Auditory Thalamostriatal and Corticostriatal Pathways Convey Complementary Information about Sound Features.

Multiple parallel neural pathways link sound-related signals to behavioral responses. For instance, the striatum, a brain structure involved in action selection and reward-related learning, receives neuronal projections from both the auditory thalamus and auditory cortex. It is not clear whether sound information that reaches the striatum through these two pathways is redundant or complementary. We used an optogenetic approach in awake mice of both sexes to identify thalamostriatal and corticostriatal neurons during extracellular recordings, and characterized neural responses evoked by sounds of different frequencies and amplitude modulation rates. We found that neurons in both pathways encode sound frequency with similar fidelity, but display different coding strategies for amplitude modulated noise. Whereas corticostriatal neurons provide a more accurate representation of amplitude modulation rate in their overall firing rate, thalamostriatal neurons convey information about the precise timing of acoustic events. These results demonstrate that auditory thalamus and auditory cortex neurons provide complementary information to the striatum, and suggest that these pathways could be differentially recruited depending on the requirements of a sound-driven behavior.SIGNIFICANCE STATEMENT Sensory signals from the cerebral cortex and the thalamus converge onto the striatum, a nucleus implicated in reward-related learning. It is not clear whether these two sensory inputs convey redundant or complementary information. By characterizing the sound-evoked responses of thalamostriatal and corticostriatal neurons, our work demonstrates that these neural pathways convey complementary information about the temporal features of sounds. This work opens new avenues for investigating how these pathways could be selectively recruited depending on task demands, and provides a framework for studying convergence of cortical and thalamic information onto the striatum in other sensory systems.

Experience shapes activity dynamics and stimulus coding of VIP inhibitory cells.

Cortical circuits can flexibly change with experience and learning, but the effects on specific cell types, including distinct inhibitory types, are not well understood. Here we investigated how excitatory and VIP inhibitory cells in layer 2/3 of mouse visual cortex were impacted by visual experience in the context of a behavioral task. Mice learned a visual change detection task with a set of eight natural scene images. Subsequently, during 2-photon imaging experiments, mice performed the task with these familiar images and three sets of novel images. Strikingly, the temporal dynamics of VIP activity differed markedly between novel and familiar images: VIP cells were stimulus-driven by novel images but were suppressed by familiar stimuli and showed ramping activity when expected stimuli were omitted from a temporally predictable sequence. This prominent change in VIP activity suggests that these cells may adopt different modes of processing under novel versus familiar conditions.

Stable representation of sounds in the posterior striatum during flexible auditory decisions.

The neuronal pathways that link sounds to rewarded actions remain elusive. For instance, it is unclear whether neurons in the posterior tail of the dorsal striatum (which receive direct input from the auditory system) mediate action selection, as other striatal circuits do. Here, we examine the role of posterior striatal neurons in auditory decisions in mice. We find that, in contrast to the anterior dorsal striatum, activation of the posterior striatum does not elicit systematic movement. However, activation of posterior striatal neurons during sound presentation in an auditory discrimination task biases the animals' choices, and transient inactivation of these neurons largely impairs sound discrimination. Moreover, the activity of these neurons during sound presentation reliably encodes stimulus features, but is only minimally influenced by the animals' choices. Our results suggest that posterior striatal neurons play an essential role in auditory decisions, and provides a stable representation of sounds during auditory tasks.

The role of sensory cortex in behavioral flexibility.

To thrive in a changing environment, organisms evolved strategies for rapidly modifying their behavioral responses to sensory stimuli. In this review, we investigate the role of sensory cortical circuits in these flexible behaviors. First, we provide a framework for classifying tasks in which flexibility is required. We then present studies in animal models which demonstrate that responses of sensory cortical neurons depend on the expected outcome associated with a stimulus. Last, we discuss inactivation studies which indicate that sensory cortex facilitates behavioral flexibility, but is not always required for adapting to changes in environmental conditions. This analysis provides insights into the contributions of cortical and subcortical sensory circuits to flexibility in behavior.