Monkey Prefrontal Single-Unit Activity Reflecting Category-Based Logical Thinking Process and Its Neural Network Model.

Category-based thinking is a fundamental form of logical thinking. Here, we aimed to investigate its neural process at the local circuit level in the prefrontal cortex (PFC). We recorded single-unit PFC activity while male monkeys (Macaca fuscata) performed a task in which the category and rule were prerequisites of logical thinking and the outcome contingency was its consequence. Different groups of neurons coded a single type of information discretely or multiple types in a transitional form. Results of time-by-time analysis of neuronal activity suggest an information flow from category-coding and rule-coding neurons to transitional intermediate neurons, and then to contingency-coding neurons. Category-coding, rule-coding, and contingency-coding neurons showed stable coding of information, whereas intermediate neurons showed dynamic coding, as if it integrated category and rule to derive contingency. A similar process was confirmed by using a spiking neural network model that consisted of subnetworks coding category and rule on the input layer and those coding contingency on the output layer, with a subnetwork for integration in the intermediate layer. These results suggest that category-based logical thinking is realized in the PFC by separated neural populations organized for working in a feedforward manner.SIGNIFICANCE STATEMENT To elucidate the neural process for logical thinking, we combined an in-depth analysis of single-unit activity data with a biologically plausible computational model. Results of time-by-time analysis of prefrontal neuronal activity suggest an information flow from category-coding and rule-coding neurons to transitional intermediate neurons, and then to contingency-coding neurons. Category-coding, rule-coding, and contingency-coding neurons showed stable coding, whereas intermediate neurons showed dynamic coding, as if they integrated category and rule to derive contingency. A spiking neural network model reproduced similar temporal changes of information as the recorded neuronal data. Our results suggest that the prefrontal cortex (PFC) is critically involved in category-based thought process, and this process may be produced by separated neural populations organized for working in a feedforward manner.

Behavioral evidence for the use of functional categories during group reversal task performance in monkeys.

A functional category is a set of stimuli that are regarded as equivalent independently of their physical properties and elicit the same behavioral responses. Major psychological theories suggest the ability to form and utilize functional categories as a basis of higher cognition that markedly increases behavioral flexibility. Vaughan claimed the category use in pigeons on the basis of partition, a mathematical criterion for equivalence, however, there have been some criticisms that the evidence he showed was insufficient. In this study, by using a group reversal task, a procedure originally used by Vaughan, we aimed to gather further evidence to prove the category use in animals. Macaque monkeys, which served as subjects in our study, could efficiently perform the task not only with familiar stimulus sets as Vaughan demonstrated but also with novel sets, and furthermore the task performance was stable even when the number of stimuli in a set was increased, which we consider as further evidence for the category use in animals. In addition, by varying the timing of the reversal, we found that a category formation takes place soon after encountering new stimuli, i.e. in a few blocks of trial after a novel stimulus set was introduced.

Representation of Functional Category in the Monkey Prefrontal Cortex and Its Rule-Dependent Use for Behavioral Selection.

Humans, monkeys, and other animals are considered to have the cognitive ability to use functional categories--that is, stimulus groups based on functional equivalence independent of physical properties. To investigate the underlying neural mechanisms of the use of functional categories, we recorded single-unit activity in the prefrontal cortex of monkeys performing a behavioral task in which the rule-dependent usage of functional category was needed to select an appropriate response. We found a neural correlate of functional categories on the single-neuron level and found that category information is coded independently of other task-relevant information such as rule and contingency information. Analysis of the time course of the information activation suggested that contingency information used for action selection is derived by integrating incoming category information with rule information maintained throughout a session. Such neural computation can be considered as the neural background of flexible behavioral control based on category and rule.

Rule-dependent anticipatory activity in prefrontal neurons.

The flexibility of the behavior of humans and other primates comes from the cognitive capability to use different behavioral modes depending on the contextual information. To investigate the neural mechanism of such a cognitive function, we trained monkeys to participate in a repeated category-outcome reversal. To perform the task efficiently, they had to explore and remember the relevant rule, i.e., which group of stimuli was associated with which outcome, and apply that rule to the visual cue in order to predict an outcome and select a response correctly. We recorded single-unit activity from the prefrontal cortex, including dorsolateral/ventrolateral prefrontal cortex and orbitofrontal cortex, and found that many neurons in these areas showed rule-dependent changes in activity during the trial and during the inter-trial-interval. The time period when a high proportion of neurons started to show rule-dependent activity was the precue period, and the typical activity pattern at that time was sustained and increasing firing towards the onset of the cue ("anticipatory" precue activity). The results indicate that the prefrontal cortex is involved in maintaining rule information in the short-term memory within and between trials and that the rule information is anticipatorily activated towards the onset of the task-relevant cue.