Intermingled Ensembles in Visual Association Cortex Encode Stimulus Identity or Predicted Outcome.

The response of a cortical neuron to a motivationally salient visual stimulus can reflect a prediction of the associated outcome, a sensitivity to low-level stimulus features, or a mix of both. To distinguish between these alternatives, we monitored responses to visual stimuli in the same lateral visual association cortex neurons across weeks, both prior to and after reassignment of the outcome associated with each stimulus. We observed correlated ensembles of neurons with visual responses that either tracked the same predicted outcome, the same stimulus orientation, or that emerged only following new learning. Visual responses of outcome-tracking neurons encoded "value," as they demonstrated a response bias to salient, food-predicting cues and sensitivity to reward history and hunger state. Strikingly, these attributes were not evident in neurons that tracked stimulus orientation. Our findings suggest a division of labor between intermingled ensembles in visual association cortex that encode predicted value or stimulus identity.

Cortical Specializations Underlying Fast Computations.

The time course of behaviorally relevant environmental events sets temporal constraints on neuronal processing. How does the mammalian brain make use of the increasingly complex networks of the neocortex, while making decisions and executing behavioral reactions within a reasonable time? The key parameter determining the speed of computations in neuronal networks is a time interval that neuronal ensembles need to process changes at their input and communicate results of this processing to downstream neurons. Theoretical analysis identified basic requirements for fast processing: use of neuronal populations for encoding, background activity, and fast onset dynamics of action potentials in neurons. Experimental evidence shows that populations of neocortical neurons fulfil these requirements. Indeed, they can change firing rate in response to input perturbations very quickly, within 1 to 3 ms, and encode high-frequency components of the input by phase-locking their spiking to frequencies up to 300 to 1000 Hz. This implies that time unit of computations by cortical ensembles is only few, 1 to 3 ms, which is considerably faster than the membrane time constant of individual neurons. The ability of cortical neuronal ensembles to communicate on a millisecond time scale allows for complex, multiple-step processing and precise coordination of neuronal activity in parallel processing streams, while keeping the speed of behavioral reactions within environmentally set temporal constraints.