B. F. Tolkunov

Collective responses of neostriatal (putamen) neurons during alternative behavior in monkeys

A monkey (Macaca nemestrina) was trained to perform a behavioral program consisting of the selection and execution of a defined sequence of actions according to a visual conditioned signal. Discriminant analysis was used to evaluate the parameters of the collective activity of six simultaneously recorded putamen neurons. The collective activity of the neurons showed significant differences associated with execution by the monkey of left- and right-sided tasks. These differences were seen to be quite consistent in different groups of neurons. Despite the fact that putamen neurons were involved in the performance of nine separately analyzed fragments of the program, differences, were seen in two of these: at the moment of taking the decision relating to the direction of movement, and after its completion when a signal indicating the completed result was presented, independently of whether the animal selected the side for the action correctly or incorrectly. In the case of erroneous decisions, the response mosaic differed from that obtained for correct decisions; however, differences due to previously taken decisions regarding the side of action were preserved. These differences were greater at the point of program completion than at the moment of deciding the direction of movement.

Neuron activity in the monkey striatum during parallel performance of actions

Spike activity was recorded from several neurons in the monkey striatum during the performance of a complex behavioral program including differentiation of conditioned signals of different levels of complexity. The most characteristic feature of spike activity in striatal neurons during behavior was found not to be the selective involvement of particular neurons in carrying out certain actions, but a reflection of behavior as a whole in the form of mosaics of neuron activity corresponding to the moments at which particular actions were performed and during the intervals between them.

Correlates of sequential elements of bimanual behavior in the neuronal activity of the neostriatum in monkeys

Neuron spike activity was recorded in the putamen of monkeys trained to perform bimanual operant behavior consisting of nine separate steps. Neuronal reactions were present at all steps: in 52–62% of cases during movement, and in 27–36% of cases during responses to the trigger and conditioned signals and as the monkeys decided which was the working hand. The proportion of inhibitory responses to the trigger stimulus was 9%, while inhibitory reactions accounted for 68% of reactions during hand movement in response to the conditioned signal, 33% of reactions when this same hand was used to collect food reinforcement, and 33% of reactions during simultaneous movement of both hands. Reactions significantly differentiating between right- and left-sided tasks were seen at all stages of working-hand decision-taking and in reactions to the signal indicating the correctness of the selection, but were not seen for reactions to the conditioned signal or for activity accompanying movements of one of the animals hands. These data provide evidence indicating that each step of the complex operant behavior, individual systems of putamen neuronal reactions were created with qualitatively different integral sensitivity to instantaneous behavior.

Model of the function of the neostriatum and its neuronal activity during behavior in monkeys

Experiments with simultaneous recording of six neostriatum neurons showed that the neurons of this structure are involved in the organization of all stages of behavior. A defined combination of neuronal activity corresponded to each action of the animal. The responses of individual neostriatal neurons were not entirely determined by the action being carried out at a particular moment, but reflected a wider aspect of the overall activity of the animal. These data, along with the established properties of neuronal responses in the neural network model, indicate that the integration of afferent signals in the neostriatum and their distribution to efferent connections is based on network mechanisms of neuronal interaction

Neuron Activity in the Monkey Striatum of Identifies Integration Sequential Actions into Functional Blocks

Spike activity in monkey striatum (putamen) neurons was recorded during the performance of a complex multistep operant task. Tonic responses propagating beyond a single action were recorded, along with phasic responses seen within a given action. The tonic type of response was recorded in 132 of 148 cells. Only 11 of these neurons showed exclusively this type of activity. The beginnings and ends of tonic responses were generally associated with key moments in the behavior, corresponding to the triggering and completion of immediate aims during the performance of the behavioral program as a whole. These results provide evidence that the role of the striatum is not limited to controlling single sequentially performed actions, but spreads to the whole structure of a behavioral act.

Dynamics of Neuron Activity Levels in the Monkey Striatum Associated with Performance of a Multistage Behavioral Program

The levels of activity of monkey putamen neurons were studied during multistage behavior. Two groups of neuron activity patterns were identified. One was a pattern of low activity, less than twice the background level; the other was a pattern of high activity, exceeding the background by a greater factor. Neither type of pattern was linked with defined neurons, but both were associated with particular stages in the behavior. Low-activity patterns were recorded primarily at stages associated with the warning signal and receipt of the food reward at the stages completing the task. High-activity patterns were associated with the animal performing actions in response to the conditioned stimulus and with the decision-taking stage, when performance of the actions involved selection of the right or left hand. In addition, the number of these patterns increased significantly in relation to signals indicating correct performance of the task. Key moments in the behavior were found to be associated with increases in the numbers of high-activity patterns and simultaneous decreases in the number of low-activity patterns.

The differentiating activity of monkey putamen neurons during performance of alternative spatial selection.

Spike activity was recorded from three zones of the putamen in monkeys trained to bimanual operant activity during performance of an alternative spatial selection task. Neuron responses were analyzed using the following criteria: a) differentiation of the side providing reinforcement (differentiating/non-differentiating responses); b) response duration (tonic/phasic); c) response laterality (contralateral/ipsilateral hemispheres); d) baseline activity frequency. The differentiating activity of cells was found to show the closest correlation with behavioral aspects of the program, particularly the tonic part and, even more so, contralateral tonic responses. It is suggested that differentiating activity, as opposed to non-differentiating activity, is less a reflection of the morphological and neurochemical characteristics of the neural elements of the putamen than of their functional homogeneity in relation to external determinants of behavior.

Sequential Rearrangements of the Ensemble Activity of Putamen Neurons in the Monkey Brain as a Correlate of Continuous Behavior

Simultaneous recordings were made of the spike activity of groups of 6–7 neurons in the putamen in two monkeys (Macaca nemestrina and Macaca mulatta) during performance of alternative spatial selection. Discriminant analysis was used to evaluate the magnitude of rearrangements in spike activity in groups of neurons during transitions from each step of the behavioral program to the next, along with the degree of differences in reactivity mosaics formed at each step in different versions of task execution. Rearrangements in spike activity were noted at all steps of the program. The dynamics of rearrangements on selection of the right and left feeders were different, leading to the appearance of significant differences in the reactivity mosaics at the decision-taking and reinforcement-receiving steps. The rearrangements preceding voluntary movement of one hand were more marked in the contralateral hemisphere. During performance of movements, the volume of rearrangements could increase, though differences in rearrangements accompanying movements of the right and left hands decreased. On receipt of reinforcement, rearrangements were greater when the animals selected a specified feeder (the left feeder) independently of which hemisphere was recorded.

Behavior-reactive neuron populations in the monkey neostriatum.

Comparative analysis of neuron activity in the monkey putamen during multistep behavior showed that putamen neurons are active during all the animals behavioral actions. The difference between the number of active neurons at a given step of the behavior as compared with the preceding step was found to be significantly smaller than the number of neurons reorganizing their activity at this step. Reorganization of neuron activity in the putamen is regarded as a reflection of the efferent code controlling the behavior, while the extent of reorganization is regarded as a measure of the change in this code in association with the organization of a sequential behavioral action. Changes in the numbers of active neurons at different stage of behavior and reorganization of their activity occurred independently of each other. This may be associated with the two afferent systems of the striatum: that ascending from the brainstem and the corticofugal, which carries differential information to the neural network of the striatum from various parts of the cortex.

Reflection of internal and external determinants of behavior in the neuronal activity of the neostriatum of monkeys

It has been demonstrated that some neurons of the neostriatum of monkeys (Macaca nemestrina) participate in supporting the reaction of the animal to the appearance of standard situations in which a decision is made on the basis of already existing skills. Other neurons (primarily non-baseline active), by contrast, are activated in nonstandard situations, when the use of existing skills is ineffective. It is hypothesized that their activity is associated with the shift of the animal to a different activity which consists in the rejection of the use of existing skills for the formation of new skills.