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Hahnloser, R. H. R.

Publications and source records attributed to Hahnloser, R. H. R..

6 recordsLinked to original sources

Neural population dynamics during sleep in a songbird vocal circuit resemble sharp wave ripple activity

Similar to motor skill learning in mammals, vocal learning in songbirds requires a set of interconnected brain areas that make up an analogous basal ganglia-thalamocortical circuit known as the anterior forebrain pathway (AFP). Although neural activity in the AFP has been extensively investigated during awake singing, very little is known about its neural activity patterns during other behavioral states. Here, we used chronically implanted Neuropixels probes to investigate spontaneous neural activity in the AFP during natural sleep and awake periods in male zebra finches. We found that during sleep, neuron populations in the pallial region LMAN (lateral magnocellular nucleus of the nidopallium) spontaneously exhibited synchronized bursts that were characterized by a negative sharp deflection in the local field potential (LFP) and a transient increase in gamma power. LMAN population bursts occurred primarily during non-rapid eye movement (NREM) sleep and were highly reminiscent of sharp-wave ripple (SWR) activity observed in rodent hippocampus. We also examined the functional connectivity within the AFP by calculating the pairwise LFP coherence. As expected, delta and theta band coherence within LMAN and Area X was higher during sleep compared to awake periods. Contrary to our expectations, we did not observe strong coherence between LMAN and Area X during sleep, suggesting that the input from LMAN into Area X is spatially restricted. Overall, these results provide the first description of spontaneous neural dynamics within the AFP across behavioral states. Significance statementAlthough cortical and basal ganglia circuits are known to be required for learning in both mammals and birds, little is known about the ongoing spontaneous activity patterns within these circuits, or how they are modulated by behavioral state. Here we prove the first description of cortical-basal ganglia network activity during sleep and awake periods in birds. Within the pallial area LMAN, we observed population-wide bursting events that were highly reminiscent of hippocampal sharp-wave ripple (SWR) activity, suggesting that large-scale population events have diverse functions across vertebrates.

neuroscience↗

Familiarity of an environment prevents song suppression in isolated zebra finches

Despite the wide use of zebra finches as an animal model to study vocal learning and production, little is known about impacts on their welfare caused by routine experimental manipulations such as changing their social context. Here we conduct a post-hoc analysis of singing rate, an indicator of positive welfare, to gain insights into stress caused by social isolation, a common experimental manipulation. We find that isolation in an unfamiliar environment reduces singing rate for several days, indicating the presence of an acute stressor. However, we find no such decrease when social isolation is caused by either removal of a social companion or by transfer to a familiar environment. Furthermore, during repeated brief periods of isolation, singing rate remains high when isolation is induced by removal of social companions, but it fails to recover from a suppressed state when isolation is induced by recurrent transfer to an unknown environment. These findings suggest that stress from social isolation is negligible compared to stress caused by environmental changes and that frequent short visits of an unfamiliar environment are detrimental rather than beneficial. Together, these insights can serve to refine experimental studies and design paradigms maximizing the birds wellbeing and vocal output.

zoology↗

Learning the action inventory of a complex skill via an intrinsic reward

Reinforcement learning (RL) is thought to underlie the acquisition of vocal skills like birdsong and speech, where sounding like ones "tutor" is rewarding. Yet, we find that the standard actor-critic RL model of birdsong learning fails to account for juvenile zebra finches efficient learning of an inventory of multiple syllables. But when we replace a single actor with multiple independent actors that jointly maximize a common intrinsic reward, then birds empirical learning trajectories are accurately reproduced. Importantly, the influence of each actor (syllable) on the magnitude of global reward is competitively determined by its acoustic similarity to target syllables. This leads to each actor matching the target it is closest to, and occasionally, to the competitive exclusion of an actor from the learning process (i.e., the learned song). We propose that a competitive-cooperative multi-actor (MARL) algorithm is key for the efficient learning of the action inventory of a complex skill.

animal behavior and cognition↗

Goal-directed vocal planning in a songbird

Songbirds vocal mastery is impressive, but to what extent is it a result of practice? Can they, based on experienced mismatch with a known target, plan the necessary changes to recover the target in a practice-free manner without intermittently singing? In adult zebra finches, we drive the pitch of a song syllable away from its stable (baseline) variant acquired from a tutor, then we withdraw reinforcement and subsequently deprive them of singing experience by muting or deafening. In this deprived state, birds do not recover their baseline song. However, they revert their songs towards the target by about one standard deviation of their recent practice, provided the sensory feedback during the latter signaled a pitch mismatch with the target. Thus, targeted vocal plasticity does not require immediate sensory experience, showing that zebra finches are capable of goal-directed vocal planning.

neuroscience↗

Sensory substitution reveals a manipulation bias

Sensory substitution is a promising therapeutic approach for replacing a missing or diseased sensory organ by translating inaccessible information into another sensory modality. What aspects of substitution are important such that subjects accept an artificial sense and that it benefits their voluntary action repertoire? To obtain an evolutionary perspective on affective valence implied in sensory substitution, we introduce an animal model of deaf songbirds. As a substitute of auditory feedback, we provide binary visual feedback. Deaf birds respond appetitively to song-contingent visual stimuli, they skillfully adapt their songs to increase the rate of visual stimuli, showing that auditory feedback is not required for making targeted changes to a vocal repertoire. We find that visually instructed song learning is basal-ganglia dependent. Because hearing birds respond aversively to the same visual stimuli, sensory substitution reveals a bias for actions that elicit feedback to meet animals manipulation drive, which has implications beyond rehabilitation.

neuroscience↗

Welfare of zebra finches used in research

Over the past 50 years, songbirds have become a valuable model organism for scientists studying vocal communication from its behavioral, hormonal, neuronal, and genetic perspectives. Many advances in our understanding of vocal learning result from research using the zebra finch, a close-ended vocal learner. We review some of the manipulations used in zebra finch research, such as isolate housing, transient/irreversible impairment of hearing/vocal organs, implantation of small devices for chronic electrophysiology, head fixation for imaging, aversive song conditioning using sound playback, and mounting of miniature backpacks for behavioral monitoring. We highlight the use of these manipulations in scientific research, and estimate their impact on animal welfare, based on the literature and on data from our past and ongoing work. The assessment of harm-benefits tradeoffs is a legal prerequisite for animal research in Switzerland. We conclude that a diverse set of known stressors reliably lead to suppressed singing rate, and that by contraposition, increased singing rate may be a useful indicator of welfare. We hope that our study can contribute to answering some of the most burning questions about zebra finch welfare in research on vocal behaviors.

animal behavior and cognition↗