The adaptive value of probability distortion and risk-seeking in macaques' decision-making

International audienceIn humans, the attitude toward risk is not neutral and is dissimilar between bets involving gains and bets involving losses. The existence and prevalence of these decision features in non-human primates are unclear. In addition, only a few studies have tried to simulate the evolution of agents based on their attitude toward risk. Therefore, we still ignore to which extent Prospect theory’s claims are evolutionary rooted. To shed light on this issue, we collected data in 9 macaques that performed bets involving gains or losses. We confirmed that their overall behaviour is coherent with Prospect theory’s claims. In parallel, we used a genetic algorithm to simulate the evolution of a population of agents across several generations. We showed that the algorithm selects progressively agents that exhibit risk-seeking and an inverted S-shape distorted perception of probability. We compared these two results and found that monkeys' attitude toward risk when facing losses only is congruent with the simulation. This result is consistent with the idea that gambling in the loss domain is analogous to deciding in a context of life-threatening challenges where a certain level of risk-seeking behaviours and probability distortions may be adaptive

Rôle du striatum sensorimoteur dans le contrôle des séquences motrices automatisées chez le primate

Le striatum, tout particulièrement sa région sensorimotrice, est connu pour jouer un rôle crucial dans l’expression de routines motrices qui nécessitent la réalisation d’une suite de mouvements. Dans ce travail, nous avons étudié la contribution respective des neurones efférents et des interneurones cholinergiques du striatum dans les processus qui sous - tendent l’expression de séquences motrices automatisées, en enregistrant l’activité unitaire de ces deux populations neuronales chez des singes entraînés à effectuer des mouvements d’atteinte manuelle de cibles. Par cette approche, nous avons examiné les modifications d’activité de ces neurones lors d’un changement des conditions de performance durant la réalisation de la séquence de mouvements. Ainsi en manipulant l’ordre habituel ou la structure temporelle de la séquence, nous avons montré, au sein du striatum sensorimoteur, que les neurones efférents et les interneurones cholinergiques participent au traitement des informations spatiales et temporelles qui caractérisent une séquence motrice automatisée. Par ailleurs, nous avons montré que ces deux populations neuronales sont différentiellement activées lorsque l’ordre de la séquence est visuellement spécifié ou déterminé sur la base d’informations mémorisées. Ces résultats apportent des informations essentielles pour mieux comprendre les mécanismes neuronaux impliqués, au niveau du striatum sensorimoteur, dans le contrôle des séquences motrices automatisées.It is well known that the striatum, especially its sensorimotor part, is involved in the expression of motor skills which require the production of a sequence of movements. In this study, we addressed the respective contribution of efferent neurons and cholinergic interneurons of the striatum in the processes underlying the expression of motor sequences, by recording single unit activity of these two neuronal populations in monkeys performing sequential arm reaching movements. By this experimental approach, we examined activity modulations of these neurons during a change in the conditions of performance of the motor sequence. Thus, by changing the habitual order or the temporal structure of the sequence, we underlined that within sensorimotor striatum, efferent neurons and cholinergic interneurons are involved in the processing of spatial and temporal information which characterize an automatic motor sequence. In addition, we reported differential activations of these two neuronal populations depending on whether the serial order of the sequence of movements is visually cued or based on internally stored information. Taken together, these results provide essential information in order to better understand the neuronal mechanisms involved, within the sensorimotor part of striatum, in the control of the automatic motor sequences

Rôle du striatum sensorimoteur dans le contrôle des séquences motrices automatisées chez le primate

Le striatum, tout particulièrement sa région sensorimotrice, est connu pour jouer un rôle crucial dans l expression de routines motrices qui nécessitent la réalisation d une suite de mouvements. Dans ce travail, nous avons étudié la contribution respective des neurones efférents et des interneurones cholinergiques du striatum dans les processus qui sous - tendent l expression de séquences motrices automatisées, en enregistrant l activité unitaire de ces deux populations neuronales chez des singes entraînés à effectuer des mouvements d atteinte manuelle de cibles. Par cette approche, nous avons examiné les modifications d activité de ces neurones lors d un changement des conditions de performance durant la réalisation de la séquence de mouvements. Ainsi en manipulant l ordre habituel ou la structure temporelle de la séquence, nous avons montré, au sein du striatum sensorimoteur, que les neurones efférents et les interneurones cholinergiques participent au traitement des informations spatiales et temporelles qui caractérisent une séquence motrice automatisée. Par ailleurs, nous avons montré que ces deux populations neuronales sont différentiellement activées lorsque l ordre de la séquence est visuellement spécifié ou déterminé sur la base d informations mémorisées. Ces résultats apportent des informations essentielles pour mieux comprendre les mécanismes neuronaux impliqués, au niveau du striatum sensorimoteur, dans le contrôle des séquences motrices automatisées.It is well known that the striatum, especially its sensorimotor part, is involved in the expression of motor skills which require the production of a sequence of movements. In this study, we addressed the respective contribution of efferent neurons and cholinergic interneurons of the striatum in the processes underlying the expression of motor sequences, by recording single unit activity of these two neuronal populations in monkeys performing sequential arm reaching movements. By this experimental approach, we examined activity modulations of these neurons during a change in the conditions of performance of the motor sequence. Thus, by changing the habitual order or the temporal structure of the sequence, we underlined that within sensorimotor striatum, efferent neurons and cholinergic interneurons are involved in the processing of spatial and temporal information which characterize an automatic motor sequence. In addition, we reported differential activations of these two neuronal populations depending on whether the serial order of the sequence of movements is visually cued or based on internally stored information. Taken together, these results provide essential information in order to better understand the neuronal mechanisms involved, within the sensorimotor part of striatum, in the control of the automatic motor sequences.AIX-MARSEILLE1-Bib.electronique (130559902) / SudocSudocFranceF

Modulation of Neuronal Activity in the Monkey Putamen Associated With Changes in the Habitual Order of Sequential Movements

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Importance of the temporal structure of movement sequences on the ability of monkeys to use serial order information

International audienceThe capacity to acquire motor skills through repeated practice of a sequence of movements underlies many everyday activities. Extensive research in humans has dealt with the importance of spatial and temporal factors on motor sequence learning, standing in contrast to the few studies available in animals, particularly in nonhuman primates. In the present experiments, we studied the effect of the serial order of stimuli and associated movements in macaque monkeys overtrained to make arm-reaching movements in response to spatially distinct visual targets. Under different conditions, the temporal structure of the motor sequence was varied by changing the duration of the interval between successive target stimuli or by adding a cue that reliably signaled the onset time of the forthcoming target stimulus. In each condition, the extent to which the monkeys are sensitive to the spatial regularities was assessed by comparing performance when stimulus locations follow a repeating sequence, as opposed to a random sequence. We observed no improvement in task performance on repeated sequence blocks, compared to random sequence blocks, when target stimuli are relatively distant from each other in time. On the other hand, the shortening of the time interval between successive target stimuli or, more efficiently, the addition of a temporal cue before the target stimulus yielded a performance advantage under repeated sequence, reflected in a decrease in the latency of arm and saccadic eye movements accompanied by an increased tendency for eye movements to occur in an anticipatory manner. Contrary to the effects on movement initiation, the serial order of stimuli and movements did not markedly affect the execution of movement. Moreover, the location of a given target in the random sequence influenced task performance based on the location of the preceding target, monkeys being faster in responding as a result of familiarity caused by extensive practice with some target transitions also used in the repeated sequence. This performance advantage was most prominently detectable when temporal prediction of forthcoming target stimuli was optimized. Taken together, the present findings demonstrate that the monkey’s capacity to make use of serial order information to speed task performance was dependent on the temporal structure of the motor sequence

Stop and Think about Basal Ganglia Functional Organization: The Pallido-Striatal “Stop” Route

International audienceThe "arkypallidal" neurons of the globus pallidus (external segment) emit feedback GABAergic projections to the striatum. In this issue of Neuron, Mallet et al. (2015) show that "arkypallidal" neurons provide a Stop signal, suppressing the development of Go-related striatal activity

The Role of Striatal Tonically Active Neurons in Reward Prediction Error Signaling during Instrumental Task Performance

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Tonically active neurons in the striatum differentiate between delivery and omission of expected reward in a probabilistic task context

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Higher neuronal discharge rate in the motor area of the subthalamic nucleus of Parkinsonian patients

International audienceIn Parkinson's disease, pathological synchronous oscillations divide the subthalamic nucleus (STN) of patients into a dorsolateral oscillatory region and ventromedial nonoscillatory region. This bipartite division reflects the motor vs. the nonmotor (associative/limbic) subthalamic areas, respectively. However, significant topographic differences in the neuronal discharge rate between these two STN subregions in Parkinsonian patients is still controversial. In this study, 119 STN microelectrode trajectories (STN length > 2 mm, mean = 5.32 mm) with discernible oscillatory and nonoscillatory regions were carried on 60 patients undergoing deep brain stimulation surgery for Parkinson's disease. 2,137 and 2,152 multiunit stable signals were recorded (recording duration > 10 s, mean = 21.25 s) within the oscillatory and nonoscillatory STN regions, respectively. Spike detection and sorting were applied offline on every multiunit stable signal using an automatic method with systematic quantification of the isolation quality (range = 0–1) of the identified units. In all, 3,094 and 3,130 units were identified in the oscillatory and nonoscillatory regions, respectively. On average, the discharge rate of better-isolated neurons (isolation score > 0.70) was higher in the oscillatory region than the nonoscillatory region (44.55 ± 0.87 vs. 39.97 ± 0.77 spikes/s, N = 665 and 761, respectively). The discharge rate of the STN neurons was positively correlated to the strength of their own and their surrounding 13- to 30-Hz beta oscillatory activity. Therefore, in the Parkinsonian STN, beta oscillations and higher neuronal discharge rate are correlated and coexist in the motor area of the STN compared with its associative/limbic area