Physiology of the medial frontal cortex during decision-making in adult and senescent rats

Abstract

Convergent evidence suggests that the dorsal medial prefrontal cortex (dmPFC) makes an important contribution to goal-directed action selection. The dmPFC is also part of a network of brain regions that becomes compromised in old age. It was hypothesized that during decision-making, some process of comparison takes place in the dmPFC between the representation of available actions and associated values, and that this process is changed with aging. These hypotheses were tested in aged and young adult rats performing a novel 3-choice, 2-cue decision task. Neuron and local field potential activity revealed that the dmPFC experienced different states during decision and outcome phases of the task, with increased local inhibition and oscillatory (gamma and theta) activity during cue presentation, and increased excitatory neuron activity (among regular firing neurons) at goal zones. Although excitatory and inhibitory activity appeared anti-correlated over phases of the decision task, cross-correlations and the prominent gamma oscillation revealed that excitation and inhibition were highly correlated on the millisecond scale. This "micro-scale" coupling between excitation and inhibition was altered in aged rats and the observed changes were correlated with changes in decision and movement speeds of the aged animals, suggesting a putative mechanism for age-related behavioral slowing. With respect to decision-making, both aged and young adult rats learned over multiple days to follow the rewarded cue in the 3-choice, 2-cue task. Support for the hypothesis that the dmPFC simultaneously represents alternative actions was not found; however, neuron activity selective for particular goal zones was observed. Interestingly, goal-selective neural activity during the decision period was more likely to take place on error trials, particularly on high-performing sessions and when rats exhibited a preference for a particular feeder. A possible interpretation of these patterns is that goal representations in the dmPFC might have sometimes overruled learned habits, which are likely to be involved in following the correct cue and which are known to be supported by other brain regions. These results describe fundamental properties of network dynamics and neural coding in the dmPFC, and have important implications for the neural basis of processing speed and goal-directed action.