The architectonic subdivisions of the brain are believed to be functional modules, each processing parts of global functions. Previously, we showed that neurons in different regions operate in different firing regimes in monkeys. It is possible that firing regimes reflect differences in underlying information processing, and consequently the firing regimes in homologous regions across animal species might be similar. We analyzed neuronal spike trains recorded from behaving mice, rats, cats, and monkeys. The firing regularity differed systematically, with differences across regions in one species being greater than the differences in similar areas across species. Neuronal firing was consistently most regular in motor areas, nearly random in visual and prefrontal/medial prefrontal cortical areas, and bursting in the hippocampus in all animals examined. This suggests that firing regularity (or irregularity) plays a key role in neural computation in each functional subdivision, depending on the types of information being carried.Key words: firing irregularity/regularity; interspecies similarity; neuronal firing pattern; neuronal firing regime Significance StatementBy analyzing neuronal spike trains recorded from mice, rats, cats, and monkeys, we found that different brain regions have intrinsically different firing regimes that are more similar in homologous areas across species than across areas in one species. Because different regions in the brain are specialized for different functions, the present finding suggests that the different activity regimes of neurons are important for supporting different functions, so that appropriate neuronal codes can be used for different modalities.

Recent studies show that task-related activity in the dorsolateral prefrontal cortex (DLPFC) is modulated by the quality and quantity of the reward, suggesting that the subject's motivational state affects cognitive operations in the DLPFC. The orbito-frontal cortex (OFC) is a possible source of motivational inputs to the DLPFC. However, it is not well known whether these two areas exhibit similar motivational effects on task-related activity. We compared motivational effects on task-related activity in these areas while a monkey performed an oculomotor delayed-response (ODR) task under two reward schedules. In the ODR-1 schedule, reward was given only after the successful completion of four consecutive trials, whereas in the ODR-2 schedule, reward was given after every correct trial. Task-related activities in both areas showed spatial selectivity. The spatial characteristics of task-related activity remained constant in both schedules. Task-related activity in both areas, especially delay-period activity, was also affected by the reward schedule and the magnitude of the activity gradually increased depending on the proximity of the reward trial in the ODR-1 schedule. More task-related OFC activities were affected by reward schedules, whereas more task-related DLPFC activities were affected by spatial factors and reward schedules. These results indicate that the OFC plays a role in monitoring the proximity of the reward trial and detecting reward delivery, whereas the DLPFC plays a role in performing cognitive operations and integrating cognitive and motivational information. These results also indicate that spatial information and the animal's motivational state independently affect neuronal activity in both areas.

Reward-period activity observed in the dorsolateral prefrontal cortex (DLPFC) and the orbitofrontal cortex (OFC) is thought to represent the detection of reward delivery. To investigate whether this activity plays the same role in these areas, we examined this activity under different reward schedules and whether the reward schedule has similar effects on this activity in each of these areas. A monkey performed an oculomotor delayed-response (ODR) task under two reward schedules. In the ODR-1 schedule, the monkey received a large amount of reward only after four successful trials, whereas in the ODR-2 schedule, it received a small amount of reward after every successful trial. Although reward-period activity was observed in both areas, more neurons exhibited this activity in the OFC. Reward-period activity was modulated by the proximity to reward delivery in both areas and this feature was observed more frequently in the OFC. The onset time of this activity also gradually advanced depending on the proximity to reward delivery. Moreover, many OFC neurons with this activity responded to free reward delivery. These results indicate that reward-period activity in the OFC represents the detection of reward delivery and that the gradual change in the magnitude and the onset time of this activity represents the expectation of reward delivery. Similar features of reward-period activity were observed in DLPFC neurons, although a significant number of DLPFC neurons did not respond to free reward delivery and no advance was observed in the onset time of this activity. These results suggest that reward-period activity in the DLPFC participates in whether or not correct performance was achieved. Thus, although similar reward-period activity was observed in both areas, the activity in the OFC represents the detection of reward delivery and is affected by the monkey's motivational state, whereas that in the DLPFC seems to participate in monitoring whether or not the necessary performance is achieved.

The orbitofrontal cortex (OFC) has strong reciprocal connections to the dorsolateral prefrontal cortex (DLPFC), which is known to participate in spatial working memory processes. However, it is not known whether or not the OFC also participates in spatial working memory and whether the OFC and DLPFC contribute equally to this process. To address these issues, we collected single-neuron activity from both areas while a monkey performed an oculomotor delayed-response task, and compared the characteristics of task-related activities between the OFC and DLPFC. All of the task-related activities observed in the DLPFC were also observed in the OFC. However, the proportion and response characteristics of task-related activities were different between the two areas. While most delay-period activity observed in the DLPFC was directionally selective and showed tonic sustained activation, most delay-period activity observed in the OFC was omni-directional and showed gradually increasing activity. Reward-period activity was predominant among task-related activities in the OFC. The proportion of neurons showing reward-period activity was significantly higher in the OFC than in the DLPFC. These results suggest that, although both the OFC and DLPFC participate in spatial working memory processes, the OFC is related more to the expectation and the detection of reward delivery, while the DLPFC is related more to the temporary maintenance of spatial information and its processing.