Behavioral decomposition reveals rich encoding structure employed across neocortex in rats.

The cortical population code is pervaded by activity patterns evoked by movement, but it remains largely unknown how such signals relate to natural behavior or how they might support processing in sensory cortices where they have been observed. To address this we compared high-density neural recordings across four cortical regions (visual, auditory, somatosensory, motor) in relation to sensory modulation, posture, movement, and ethograms of freely foraging male rats. Momentary actions, such as rearing or turning, were represented ubiquitously and could be decoded from all sampled structures. However, more elementary and continuous features, such as pose and movement, followed region-specific organization, with neurons in visual and auditory cortices preferentially encoding mutually distinct head-orienting features in world-referenced coordinates, and somatosensory and motor cortices principally encoding the trunk and head in egocentric coordinates. The tuning properties of synaptically coupled cells also exhibited connection patterns suggestive of area-specific uses of pose and movement signals, particularly in visual and auditory regions. Together, our results indicate that ongoing behavior is encoded at multiple levels throughout the dorsal cortex, and that low-level features are differentially utilized by different regions to serve locally relevant computations.

Action representation in the mouse parieto-frontal network.

The posterior parietal cortex (PPC) and frontal motor areas comprise a cortical network supporting goal-directed behaviour, with functions including sensorimotor transformations and decision making. In primates, this network links performed and observed actions via mirror neurons, which fire both when individuals perform an action and when they observe the same action performed by a conspecific. Mirror neurons are believed to be important for social learning, but it is not known whether mirror-like neurons occur in similar networks in other social species, such as rodents, or if they can be measured in such models using paradigms where observers passively view a demonstrator. Therefore, we imaged Ca2+ responses in PPC and secondary motor cortex (M2) while mice performed and observed pellet-reaching and wheel-running tasks, and found that cell populations in both areas robustly encoded several naturalistic behaviours. However, neural responses to the same set of observed actions were absent, although we verified that observer mice were attentive to performers and that PPC neurons responded reliably to visual cues. Statistical modelling also indicated that executed actions outperformed observed actions in predicting neural responses. These results raise the possibility that sensorimotor action recognition in rodents could take place outside of the parieto-frontal circuit, and underscore that detecting socially-driven neural coding depends critically on the species and behavioural paradigm used.

Efficient cortical coding of 3D posture in freely behaving rats.

Animals constantly update their body posture to meet behavioral demands, but little is known about the neural signals on which this depends. We therefore tracked freely foraging rats in three dimensions while recording from the posterior parietal cortex (PPC) and the frontal motor cortex (M2), areas critical for movement planning and navigation. Both regions showed strong tuning to posture of the head, neck, and back, but signals for movement were much less dominant. Head and back representations were organized topographically across the PPC and M2, and more neurons represented postures that occurred less often. Simultaneous recordings across areas were sufficiently robust to decode ongoing behavior and showed that spiking in the PPC tended to precede that in M2. Both the PPC and M2 strongly represent posture by using a spatially organized, energetically efficient population code.

Sparsened neuronal activity in an optogenetically activated olfactory glomerulus.

Glomeruli are the functional units of olfactory information processing but little remains known about their individual unit function. This is due to their widespread activation by odor stimuli. We expressed channelrhodopsin-2 in a single olfactory sensory neuron type, and used laser stimulation and simultaneous in vivo calcium imaging to study the responses of a single glomerulus to optogenetic stimulation. Calcium signals in the neuropil of this glomerulus were representative of the sensory input and nearly identical if evoked by intensity-matched odor and laser stimuli. However, significantly fewer glomerular layer interneurons and olfactory bulb output neurons (mitral cells) responded to optogenetic versus odor stimuli, resulting in a small and spatially compact optogenetic glomerular unit response. Temporal features of laser stimuli were represented with high fidelity in the neuropil of the glomerulus and the mitral cells, but not in interneurons. Increases in laser stimulus intensity were encoded by larger signal amplitudes in all compartments of the glomerulus, and by the recruitment of additional interneurons and mitral cells. No spatial expansion of the glomerular unit response was observed in response to stronger input stimuli. Our data are among the first descriptions of input-output transformations in a selectively activated olfactory glomerulus.