Ludwig-Maximilians-Universität München
Gross, Isa-Maria (2021): Combined behavioral and neural investigations of pup retrieval: a neural code for pup call representations in the mouse auditory cortex. Dissertation, LMU München: Faculty of Biology
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Abstract

The ability to adequately adapt to a dramatically changing environment is crucial for an animal’s survival. When female mice give birth to their offspring, their environment changes drastically and they immediately need to care for the offspring, thereby ensuring the offspring’s wellbeing. Pups completely transform the environment around the mouse, triggering a number of new behaviors, as they provide a slew of new sensory inputs, including tactile and olfactory, but also auditory. Pups emit ultrasonic vocalizations (USVs) when isolated outside the nest, triggering retrieval behavior in mothers (MTs). After pups have returned to the nest and are cared for, the USV emission ceases. Interestingly, not only MTs but also virgin mice can perform pup retrieval, provided that they either have experience with pups in their home cage or are repeatedly exposed to pups in a pup retrieval task. Those two animal groups are referred to as experienced (EVs) and naive virgins (NVs). Studies have shown that excitatory neurons in the auditory cortex of MTs and EVs respond more strongly to pup calls over time. However, these studies have been performed under head-restrained unnatural conditions. Here, we provide a framework in which MTs, EVs and NVs retrieve pups in a semi-natural, freely behaving setting. During the experiment, they carry a head-mounted miniscope that allows for imaging neural activity in multiple neurons in the auditory cortex. The entire multisensory scenery is therefore accessible to mice, which was shown to impact auditory responses to pup calls. In our study, we show differences in behavioral performances of these three groups, with MTs displaying the most skilled and fine-tuned pup retrieval behavior, already highly effective during the final pregnancy stage. EVs show slightly reduced pup retrieval abilities, but superior to NVs, which retrieve pups effectively only after a few days. Additionally, we discovered that not only pups emitted USVs, but also adult mice vocalized. Intriguingly, they vocalized significantly more when pups were present in the behavioral arena, as compared to when they were alone. Clear pup call responsive neurons in the auditory cortex of all groups were scarce. Nevertheless, the overall neuronal population showed significant responses to pup calls at least in MTs, less so in EVs and least pronounced in NVs. Strikingly, other more global and behaviorally relevant events, such as pup retrievals and nest entries and exits, showed a distinct neural signature. Despite the scarcity of clear single cell responses to pup calls, the population of auditory cortex neurons carried information about pup call presence throughout all sessions in all groups, measured by a decoding analysis. This population code could be described as a sparse and dynamic code containing a few highly informative neurons, i.e. high weight neurons, that carried most of the decoding weight in a given session. This sparsity was most pronounced in MTs and least so in NVs. Besides, these high weight neurons were largely non-overlapping with high weight neurons for other non-pup call related event types. When relating single trial pup call decoding accuracies with the associated behavioral performance in a given trial, we could identify a significant relationship in EVs that was absent in MTs and NVs, suggesting that improved single trial decoding accuracies were linked to improved pup retrieval abilities. Altogether, this study shows how different pup exposure regimes can affect the learning of an essential offspring caring behavior and, that these different learning types differently enhance the neural representations of associated sensory cues.