Reorganization of Composition of Striatal Neurons Correlating with Behavior in the Monkey Macaca nemestrina

The available experimental data do not provide a sufficiently complete picture of the neuronal activity connected with some action of the animal, as they have been obtained under different experimental protocols and as a result of study of different cells. The present work was aimed at studying activity of the same neuron group at different moments of animal's behavior. A monkey (Macaca nemestrina) was taught to perform a behavioral program consisting of several functional heterogeneous actions. The impulsive activity of striatal neurons was recorded in the central region of putamen with coordinates A 16.5, L7, and H 8–10 [18]. The activity of each neuron was recorded during 13 consecutive stages of the same behavioral task. As a whole, in 59 putamen neurons, 767 fragments of neuronal activity were studied. It was shown that the same neurons could be involved at different behavioral stages when the animal performed different actions. At individual stages, the number of neurons common with other behavioral stages reached 70–80% of all reactive cells at the stage. The number of the neurons common within the rest of 12 stages was determined for every program stage. The number of such common neurons established in the experiment was in 142 out of 156 cases higher than their number that could be expected on the basis of statistical relations. The data obtained indicate that the reorganization in composition of behavior-reactive cells at every behavioral stage occurs mainly by using the same neurons but not only the neurons that are specialized for the given action. The polymodality of individual striatal neurons is unlikely to be connected with that they have several functions, but results from that the same neuron can be a constituent of neuronal mosaics of different configurations corresponding to different behavioral moments.     

The dynamics of neuron activity level in the striatum of the monkey brain in relation to the realization of multistage behavior

Level of the unit activity was studied in the monkey putamen during multistage behavior. Two groups of neuron activity patterns were distinguished. The first one involved patterns of low level neuron activity less exceeding the background level than the second one; the other group involved patterns of high level neuron activity exceeding the background level in the second time. These kinds of patterns were behavior-related. Patterns with low level neuron activity were recorded preferentially in relation to the trigger stimuli and reward. Patterns of high level neuron activity were recorded in relation to the decision-making, movements of arms in the left and right directions. Besides, their number rose in relation to the auditory cue reported to right realization of the task. It was established that the number of patterns of high level neuron activity rose in key moments of behavior, while the number of the patterns of low level neuron activity decreased.     

Population-Vector Analysis by Primate Prefrontal Neuron Activities

The population-vector analysis was applied to visualize neuronal processes of sensory-to-motor transformation in the prefrontal cortex while two monkeys performed two types of oculomotor delayed-response (ODR) tasks. In a standard ODR task, monkeys were required to make a quick eye movement to where thevisual cue had been presented 3 s before, whereas in R-ODR task, monkeys wererequired to make an eye movement 90^°clockwise to the direction that the visual cue had been presented. In both tasks, directions of population vectors calculated from cue- and response-period activity were almost the same as cue directions and saccade directions, respectively, indicating that population vectors of cue- and response-period activity represent information of visual inputs and motor outputs, respectively. To visualize neuronal processes of information transformation, population vectors were calculated every 250 ms during a whole trial. In ODR task, population vectors weredirected the same direction as the cue direction during the delay period. However, in R-ODR task, population vector rotated gradually from the direction similar to the cue direction to the saccade direction during the delay period. These results indicate that visual-to-motor transformation occurs during the delay period and that this process can be visualized by the population-vectoranalysis.     

Populations of behavior-reactive neurons in the monkey neostriatum

Comparative analysis of the unit activity of the monkey putamen during multistage behavior showed that neurons of the putamen are active during all the behavioral actions. It was established that the number of the behavior-related neurons changes considerably less than number of neurons which reorganize their activity at the time. Reorganization of unit activity in the putamen is considered as reflecting the efferent code which controls behavior, and the degree of reorganization--as a measure of change of this code in relation to organization of ongoing behavioral action. It has been discovered that the change in the number of the active neurons at various steps of behavior and reorganization of their activity occurs independently. It may be related to two main afferent systems of striatum: ascending from rhe brain stem, and corticofugal which brings differentiated information to the neuronal net of striatum from various parts of the cortex.     

Spike synchronization and firing rate in a population of motor cortical neurons in relation to movement direction and reaction time

 We studied the dynamics of precise spike synchronization and rate modulation in a population of neurons recorded in monkey motor cortex during performance of a delayed multidirectional pointing task and determined their relation to behavior. We showed that at the population level neurons coherently synchronized their activity at various moments during the trial in relation to relevant task events. The comparison of the time course of the modulation of synchronous activity with that of the firing rate of the same neurons revealed a considerable difference. Indeed, when synchronous activity was highest, at the end of the preparatory period, firing rate was low, and, conversely, when the firing rate was highest, at movement onset, synchronous activity was almost absent. There was a clear tendency for synchrony to precede firing rate, suggesting that the coherent activation of cell assemblies may trigger the increase in firing rate in large groups of neurons, although it appeared that there was no simple parallel shifting in time of these two activity measures. Interestingly, there was a systematic relationship between the amount of significant synchronous activity within the population of neurons and movement direction at the end of the preparatory period. Furthermore, about 400 ms later, at movement onset, the mean firing rate of the same population was also significantly tuned to movement direction, having roughly the same preferred direction as synchronous activity. Finally, reaction time measurements revealed a directional preference of the monkey with, once again, the same preferred direction as synchronous activity and firing rate. These results lead us to speculate that synchronous activity and firing rate are cooperative neuronal processes and that the directional matching of our three measures – firing rate, synchronicity, and reaction times – might be an effect of behaviorally induced network cooperativity acquired during learning. Received: 16 January 2002 / Accepted in revised form: 26 November 2002 / Published online: 7 April 2003 RID="*" ID="*" Present address: Istituto di Fisiologia Umana, Università di Parma, Via Volturno 39, 43100 Parma, Italy Correspondence to: A. Riehle (e-mail: ariehle@lnf.cnrs-mrs.fr, Tel.: +33-491-164329, Fax: +33-491-774969) Acknowledgements. We wish to thank Sonja Grün, Markus Diesmann, and Bill MacKay for many helpful and exciting discussions and one anonymous referee for her/his helpful comments. Special thanks go to Annette Bastian for her help in data collection, Michèle Coulmance for writing data acquisition and parts of data analysis software, and Marc Martin for animal welfare. This research was supported in part by the CNRS, GIS (Sciences de la Cognition), and ACI Cognitique (Invariants and Variability). FG was supported by the French government (MENRT).     

Studies on activity pattern of the patellid limpet Cellana toreuma (Reeve)

The habits and activity of Cellana toreuma (Reeve) have been studied in a field population. Activity is very high at ebb and flood tide, independent of the time of day, and sharply decreases during complete submergence or complete exposure. Duration of movement fluctuates with tidal amplitude; when neap tide, movement does not stop during low tide owing to continuous awash conditions. Vertical movement entirely coincides with tidal direction at day and night. In this way, the movement does not depend on light but chiefly the tide. Compared with a nocturnal limpet, C. nigrolineata (Reeve), the divergence in the behavioural patterns may be a function of the extent to which limpets are influenced by light. Duration of movement and distance increase with limpet size. Homing behaviour was not observed.     

Temporal Production Signals in Parietal Cortex

We often perform movements and actions on the basis of internal motivations and without any explicit instructions or cues. One common example of such behaviors is our ability to initiate movements solely on the basis of an internally generated sense of the passage of time. In order to isolate the neuronal signals responsible for such timed behaviors, we devised a task that requires nonhuman primates to move their eyes consistently at regular time intervals in the absence of any external stimulus events and without an immediate expectation of reward. Despite the lack of sensory information, we found that animals were remarkably precise and consistent in timed behaviors, with standard deviations on the order of 100 ms. To examine the potential neural basis of this precision, we recorded from single neurons in the lateral intraparietal area (LIP), which has been implicated in the planning and execution of eye movements. In contrast to previous studies that observed a build-up of activity associated with the passage of time, we found that LIP activity decreased at a constant rate between timed movements. Moreover, the magnitude of activity was predictive of the timing of the impending movement. Interestingly, this relationship depended on eye movement direction: activity was negatively correlated with timing when the upcoming saccade was toward the neuron''s response field and positively correlated when the upcoming saccade was directed away from the response field. This suggests that LIP activity encodes timed movements in a push-pull manner by signaling for both saccade initiation towards one target and prolonged fixation for the other target. Thus timed movements in this task appear to reflect the competition between local populations of task relevant neurons rather than a global timing signal.     

Activity in the lateral prefrontal cortex reflects multiple steps of future events in action plans

To achieve a behavioral goal in a complex environment, we must plan multiple steps of motor behavior. On planning a series of actions, we anticipate future events that will occur as a result of each action and mentally organize the temporal sequence of events. To investigate the involvement of the lateral prefrontal cortex (PFC) in such multistep planning, we examined neuronal activity in the PFC of monkeys performing a maze task that required the planning of stepwise cursor movements to reach a goal. During the preparatory period, PFC neurons reflected each of all forthcoming cursor movements, rather than arm movements. In contrast, in the primary motor cortex, most neuronal activity reflected arm movements but little of cursor movements during the preparatory period, as well as during movement execution. Our data suggest that the PFC is involved primarily in planning multiple future events that occur as a consequence of behavioral actions.     

Differentiating activity of monkey putamen neurons during performance of the alternative spatial choice

Single unit activity was recorded in monkeys in three putamen zones learned a bimanual operant activity during performance of the task of alternative spatial choice. The neuronal reactions were specially analyzed by the criteria as follows: a) differentiation of the side of reward (differentiating--non-differentiating reactions); b) character of reaction by duration (tonic-phasic); c) laterality (contra- and ipsilateral reactions as related to hemisphere); d) frequency of background activity. It was shown that differentiating cell activity, especially their tonic part and in still greater degree contra-lateral tonic reactions most closely correlate with behavioral aspects of the program. The assumption that differentiating activity, unlike non-differentiating one, is the reflection of not only morphological and neurochemical characteristic features of nervous elements of putamen but of its functional uniformity in relation to external determinants of behavior, was put forward.     

Set-related neuronal activity in the premotor cortex of rhesus monkeys: effects of changes in motor set

Previous studies have suggested that the premotor cortex plays a role in motor preparation. We have tested this hypothesis in macaque monkeys by examining neuronal activity during an enforced, 1.5-3.0 s delay period between the presentation of an instruction for movement and the onset of that movement. Two targets for movement were available to the monkey, one on the left and one on the right. Illumination of one of the targets served as the instruction for a forelimb movement. It is known that there are cells in the premotor cortex that have directionally specific, sustained activity increases or decreases following such instructions. If the premotor cortex is involved in the preparation for movement in a particular direction, then changing the target from one to the opposite side during the delay period should lead to a pronounced change in sustained neuronal activity. Further, removing the instruction, while still requiring movement to the target, should have little or no sustained effect. Seventy cells showed the predicted activity patterns, thus supporting the view that the premotor cortex plays a role in motor preparation.     

Convergence of Signals and Reorganization of Neuronal Activity in a Model of Neuronal Network and in Striatum of the Monkey Brain

To elucidate principles of neuronal organization providing preservation of informational content of converging impulse flows in afferent impulsation of neurons, a comparison is performed of results obtained in the previously carried out experiments on a model of neuronal network and in a study of correlates of behavior in the neuronal network of the monkey brain neostriatum (putamen). This comparison has shown that responses of the neuronal network model to different ratio of input impulse flows and changes of the neostriatal neuronal activity, which accompany different behavioral actions, are seen the most clearly in reorganization of composition of the most active neurons. Each combination of input signals and each behavioral action of the animal correspond to a non-repeated mosaic of neuronal activity. The data obtained indicate that the neuronal network, both real and in the simplest model variant, is able to transform the converging input signals into the mosaic equivalent to their entire combination and thereby to transmit the result of generalization of the input signals of the network to the innervated brain structures.     

Driving oscillatory activity in the human cortex enhances motor performance

Voluntary movement is accompanied by changes in the degree to which neurons in the brain synchronize their activity within discrete frequency ranges. Two patterns of movement-related oscillatory activity stand out in human cortical motor areas. Activity in the beta frequency (15-30 Hz) band is prominent during tonic contractions but is attenuated prior to and during voluntary movement. Without such attenuation, movement may be slowed, leading to the suggestion that beta activity promotes postural and tonic contraction, possibly at a cost to the generation of new movements. In contrast, activity in the gamma (60-90 Hz) band increases during movement. The direction of change suggests that gamma activity might facilitate motor processing. In correspondence with this, increased frontal gamma activity is related with reduced reaction times. Yet the possibility remains that these functional correlations reflect an epiphenomenal rather than causal relationship. Here we provide strong evidence that oscillatory activities at the cortical level are mechanistically involved in determining motor behavior and can even improve performance. By driving cortical oscillations using noninvasive electrical stimulation, we show opposing effects at beta and gamma frequencies and interactions with motor task that reveal the potential quantitative importance of oscillations in motor behavior.     

Sequential rearrangements of ensemble activity of the putamen neurons of monkeys as a correlate to continuous behavior

Simultaneous recording of unit activity of 6-8 putamen neurons in two monkeys (M. nemestrina and M. mulatta) during performance of the task of alternative spatial choice, was carried out. The extent of rearrangements of the activity in the groups of neurons with the transition from every step of the behavioral program to the next one and the degree of difference in mosaics of reactivity, forming at every step with a different variants of performance, were evaluated using discriminative analysis. The rearrangements of the impulse activity were recorded in all steps of the program. The dynamics of rearrangements with the choice of right or left feeder was different, which resulted in appearance of significant differences in mosaics of reactivity at the stage of decision making and receiving reward. The rearrangements preceding the task-oriented movement of one hand were more pronounced in the contralateral hemisphere. The volume of rearrangements may increase with the performance of movement but the differences of mosaics formed during the movement of right and left hand are decreasing. At the stage of reception of the reward, the rearrangements were greater in case the animal chose the certain (left) feeder irrespective of the side of recording the unit activity.     

Effects of applying microelectrostimulation to different cell type zones in the caudate nucleus

The effects of applying electromicrostimulation to areas of the caudate nucleus with different neuronal activity patterns were investigated during chronic experiments on four cats. Caudate sites containing neurons responding to presentation of various sensory stimuli were selected for the first set of experiments and those where no neuronal activity manifested in the second series. Histological verification of electrolytic marker sites produced by electrical stimulation took place at the end of each experimental sequence and the cell types surrounding these lesions were examined. Microelectrostimulation consistently produced movement in the animal in the first set of experiments; markers were located along the surface of striosomes among large-sized cells, bundles of fibers, and blood vessels. In the second, electrical stimulation produced no alteration in naturally occurring animal behavior; markers were located within striosomes in accumulations of small- and medium-sized cells. A survey of the findings obtained would confirm our hypothesis that the neurons from which activity had been recorded by extracellular techniques in the caudate nucleus are large-sized cells with long axons.Institute for Research into Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 22, No. 2, pp. 162–171, March–April, 1990.     

The effect of foot orthotics on myoelectric fatigue in the vastus lateralis during a simulated skier’s squat

Fatigue in the legs is a problem experienced by skiers. It has been suggested that optimal orthotics may reduce muscle fatigue for a given movement task by minimising muscle activity (Med. Sci. Sports Exerc. 31 (1999) S421). The aims were to determine whether EMG would provide an independent method of analysing myoelectric fatigue in the vastus lateralis (VL) during a skier’s squat and whether orthotics could affect this fatigue response. Six skiers performed skier’s squats for as long as possible with no orthotic, low volume orthotics and high volume orthotics in their ski boots. Bipolar, active surface electrodes recorded EMG activity in the VL throughout each squat. Results for the EMG median frequency showed a significant shift in the power density spectrum towards the lower frequencies (P<0.05) at the end of the contraction, suggesting that myoelectric fatigue was occurring and was measurable using EMG. All conditions displayed a significant decrease in median frequency at the end of the contraction (P=0.001). The high volume orthotic showed a significant reduction in myoelectric fatigue, however, there was no difference in the duration of squats across the three conditions (P>0.05). Subjective and objective findings support the use of the high volume foot orthotic for skiers.     

Complex Population Response of Dorsal Putamen Neurons Predicts the Ability to Learn

Day-to-day variability in performance is a common experience. We investigated its neural correlate by studying learning behavior of monkeys in a two-alternative forced choice task, the two-armed bandit task. We found substantial session-to-session variability in the monkeys’ learning behavior. Recording the activity of single dorsal putamen neurons we uncovered a dual function of this structure. It has been previously shown that a population of neurons in the DLP exhibits firing activity sensitive to the reward value of chosen actions. Here, we identify putative medium spiny neurons in the dorsal putamen that are cue-selective and whose activity builds up with learning. Remarkably we show that session-to-session changes in the size of this population and in the intensity with which this population encodes cue-selectivity is correlated with session-to-session changes in the ability to learn the task. Moreover, at the population level, dorsal putamen activity in the very beginning of the session is correlated with the performance at the end of the session, thus predicting whether the monkey will have a "good" or "bad" learning day. These results provide important insights on the neural basis of inter-temporal performance variability.     

The analytical characteristics of the dynamics of interneuronal functional connections during conditioned-reflex activity]

The dynamics of functional relations between neurons was studied in the frontal cortex of dogs performing reversal conditioning task. To reveal the functionally relevant relationships between the temporal patterns of correlated firing and behavioral events, we developed an original processing technique. The technique included the following procedures: a) isolation of the "coupled spikes" (CS) from simultaneously recorded impulse trains: b) search for the temporal patterns of correlated firings and their classification by clustering single trials with similar temporal distribution of CS; c) assessment of behavioral significance of the identified patterns by evaluation of the probabilities of coincidence of behavioral events and different CS patterns. Significant correlations between impulse trains were revealed in 38 neuronal pairs of 456 analyzed. The effects of change in behavioral context on the CS dynamics during the task performance were found in 87% of neuronal pairs with correlated activity. In 17 pairs the behavioral conditions were identified, under which potentially connected neurons fired independently during all the periods of the behavioral task. The potentialities of the advanced processing technique are discussed. We suggest that this analysis can provide useful information about the temporal distribution of correlated firings under conditions of nonstereotyped behavior, when an animal reacts in the dynamically organized experimental context.     

Coemergence of regularity and complexity during neural network development

With the growing recognition that rhythmic and oscillatory patterns are widespread in the brain and play important roles in all aspects of the function of our nervous system, there has been a resurgence of interest in neuronal synchronized bursting activity. Here, we were interested in understanding the development of synchronized bursts as information-bearing neuronal activity patterns. For that, we have monitored the morphological organization and spontaneous activity of neuronal networks cultured on multielectrode-arrays during their self-executed evolvement from a mixture of dissociated cells into an active network. Complex collective network electrical activity evolved from sporadic firing patterns of the single neurons. On the system (network) level, the activity was marked by bursting events with interneuronal synchronization and nonarbitrary temporal ordering. We quantified these individual-to-collective activity transitions using newly-developed system level quantitative measures of time series regularity and complexity. We found that individual neuronal activity before synchronization was characterized by high regularity and low complexity. During neuronal wiring, there was a transient period of reorganization marked by low regularity, which then leads to coemergence of elevated regularity and functional (nonstochastic) complexity. We further investigated the morphology-activity interplay by modeling artificial neuronal networks with different topological organizations and connectivity schemes. The simulations support our experimental results by showing increased levels of complexity of neuronal activity patterns when neurons are wired up and organized in clusters (similar to mature real networks), as well as network-level activity regulation once collective activity forms.     

The kinematics of the scapulae and spine during a lifting task

Simultaneous motion of the scapula and humerus is widely accepted as a feature of normal upper limb movement, however this has usually been investigated under conditions in which purposeful, functional tasks were not considered. The aim of this study was to investigate the synchrony and coordination of the constituent 3D movements of the shoulder girdle and trunk, during a functional activity. 45 healthy women, aged between 20 and 80 years, performed a simple lifting task, moving a loaded box from a shelf at waist level to one at shoulder level and then reversed the movement, during which the linear and angular motions of the scapulae, upper and lower thoracic spine and upper limbs were monitored and analysed using cross-correlation techniques. Results indicated a close and consistent set of coordinated movement patterns, which suggest biomechanical invariance in the responses of the structures adjacent to the upper limb during such a lifting task. These scapulohumeral relationships were, however, more constant and phase-locked when there was a specific purpose to the movement than during periods in which the arm was lowered without load. There were no age-related differences in any movement responses.