Learning‐dependent dynamics of beta‐frequency oscillations in the basal forebrain of rats

Abstract

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.

Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus

“…In addition to SPW-Rs and slow oscillations, optogenetic stimulation of the MS also suppressed power in the supratheta frequency band. These observations parallel the competing effects between theta and supratheta band activity because termination of theta-associated exploration in the intact animal is regularly coupled with enhanced "beta" power (47). The mechanisms of the suppressive effects of ACh on these oscillations are likely similar in the hippocampus and neocortex (43) and may be mediated, at least partially, by presynaptic M2 cholinergic receptor-mediated blockade of GABA release from basket and other interneurons (48).…”

Beta2 oscillations (23–30 Hz) in the mouse hippocampus during novel object recognition

“…These results suggest a certain specificity of novelty‐related beta2 activity to the hippocampus. Nevertheless, beta2 oscillations were also recently reported in the basal forebrain of rats during an associative learning task (Quinn et al ., ). In this study, beta2 power was higher in the first day of learning in which the object–reward pairs were novel than in subsequent days when pairings became familiar (Quinn et al ., ).…”

Basal forebrain contributes to default mode network regulation

“…Along related lines, BF stimulation also accelerates visual learning and up-regulates cortical visually-evoked potentials (51,52) as well as boosting the reliability of neural signals about sensory information (53)(54)(55). Demonstrations linking BF activity to reward expectation and reward processing further implicate this brain area in goal-directed, externally focused behaviors (56,57). Many of these BF functions are linked to cholinergic projections, which represent one of the major output pathways by which the BF can modulate cortex and other brain structures (32, 58, 59).…”