A recent model of the hippocampus predicts that the unique properties of the dentate gyrus allow for temporal separation of events. This temporal separation is accomplished in part through the continual generation of new neurons, which, due to a transient window of hyperexcitability, could allow for preferential encoding of information present during their development. Here we obtain in vivo electrophysiological recordings and identify a cell population exhibiting activity that is selective to single contexts when rats experience a long temporal separation between context exposures during training. This selectivity is attenuated as the temporal separation between context exposures is shortened and is further attenuated when neurogenesis is reduced. Our data reveal the existence of a temporal orthogonalizing neuronal code within the dentate gyrus, a hallmark feature of episodic memory.

Cholinergic, GABAergic and glutamatergic projection neurons of the basal forebrain (BF) innervate widespread regions of the neocortex and are thought to modulate learning and attentional processes. Although it is known that neuronal cell types in the BF exhibit oscillatory firing patterns, whether the BF as a whole shows oscillatory field potential activity, and whether such neuronal patterns relate to components of cognitive tasks, has yet to be determined. To this end, local field potentials (LFPs) were recorded from the BF of rats performing an associative learning task wherein neutral objects were paired with differently valued reinforcers (pellets). Over time, rats developed preferences for the different objects based on pellet-value, indicating that the pairings had been well learned. LFPs from all rats revealed robust, short-lived bursts of beta-frequency oscillations (∼25 Hz) around the time of object encounter. Beta-frequency LFP events were found to be learning-dependent, with beta-frequency peak amplitudes significantly greater on the first day of the task when object-reinforcement pairings were novel than on the last day when pairings were well learned. The findings indicate that oscillatory bursting field potential activity occurs in the BF in freely behaving animals. Furthermore, the temporal distribution of these bursts suggests that they are probably relevant to associative learning.

The basal forebrain comprises several heterogeneous neuronal subgroupings having modular projection patterns to discrete sets of cortical subregions. Each cortical region forms recurrent projections, via prefrontal cortex, that reach the specific basal forebrain subgroups from which they receive afferents. This architecture enables the basal forebrain to selectively modulate cortical responsiveness according to current processing demands. Theoretically, optimal functioning of this distributed network would be enhanced by temporal coordination among coactive basal forebrain neurons, or the emergence of "cell assemblies." The present work demonstrates assembly formation in rat basal forebrain neuronal populations during a selective attention task. Neuron pairs exhibited coactivation patterns organized within beta-frequency time windows (55 ms), regardless of their membership within distinct bursting versus nonbursting basal forebrain subpopulations. Thus, the results reveal a specific temporal framework for integration of information within basal forebrain networks and for the modulation of cortical responsiveness.

Basal forebrain transforms multiplexed oscillatory inputs into a phase rate–coded output of task phase during complex behavior.

The hippocampus is an important structure for learning and memory processes, and has strong rhythmic activity. Although a large amount of research has been dedicated toward understanding the rhythmic activity in the hippocampus during exploratory behaviors, specifically in the theta (5–10 Hz) frequency range, few studies have examined the temporal interplay of theta and other frequencies during the presentation of meaningful cues. We obtained in vivo electrophysiological recordings of local field potentials (LFP) in the dentate gyrus (DG) of the hippocampus as rats performed three different associative learning tasks. In each task, cue presentations elicited pronounced decrements in theta amplitude in conjunction with increases in beta (15–30 Hz) amplitude. These changes were often transient but were sustained from the onset of cue encounters until the occurrence of a reward outcome. This oscillatory profile shifted in time to precede cue encounters over the course of the session, and was not present during similar behaviors in the absence of task relevant stimuli. The observed decreases in theta amplitude and increases in beta amplitude in the DG may thus reflect a shift in processing state that occurs when encountering meaningful cues.