Effect of sensory and motivation factors on unit activity in the monkey frontal cortex.
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Biomedical subjects
Publications and source records attributed to A A Orlov.
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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.
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 animal's 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.
The activity of central integrative brain neurons is associated with the overall assessment of functionally diverse signals of different sensory modalities which converge on these neurons via parallel inputs. Processing this information, these neurons take part in organizing the animal's various actions and in the mechanisms involved in switching from one action to another. Therefore, understanding of the functional characteristics of central brain neurons requires studies in which the dynamics of neuron activity are recorded continuously throughout a sequence of actions performed by an animal. Traditional methods of analyzing neuron activity, such as the construction of post- and peristimulus histograms and cross-correlation analysis, are inadequate for this purpose. These methods allow analysis to be applied to neuron spike activity only around each synchronization point Their use for studies of a developed program of animal actions unavoidably leads to a set of separate histograms providing no information on the dynamics of neuron activity corresponding to continuous behavior. A complex approach to studying the neuronal correlates of behavior is suggested, designed to overcome these difficulties. The method is based on the use of a developed behavioral program with recording of several neurons in parallel, with analysis of neuron activity using a relative time scale based on the duration of each sequentially performed action. Non-traditional methods of processing neuron spike activity were developed for analysis of the resulting data, including construction of relative histograms and multidimensional statistics methods. These approaches allowed us to study the dynamics of neuron activity continuously through all the stages of performance of a behavioral program and obtain data on the involvement of each group of those neurons which were studied in functionally different actions. This methodology was tested using studies of the functional characteristics of striatum neurons in monkeys. Comparable data were obtained on the individual responses of neurons and on the dynamics of their activity at different stages of the animals' performance of a multicomponent behavioral program. This revealed the lack of functional specialization in striatum neurons and different patterns of their involvement in motor and cognitive functions.
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.
Putamen neuron spike activity associated with motor and nonmotor functions was studied in monkeys trained to behavioral programs consisting of a series of sequential actions. In general, each putamen neuron was activated during particular behavior fragments. The association of each individual neostriatal neuron with particular behavioral fragments was not constant. When the animal performed a different version of the same program (using different conditioned signals, right- or left-sided tasks, correct or erroneous performance), the neuron could lose its association with the animal's action and become involved in a different action to which it had previously produced no response. Thus, putamen neurons could demonstrate different functional modalities in different versions of the same actions. The use of additional versions of the given program always led to increases in the numbers of behavior fragments during which there were changes in the spike activity of the neurons of interest. This effect was significantly stronger in motor fragments of the program than in nonmotor fragments. These results show that putamen neurons do not have any defined specialization and have different functional modalities when the animal performs different versions of the same action. The nature of putamen neuron involvement in sensory-cognitive processes was more stable than in the organization of motor responses.
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.
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 interactions.
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Each putamen neuron responded to several fragments of a behavioural programme, the pattern of such connections being not constant. The response could disappear in a different variant of the behavioural programme while a response to another fragment could occur. Therefore additional variants of the programme were followed by an increase in number of functional modality of a neuron. This was more obvious in motor fragments of the programme. The data obtained suggest that the putamen neurons have no particular specifics, and so involvement of its units in sensory-cognitive processes seem to be more stable than in organisation of movements.
Significant differences were found in collective unit activity of 6 neostriatum neurons associated with performance of either left- or right-sided task by monkeys: at the moment of decision-making regarding the direction of the movement, and after its completion, irrespective of correctness of the choice. The differences at the moment of the programme completion were significantly greater than at the moment of the decision-making.
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With the use of microelectrode techniques (extracellular recordings) and the method of post-stimulus histograms, the functional characteristics of medulla oblongata neurons of sea catfish Plotosus were investigated under stimulation of electroreceptors by a homogeneous electric field of different duration, intensity, and direction. Two types of the cells possessing, accordingly, tonic or phase activity were registered among 66 neurons investigated. The mode of responses (inhibition or acceleration) of tonic neurons to the direction of the applied electric current is typical for central neurons of fresh-water catfish connected with ampullae's electroreceptors. Neurons showing a substantial response to fields of an intensity less than 1 microV/cm were registered. The reactions were most pronounced with the duration of electric stimuli in the range of 20-200 ms; however, particularly sensitive neurons showed distinct responses to stimuli of duration of 5 and even 2 ms. Thus, for the first time a high sensitivity of ampullae's electroreceptors to high-frequency stimulus was discovered, which allows one to expand the range of studying electric signals used by weakly electric fish for electrolocation and communication.
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