SUMMARY Neurons in cortical circuits are often coactivated as ensembles, yet it is unclear whether ensembles play a functional role in behavior. Some ensemble neurons have pattern completion properties, triggering the entire ensemble when activated. Using two-photon holographic optogenetics in mouse primary visual cortex, we tested whether recalling ensembles by activating pattern completion neurons alters behavioral performance in a visual task. Disruption of behaviorally relevant ensembles by activation of non-selective neurons decreased performance, whereas activation of only two pattern completion neurons from behaviorally relevant ensembles improved performance, by reliably recalling the whole ensemble. Also, inappropriate behavioral choices were evoked by the mistaken activation of behaviorally relevant ensembles. Finally, in absence of visual stimuli, optogenetic activation of two pattern completion neurons could trigger behaviorally relevant ensembles and correct behavioral responses. Our results demonstrate a causal role of neuronal ensembles in a visually guided behavior and suggest that ensembles implement internal representations of perceptual states.
Neural processing of sensory information is strongly influenced by context. For instance, cortical responses are reduced to predictable stimuli, while responses are increased to novel stimuli that deviate from contextual regularities. Such bidirectional modulation based on preceding sensory context is likely a critical component or manifestation of attention, learning, and behavior, yet how it arises in cortical circuits remains unclear. Using volumetric two-photon calcium imaging and local field potentials in primary visual cortex (V1) from awake mice presented with visual “oddball” paradigms, we identify both reductions and augmentations of stimulus-evoked responses depending, on whether the stimulus was redundant or deviant, respectively. Interestingly, deviance-augmented responses were limited to a specific subset of neurons mostly in supragranular layers. These deviance-detecting cells were spatially intermixed with other visually responsive neurons and were functionally correlated, forming a neuronal ensemble. Optogenetic suppression of prefrontal inputs to V1 reduced the contextual selectivity of deviance-detecting ensembles, demonstrating a causal role for top-down inputs. The presence of specialized context-selective ensembles in primary sensory cortex, modulated by higher cortical areas, provides a circuit substrate for the brain’s construction and selection of prediction errors, computations which are key for survival and deficient in many psychiatric disorders.
Animal behavior has been studied for centuries, but few efficient methods are available to automatically identify and classify it. Quantitative behavioral studies have been hindered by the subjective and imprecise nature of human observation, and the slow speed of annotating behavioral data. Here, we developed an automatic behavior analysis pipeline for the cnidarian Hydra vulgaris using machine learning. We imaged freely behaving Hydra, extracted motion and shape features from the videos, and constructed a dictionary of visual features to classify pre-defined behaviors. We also identified unannotated behaviors with unsupervised methods. Using this analysis pipeline, we quantified 6 basic behaviors and found surprisingly similar behavior statistics across animals within the same species, regardless of experimental conditions. Our analysis indicates that the fundamental behavioral repertoire of Hydra is stable. This robustness could reflect a homeostatic neural control of "housekeeping" behaviors which could have been already present in the earliest nervous systems.
In neocortex, each sensory modality engages distinct primary and secondary areas that route information further to association areas. Where signal flow may converge for maintaining information in short-term memory and how behavior may influence signal routing remain open questions. Using wide-field calcium imaging, we compared cortexwide neuronal activity in layer 2/3 for mice trained in auditory and whisker-based tactile discrimination tasks with delayed response. In both tasks, mice were either active or passive during stimulus presentation, engaging in body movements or sitting quietly. Irrespective of behavioral strategy, auditory and tactile stimulation activated spatially segregated subdivisions of posterior parietal cortex (areas A and RL, respectively). In the subsequent delay period, in contrast, behavioral strategy rather than sensory modality determined where short-term memory was located: frontomedially in active trials and posterolaterally in passive trials. Our results suggest behavior-dependent routing of sensory-driven cortical information flow from modality-specific PPC subdivisions to higher association areas..
Highlights d Cellular resolution population recordings of mLOC in mice and humans d mLOC is associated with a decreased cortical repertoire of discriminable microstates d Neuronal ensemble fragmentation toward independent single neuron activity during mLOC
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