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Avila, E.

Publications and source records attributed to Avila, E..

6 recordsLinked to original sources

Dynamical Latent State Computation in the Posterior Parietal Cortex

Success in many real-world tasks depends on our ability to dynamically track hidden states of the world. To understand the underlying neural computations, we recorded brain activity in posterior parietal cortex (PPC) of monkeys navigating by optic flow to a hidden target location within a virtual environment, without explicit position cues. In addition to sequential neural dynamics and strong interneuronal interactions, we found that the hidden state - monkeys displacement from the goal - was encoded in single neurons, and could be dynamically decoded from population activity. The decoded estimates predicted navigation performance on individual trials. Task manipulations that perturbed the world model induced substantial changes in neural interactions, and modified the neural representation of the hidden state, while representations of sensory and motor variables remained stable. The findings were recapitulated by a task-optimized recurrent neural network model, suggesting that neural interactions in PPC embody the world model to consolidate information and track task-relevant hidden states.

neuroscience↗

Flexible neural coding in sensory, parietal, and frontal cortices during goal-directed virtual navigation

We do not understand how neural nodes operate and coordinate within the recurrent action-perception loops that characterize naturalistic self-environment interactions. Here, we record single-unit spiking activity and local field potentials (LFPs) simultaneously from the dorsomedial superior temporal area (MSTd), parietal area 7a, and dorsolateral prefrontal cortex (dlPFC) as monkeys navigate in virtual reality to "catch fireflies." This task requires animals to actively sample from a closed-loop virtual environment while concurrently computing continuous latent variables: (i) the distance and angle travelled (i.e., path integration) and (ii) the distance and angle to a memorized firefly location (i.e., a hidden spatial goal). We observed a patterned mixed selectivity, with the prefrontal cortex most prominently coding for latent variables, parietal cortex coding for sensorimotor variables, and MSTd most often coding for eye-movements. However, even the traditionally considered sensory area (i.e., MSTd) tracked latent variables, demonstrating path integration and vector-coding of hidden spatial goals. Further, global encoding profiles and unit-to-unit coupling (i.e., noise correlations) suggested a functional subnetwork composed by MSTd and dlPFC, and not between these and 7a, as anatomy would suggest. We show that the greater the unit-to-unit coupling between MSTd and dlPFC, the more the animals gaze position was indicative of the ongoing location of the hidden spatial goal. We suggest this MSTd-dlPFC subnetwork reflects the monkeys natural and adaptive task strategy wherein they continuously gaze toward the location of the (invisible) target. Together, these results highlight the distributed nature of neural coding during closed action-perception loops and suggest that fine-grain functional subnetworks may be dynamically established to subserve (embodied) task strategies.

neuroscience↗

Purkinje Cell Activity During Suppression of Voluntary Eye Movements in Rhesus Macaques

Volitional suppression of responses to distracting external stimuli enables us to achieve our goals. This volitional inhibition of a specific behavior is supposed to be mainly mediated by the cerebral cortex. However, recent evidence supports the involvement of the cerebellum in this process. It is currently not known whether different parts of the cerebellar cortex play differential or synergistic roles in planning and execution of this behavior. Here, we measured Purkinje cell (PC) responses in the medial and lateral cerebellum in two rhesus macaques during a pro- and antisaccade task. During an antisaccade trial, non-human primates were instructed to make a saccadic eye movement away from a target, rather than towards it, as in prosaccade trials. Our data shows that the cerebellum plays an important role not only during execution of the saccades, but also during the volitional inhibition of eye movements towards the target. Simple Spike (SS) modulation during the instruction and execution period of pro- and antisaccades was prominent in PCs of both medial and lateral cerebellum. However, only the SS activity in the lateral cerebellar cortex contained information about trial identity and showed a stronger reciprocal interaction with complex spikes. Moreover, SS activity of different PC groups modulated bidirectionally in both regions, but the PCs that showed facilitating and suppressive activity were predominantly associated with instruction and execution, respectively. These findings show that different cerebellar regions and PC groups contribute to goal-directed behavior and volitional inhibition, but with different propensities, highlighting the rich repertoire of cerebellar control in executive functions. Significance StatementThe antisaccade task is commonly used in research and clinical evaluation as a test of volitional and flexible control of behavior. It requires volitional suppression of prosaccades, a function that has been attributed to the neocortex. However, recent findings indicate that cerebellum also contributes to this behavior. We recorded from neurons in the medial and lateral cerebellum to evaluate their responses in this task. We found that both regions significantly modulated their activity during this task, but only cells in the lateral cerebellum encoded the stimulus identity in each trial. These results indicate that the cerebellum actively contributes to the control of flexible behavior and that lateral and medial cerebellum play different roles during volitional eye movements.

neuroscience↗

Spatial representations in macaque hippocampal formation

The hippocampal formation is linked to spatial navigation, but there is little corroboration from freely-moving primates with concurrent monitoring of three-dimensional head and gaze stances. We recorded neurons and local field potentials across hippocampal regions in rhesus macaques during free foraging in an open environment while tracking their head and eye. Theta band activity was intermittently present at movement onset and modulated by saccades. Many cells were phase-locked to theta, with few showing theta phase precession. Most hippocampal neurons encoded a mixture of spatial variables beyond place fields and a negligible number showed prominent grid tuning. Spatial representations were dominated by facing location and allocentric direction, mostly in head, rather than gaze, coordinates. Importantly, eye movements strongly modulated neural activity in all regions. These findings reveal that the macaque hippocampal formation represents three-dimensional space using a multiplexed code, with head orientation and eye movement properties dominating over simple place and grid coding during free exploration.

neuroscience↗

Tracking the mind’s eye: Primate gaze behavior during virtual visuomotor navigation reflects belief dynamics

To take the best actions, we often need to maintain and update beliefs about variables that cannot be directly observed. To understand the principles underlying such belief updates, we need tools to uncover subjects belief dynamics from natural behaviour. We tested whether eye movements could be used to infer subjects beliefs about latent variables using a naturalistic, visuomotor navigation task. We observed eye movements that appeared to continuously track the goal location even when no visible target was present there. Accurate goal-tracking was associated with improved task performance, and inhibiting eye movements in humans impaired navigation precision. By using passive stimulus playback and manipulating stimulus reliability, we show that subjects eye movements are likely voluntary, rather than reflexive. These results suggest that gaze dynamics play a key role in action-selection during challenging visuomotor behaviours, and may possibly serve as a window into the subjects dynamically evolving internal beliefs.

animal behavior and cognition↗

Speed tuning in the macaque posterior parietal cortex

Neurons in the macaque posterior parietal cortex are known to encode the direction of self-motion. But do they also encode ones speed? To test this, we performed neural recordings from area 7a while monkeys were passively translated or rotated at various speeds. Visual stimuli were delivered as optic flow fields and vestibular stimuli were generated by a motion platform. Under both conditions, the responses of a fraction of neurons scaled linearly with self-motion speed, and speed-selective neurons were not localized to specific layers or columns. We analyzed ensembles of simultaneously recorded neurons and found that the precision of speed representation was sufficient to support path integration over modest distances. Our findings describe a multisensory neural code for linear and angular self-motion speed in the posterior parietal cortex of the macaque brain, and suggest a potential role for this representation.

neuroscience↗