bioRxiv Science⌕ Search

Biology subjects

Quass, G. L.

Publications and source records attributed to Quass, G. L..

3 recordsLinked to original sources

Mixed representations of sound and action in the auditory midbrain

Linking sensory input and its consequences is a fundamental brain operation. Accordingly, neural activity of neo-cortical and limbic systems often reflects dynamic combinations of sensory and behaviorally relevant variables, and these "mixed representations" are suggested to be important for perception, learning, and plasticity. However, the extent to which such integrative computations might occur in brain regions upstream of the forebrain is less clear. Here, we conduct cellular-resolution 2-photon Ca2+ imaging in the superficial "shell" layers of the inferior colliculus (IC), as head-fixed mice of either sex perform a reward-based psychometric auditory task. We find that the activity of individual shell IC neurons jointly reflects auditory cues and mices actions, such that trajectories of neural population activity diverge depending on mices behavioral choice. Consequently, simple classifier models trained on shell IC neuron activity can predict trial-by-trial outcomes, even when training data are restricted to neural activity occurring prior to mices instrumental actions. Thus in behaving animals, auditory midbrain neurons transmit a population code that reflects a joint representation of sound and action. Significance StatementNeurons in ICs superficial "shell" layers preferentially project to higher-order thalamic nuclei that are strongly activated by sounds and their behavioral consequences. This integrative computation is thought critical for a variety of behaviorally relevant functions, such as establishing learned sound valence. However, whether such "mixed representations" reflect unique properties of thalamocortical networks, or rather are inherited from afferent inputs, is unclear. We show that in behaving mice, many shell IC neurons are modulated by sounds and mices actions. Consequently, shell IC population activity suffices to predict behavioral outcomes even prior to the goal-directed action. Our data thus establish shell IC nuclei as a novel, ascending source of mixed representations for the thalamocortical system.

neuroscience↗

Population coding of time-varying sounds in the non-lemniscal Inferior Colliculus

The inferior colliculus (IC) of the midbrain is important for complex sound processing, such as discriminating conspecific vocalizations and human speech. The ICs non-lemniscal, dorsal "shell" region is likely important for this process, as neurons in these layers project to higher-order thalamic nuclei that subsequently funnel acoustic signals to the amygdala and non-primary auditory cortices; forebrain circuits important for vocalization coding in a variety of mammals, including humans. However, the extent to which shell IC neurons transmit acoustic features necessary to discern vocalizations is less clear, owing to the technical difficulty of recording from neurons in the ICs superficial layers via traditional approaches. Here we use 2-photon Ca2+ imaging in mice of either sex to test how shell IC neuron populations encode the rate and depth of amplitude modulation, important sound cues for speech perception. Most shell IC neurons were broadly tuned, with a low neurometric discrimination of amplitude modulation rate; only a subset were highly selective to specific modulation rates. Nevertheless, neural network classifier trained on fluorescence data from shell IC neuron populations accurately classified amplitude modulation rate, and decoding accuracy was only marginally reduced when highly tuned neurons were omitted from training data. Rather, classifier accuracy increased monotonically with the modulation depth of the training data, such that classifiers trained on full-depth modulated sounds had median decoding errors of [~]0.2 octaves. Thus, shell IC neurons may transmit time-varying signals via a population code, with perhaps limited reliance on the discriminative capacity of any individual neuron. Significance StatementThe ICs shell layers originate a "non-lemniscal" pathway whose first- and second-order targets are thought important for perceiving conspecific vocalizations and human speech. However, prior studies suggest that individual shell IC neurons are broadly tuned and have high response thresholds, implying a limited reliability of efferent signals. Here we use Ca2+ imaging to test how shell IC neurons encode amplitude modulation, a key sound cue for speech perception and stream segregation. We show that the rate and depth of amplitude modulation is accurately represented in the ensemble activity of shell IC neuron populations. Thus, downstream targets can read out a sounds temporal envelope from a distributed rate code transmitted by populations of broadly tuned neurons.

neuroscience↗

Auditory corticofugal neurons transmit non-auditory signals to support discriminative learning

Layer 5 pyramidal neurons of sensory cortices project "corticofugal" axons to myriad sub-cortical targets, thereby broadcasting high-level signals important for perception and learning. Recent studies suggest dendritic Ca2+ spikes as key biophysical mechanisms supporting corticofugal neuron function: These long-lasting events drive burst firing, thereby initiating uniquely powerful signals to modulate sub-cortical representations and trigger learning-related plasticity. However, the behavioral relevance of corticofugal dendritic spikes is poorly understood. We shed light on this issue using 2-photon Ca2+ imaging of auditory corticofugal dendrites as mice of either sex engage in a GO/NO-GO sound-discrimination task. Unexpectedly, only a minority of dendritic spikes were triggered by behaviorally relevant sounds under our conditions. Task related dendritic activity instead mostly followed sound cue termination and co-occurred with mices instrumental licking during the answer period of behavioral trials, irrespective of reward consumption. Temporally selective, optogenetic silencing of corticofugal neurons during the trial answer period impaired auditory discrimination learning. Thus, auditory corticofugal systems contribution to learning and plasticity may be partially non-sensory in nature. Significance StatementThe auditory cortex sends a massive "feedback" projection to the inferior colliculus (IC) which controls IC neuron plasticity and some types of perceptual learning. Precisely what signals are fed back during behavior is unclear. Using multiphoton imaging of auditory cortico-collicular neurons as mice engage in a sound discrimination task, we find that activity coincides more with mices instrumental actions rather than sound cues. Dendritic Ca2+ spikes and burst firing contributed to this non-auditory activity, which is notable given that dendritic spikes instruct synaptic plasticity in many other circuits. Accordingly, optogenetic silencing of corticofugal neurons during mices instrumental actions impaired discriminative learning. Auditory corticofugal neurons may thus transmit significant non-auditory information that contributes to learning-related plasticity.

neuroscience↗