Learning-associated gamma-band phase-locking of action-outcome selective neurons in orbitofrontal cortex

Gamma oscillations (30-100 Hz) correlate to a variety of neural functions, including sensory processing, attention, and action selection. However, they have barely been studied in relation to emotional processing and valuation of sensory signals and actions. We conducted multineuron and local field potential recordings in the orbitofrontal cortex (OFC) of rats performing a task in which they made go or no-go decisions based on two olfactory stimuli predicting appetitive or aversive outcomes. Gamma power was strongest during the late phase of odor sampling, just before go/no-go movement, and increased with behavioral learning. Learning speed was correlated to the slope of the gamma power increment. Spikes of OFC neurons were consistently timed to the gamma rhythm during odor sampling, regardless of the associated outcome. However, only a specific subgroup of cells showed consistent phase timing. These cells showed action-outcome selective activity, not during stimulus sampling but during subsequent movement responses. During sampling, this subgroup displayed a suppression in firing rate but a concurrent increment in the consistency of spike timing relative to gamma oscillations. In addition to gamma rhythm, OFC field potentials were characterized by theta oscillations during odor sampling. Neurons phase-locked to either theta or gamma rhythms but not to both, suggesting that they become associated with separate rhythmic networks involving OFC. Altogether, these results suggest that OFC gamma-band synchronization reflects inhibitory control over a subpopulation of neurons that express information about the emotional valence of actions after a motor decision, which suggests a novel mechanism for response inhibition

Fast-spiking interneurons of the rat ventral striatum: temporal coordination of activity with principal cells and responsiveness to reward

Although previous in vitro studies revealed inhibitory synaptic connections of fast-spiking interneurons to principal cells in the striatum, uncertainty remains about the nature of the behavioural events that correlate with changes in interneuron activity and about the temporal coordination of interneuron firing with spiking of principal cells under natural conditions. Using in vivo tetrode recordings from the ventral striatum in freely moving rats, fast-spiking neurons were distinguished from putative medium-sized spiny neurons on the basis of their spike waveforms and rates. Cross-correlograms of fast-spiking and putative medium-sized spiny neuron firing patterns revealed a variety of temporal relationships, including peaks of concurrent firing and transient decrements in medium-sized spiny neuron spiking around fast-spiking unit activity. Notably, the onset of these decrements was mostly in advance of the fast-spiking unit firing. Many of these temporal relationships were dependent on the sleep-wake state. Coordinated activity was also found amongst pairs of the same phenotype, both fast-spiking units and putative medium-sized spiny neurons, which was often marked by a broad peak of concurrent firing. When studying fast-spiking neurons in a reward-searching task, they generally showed a pre-reward ramping increment in firing rate but a decrement specifically when the rat received reward. In conclusion, our data indicate that various forms of temporally coordinated activity exist amongst ventral striatal interneurons and principal cells, which cannot be explained by feed-forward inhibitory circuits alone. Furthermore, firing patterns of ventral striatal fast-spiking interneurons do not merely correlate with the general arousal state of the animal but display distinct reward-related changes in firing rate