Search bioRxiv⌕ Search

Biology subjects

Safaryan, K.

Publications and source records attributed to Safaryan, K..

5 recordsLinked to original sources

Attentional modulation of persistent visual representations after stimulus offset is coordinated across primary visual and anterior cingulate cortices

Flexible behavior in complex environments requires animals to infer which sensory inputs are relevant for guiding action and which need to be ignored. Yet, how cognitive control circuits apply contextual knowledge during decision-making is poorly understood. To address this question, we trained head-fixed mice on a cross-modal, context-dependent two-alternative forced-choice (2-AFC) decision-making task. In this task, animals simultaneously received visual and auditory inputs, and the behaviorally relevant modality switched covertly between blocks of trials, requiring animals to infer rule changes from reward feedback alone. Mice successfully adapted their behavior after rule switches and recovered to expert performance. Using simultaneous Neuropixels recordings in the primary visual cortex (V1) and the anterior cingulate cortex (ACC) during task performance, we found that neuronal responses in both regions showed mixed selectivity, multiplexing sensory, choice, and outcome signals. However, V1 neural responses more strongly encoded visual stimulus orientation, while ACC neural responses preferentially encoded outcome. Population decoding further revealed that V1 and ACC neurons maintained a persistent representation of task context throughout the trial, occupying a subspace approximately orthogonal to visual stimulus coding. This contextual representation strengthened progressively as mice adapted their behavior following each switch. Critically, context representations emerged in parallel in V1 and ACC, and decoding accuracies in these two regions were strongly correlated with each other and with behavioral performance across trial blocks. Orthogonal to this shared emergent and sustained context signal, visual stimulus decoding was enhanced when vision was task-relevant. This attentional enhancement in V1 occurred not only during the stimulus presentation period but also after stimulus offset. Similarly, in ACC, a persistent increase of visual stimulus identity encoding in visually relevant session blocks was present after stimulus offset. Taken together, these findings reveal a distributed, inter-areal representation of task context spanning sensory and frontal cortices, suggesting that V1 and ACC contribute to maintaining task-relevant sensory information beyond the immediate sensory response period to provide a circuit-level mechanism for cross-modal attentional control.

neuroscience↗

Shifts in attention drive context-dependent subspace encoding in anterior cingulate cortex during decision making

Attention is a cognitive faculty that selects part of a larger set of percepts, driven by cues such as stimulus saliency, internal goals or priors. The enhancement of the attended representation and inhibition of distractors have been proposed as potential neural mechanisms driving this selection process. Yet, how attention operates when the cue has to be internally constructed from conflicting stimuli, decision rules, and reward contingencies, is less understood. Here we recorded from populations of neurons in the anterior cingulate cortex (ACC), an area implicated in ongoing error monitoring and correction during decision conflicts, in a challenging attention-shifting task. In this task, mice had to attend to the rewarded modality when presented identical auditory and visual stimuli in two contexts without direct external cues. In the ACC, the irrelevant stimulus continuously became less decodable than the relevant stimulus as the trial progressed to the decision point. This contrasted strongly with our previous findings in V1 where both relevant and irrelevant stimuli were equally decodable throughout the trial. Using analytical tools and a recurrent neural network (RNN) model, we found that the linearly independent representation of stimulus modalities in ACC was well suited to context-gated suppression of a stimulus modality. We demonstrated that the feedback structure of lateral connections in the RNN consisted of excitatory interactions between cell ensembles representing the same modality and mutual inhibition between cell ensembles representing distinct stimulus modalities. Using this RNN model showing signatures of context-gated suppression, we predicted that the level of contextual modulation of individual neurons should be correlated with their relative responsiveness to the two stimulus modalities used in the task. We verified this prediction in recordings from ACC neurons but not from recordings from V1 neurons. Therefore, ACC effectively operates on low-dimensional neuronal subspaces to combine stimulus related information with internal cues to drive actions under conflict.

neuroscience↗

Correlated signatures of social behavior in cerebellum and anterior cingulate cortex

The cerebellum has been implicated in the regulation of social behavior. Its influence is thought to arise from communication, via the thalamus, to forebrain regions integral in the expression of social interactions, including the anterior cingulate cortex (ACC). However, the signals encoded or the nature of the communication between the cerebellum and these brain regions is poorly understood. Here, we describe an approach that overcomes technical challenges in exploring the coordination of distant brain regions at high temporal and spatial resolution during social behavior. We developed the E-Scope, an electrophysiology-integrated miniature microscope, to synchronously measure extracellular electrical activity in the cerebellum along with calcium imaging of the ACC. This single coaxial cable device combined these data streams to provide a powerful tool to monitor the activity of distant brain regions in freely behaving animals. During social behavior, we recorded the spike timing of multiple single units in cerebellar right Crus I (RCrus I) Purkinje cells (PCs) or dentate nucleus (DN) neurons while synchronously imaging calcium transients in contralateral ACC neurons. We found that during social interactions a significant subpopulation of cerebellar PCs were robustly inhibited, while most modulated neurons in the DN were activated, and their activity was correlated with positively modulated ACC neurons. These distinctions largely disappeared when only non-social epochs were analyzed suggesting that cerebellar-cortical interactions were behaviorally specific. Our work provides new insights into the complexity of cerebellar activation and co-modulation of the ACC during social behavior and a valuable open-source tool for simultaneous, multimodal recordings in freely behaving mice.

neuroscience↗

Continuous multiplexed population representations of task context in the mouse primary visual cortex

Primary visual cortex (V1) neurons integrate motor and multisensory information with visual inputs during sensory processing. However, whether V1 neurons also integrate and encode higher-order cognitive variables is less understood. We trained mice to perform a context-dependent cross-modal decision task where the interpretation of identical audio-visual stimuli depends on task context. We performed silicon probe population recordings of neuronal activity in V1 during task performance and showed that task context (whether the animal should base its decision on visual or auditory stimuli) can be decoded during both intertrial intervals and stimulus presentations. Context and visual stimuli were represented in overlapping populations but were orthogonal in the population activity space. Context representation was not static but displayed distinctive dynamics upon stimulus onset and offset. Thus, activity patterns in V1 independently represent visual stimuli and cognitive variables relevant to task execution.

neuroscience↗

Enhanced hippocampal theta rhythmicity and emergence of eta oscillation in virtual reality

Hippocampal theta oscillations in rodents profoundly impact neural activity, spatial coding, and synaptic plasticity and learning. What are the sensory mechanisms governing slow oscillations? We hypothesized that the nature of multisensory inputs is a crucial factor in hippocampal rhythmogenesis. We compared the rat hippocampal slow oscillations in the multisensory-rich real world (RW) and in a body-fixed, visual virtual reality (VR). The amplitude and rhythmicity of the hippocampal ~8 Hz theta were enhanced in VR compared to RW. This was accompanied by the emergence of a ~4 Hz oscillation, termed the eta rhythm, evident in the local field potential (LFP) in VR, but not in RW. Similar to theta, eta band amplitude increased with running speed in VR, but not in RW. However, contrary to theta, eta amplitude was highest in the CA1 cell layer, implicating intra-CA1 mechanisms. Consistently, putative CA1 interneurons, but not pyramidal neurons, showed substantially more eta modulation in VR than in RW. These results elucidate the multisensory mechanisms of hippocampal rhythms and the surprising effects of VR on enhancing these rhythms, which has not been achieved pharmacologically and has significant broader implications for VR use in humans. One Sentence SummaryNavigation in virtual reality greatly enhances hippocampal 8Hz theta rhythmicity, and generates a novel, ~4Hz eta rhythm that is localized in the CA1 cell layer and influences interneurons more than pyramidal neurons.

neuroscience↗