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An operant is a behavioral act that has an impact on the environment to produce an outcome, constituting an important component of voluntary behavior. Because the environment can be volatile, the same action may cause different consequences. Thus to obtain an optimal outcome, it is crucial to detect action-outcome relationships and adapt the behavior accordingly. Although prefrontal neurons are known to change activity depending on expected reward, it remains unknown whether prefrontal activity contributes to obtaining reward. We investigated this issue by setting variable relationships between levels of single-neuron activity and rewarding outcomes. Lateral prefrontal neurons changed their spiking activity according to the specific requirements for gaining reward, without the animals making a motor response. Thus spiking activity constituted an operant response. Data from a control task suggested that these changes were unlikely to reflect simple reward predictions. These data demonstrate a remarkable capacity of prefrontal neurons to adapt to specific operant requirements at the single-neuron level.
Adapting one's behavior to environmental conditions and past experience is a key trait of living systems. In the biological world, there is evidence for adaptive behaviors such as learning even in naturally occurring, non-neural, single-celled organisms. In the bioengineered world, advances in synthetic cell engineering and biorobotics have created the possibility of implementing lifelike systems engineered from the bottom up. This will require the development of programmable control circuitry for such biomimetic systems that is capable of realizing such non-trivial and adaptive behavior, including modification of subsequent behavior in response to environmental feedback. To this end, we report the design of novel stochastic chemical reaction networks capable of probabilistic decision-making in response to stimuli. We show that a simple chemical reaction network motif can be tuned to produce arbitrary decision probabilities when choosing between two or more responses to a stimulus signal. We further show that simple feedback mechanisms from the environment can modify these probabilities over time, enabling the system to adapt its behavior dynamically in response to positive or negative reinforcement based on its decisions. This system thus acts as a form of operant conditioning of the chemical circuit, in the sense that feedback provided based on decisions taken by the circuit form the basis of the learning process. Our work thus demonstrates that simple chemical systems can be used to implement lifelike behavior in engineered biomimetic systems.
Recent advances in neuroimaging and genetics have made mice an advantageous animal model for studying the neurophysiology of sensation, cognition, and locomotion. A key benefit of mice is that they provide a large population of test subjects for behavioral screening. Reflex-based assays of hearing in mice, such as the widely used acoustic startle response, are less accurate than operant conditioning in measuring auditory processing. To date, however, there are few cost-effective options for scalable operant conditioning systems. Here, we describe a new system for automated operant conditioning, the Psibox. It is assembled from low cost parts, designed to fit within typical commercial wire-top cages, and allows large numbers of mice to train independently in their home cages on positive reinforcement tasks. We found that groups of mice trained together learned to accurately detect sounds within 2 weeks of training. In addition, individual mice isolated from groups also showed good task performance. The Psibox facilitates high-throughput testing of sensory, motor, and cognitive skills in mice, and provides a readily available animal population for studies ranging from experience-dependent neural plasticity to rodent models of mental disorders.
Operant conditioning (OC) is a classical paradigm and a standard technique used in experimental psychology in which animals learn to perform an action to achieve a reward. By using this paradigm, it is possible to extract learning curves and measure accurately reaction times (RTs). Both these measurements are proxy of cognitive capabilities and can be used to evaluate the effectiveness of therapeutic interventions in mouse models of disease. Here, we describe a fully 3D printable device that is able to perform OC on freely moving mice, while performing real-time tracking of the animal position. We successfully trained six mice, showing stereotyped learning curves that are highly reproducible across mice and reaching >70% of accuracy after 2 d of conditioning. Different products for OC are commercially available, though most of them do not provide customizable features and are relatively expensive. This data demonstrate that this system is a valuable alternative to available state-of-the-art commercial devices, representing a good balance between performance, cost, and versatility in its use.
Numerical discrimination is widespread in vertebrates, but this capacity varies enormously between the different species examined. The guppy (Poecilia reticulata), the only teleost examined following procedures that allow a comparison with the other vertebrates, outperforms amphibians, reptiles and many warm-blooded vertebrates, but it is unclear whether this is a feature shared with the other teleosts or represents a peculiarity of this species. We trained zebrafish (Danio rerio) to discriminate between numbers differing by one unit, varying task difficulty from 2 versus 3 to 5 versus 6 items. Non-numerical variables that covary with number, such as density or area, did not affect performance. Most fish reached learning criterion on all tasks up to 4 versus 5 discrimination with no sex difference in accuracy. Although no individual reached learning criterion in the 5 versus 6 task, performance was significant at the group level, suggesting that this may represent the discrimination threshold for zebrafish. Numerosity discrimination abilities of zebrafish compare to those of guppy, being higher than in some warm-blooded vertebrates, such as dogs, horses and domestic fowl, though lower than in parrots, corvids and primates. Learning rate was similar in a control group trained to discriminate between different-sized shapes, but zebrafish were slightly more accurate when discriminating areas than numbers and males were more accurate than females. At the end of the experiment, fish trained on numbers and controls trained on areas generalized to the reciprocal set of stimuli, indicating they had used a relational strategy to solve these tasks.
Brain activity is known to be voluntarily controllable by neurofeedback, a kind of electroencephalographic (EEG) operant conditioning. Although its efficacy in clinical effects has been reported, it is yet to be uncovered whether or how a specific band activity is controllable. Here, we examined EEG spectral profiles along with conditioning training of a specific brain activity, theta band (4-8 Hz) amplitude, in rats.
Operant conditioning of aerial respiratory behaviour and its consolidation into long-term memory in Lymnaea has been previously studied in both intact, freely moving snails and in in vitro preparations made from previously trained snails. Here, we show in previously untrained semi-intact in vitro Lymnaea preparations that aerial respiratory behaviour can also be operantly conditioned. Neither yoked control nor 'run-down' control procedures in these in vitro preparations result in an alteration of aerial respiratory behaviour. Memory in the operantly trained semi-intact preparations persists for at least 1h after training. Intracellular recordings made from RPeD1, one of the 3-CPG neurons and the neuron that initiates CPG activity; show that there are specific changes in central excitatory input to this neuron concurrent with learning and its consolidation into memory. In addition following the acquisition of learning and its consolidation into memory the ability of RPeD1 and VI/J neurons when depolarized to cause a pneumostome opening is significantly decreased. Thus, previously untrained in vitro semi-intact preparations can be used to study changes in neuronal activity in a neuron known to be both necessary for the behaviour and for memory formation.
Loss of motivation and learning impairments are commonly accepted core symptoms of psychiatric disorders such as depression and schizophrenia. Reward-motivated learning is dependent on the hippocampal formation but the molecular mechanisms that lead to functional incentive motivation in this brain region are still largely unknown. Recent evidence implicates neurotransmission via metabotropic glutamate receptors and Homer1, their interaction partner in the postsynaptic density, in drug addiction and motivational learning. As previous reports mainly focused on the prefrontal cortex and the nucleus accumbens, we now investigated the role of hippocampal Homer1 in operant reward learning in the present study. We therefore tested either Homer1 knockout mice or mice that overexpress Homer1 in the hippocampus in an operant conditioning paradigm. Our results show that deletion of Homer1 leads to a diverging phenotype that either displays an inability to perform the task or outstanding hyperactivity in both learning and motivational sessions. Due to the apparent bimodal distribution of this phenotype, the overall effect of Homer1 deletion in this paradigm is not significantly altered. Overexpression of hippocampal Homer1 did not lead to a significantly altered learning performance in any stage of the testing paradigm, yet may subtly contribute to emerging motivational deficits. Our results indicate an involvement of Homer1-mediated signaling in the hippocampus in motivation-based learning tasks and encourage further investigations regarding the specific molecular underpinnings of the phenotypes observed in this study. We also suggest to cautiously interpret the results of this and other studies regarding the phenotype following Homer1 manipulations in animals, since their behavioral phenotype appears to be highly diverse. Future studies would benefit from larger group sizes that would allow splitting the experimental groups in responders and non-responders.
Stroke-related sensory and motor deficits often steal away the independent mobility and balance from stroke survivors. Often, this compels the stroke survivors to rely heavily on their non-paretic leg during weight shifting to execute activities of daily living (ADL), with reduced usage of the paretic leg. Increased reliance on non-paretic leg often leads to learned nonuse of the paretic leg. Therefore, it is necessary to measure the contribution of individual legs toward one's overall balance. In turn, techniques can be developed to condition the usage of both the legs during one's balance training, thereby encouraging the hemiplegic patients for increased use of their paretic leg. The aim of this study is to (1) develop a virtual reality (VR)-based balance training platform that can estimate the contribution of each leg during VR-based weight-shifting tasks in an individualized manner and (2) understand the implication of operant conditioning paradigm during balance training on the overall balance of hemiplegic stroke patients.
To study the heritability of different training stages of appetitive operant conditioning, we carried out behavioral screening of 5 standard inbred mouse strains, 28 recombinant-inbred (BxD) mouse lines and their progenitor strains C57BL/6J and DBA/2J. We also computed correlations between successive training stages to study whether learning deficits at an advanced stage of operant conditioning may be dissociated from normal performance in preceding phases of training. The training consisted of two phases: an operant nose poking (NP) phase, in which mice learned to collect a sucrose pellet from a food magazine by NP, and an operant lever press and NP phase, in which mice had to execute a sequence of these two actions to collect a food pellet. As a measure of magazine oriented exploration, we also studied the nose poke entries in the food magazine during the intertrial intervals at the beginning of the first session of the nose poke training phase. We found significantly heritable components in initial magazine checking behavior, operant NP and lever press-NP. Performance levels in these phases were positively correlated, but several individual strains were identified that showed poor lever press-NP while performing well in preceding training stages. Quantitative trait loci mapping revealed suggestive likelihood ratio statistic peaks for initial magazine checking behavior and lever press-NP. These findings indicate that consecutive stages toward more complex operant behavior show significant heritable components, as well as dissociability between stages in specific mouse strains. These heritable components may reside in different chromosomal areas.
Executive functions, learning and attention are imperative facets of cognitive performance, affected in many neuropsychiatric disorders. Recently, we have shown that recombinant human erythropoietin improves cognitive functions in patients with chronic schizophrenia, and that it leads in healthy mice to enhanced hippocampal long-term potentiation, an electrophysiological correlate of learning and memory. To create an experimental basis for further mechanistic insight into erythropoietin-modulated cognitive processes, we employed the Five Choice Serial Reaction Time Task. This procedure allows the study of the effects of erythropoietin on discrete processes of learning and attention in a sequential fashion.
The common marmoset (Callithrix jacchus) is a small New World primate that has increasingly been used as a non-human model in the fields of sensory, motor, and cognitive neuroscience. However, little knowledge exists regarding behavioral methods in this species. Developing an understanding of the neural basis of perception and cognition in an animal model requires measurement of both brain activity and behavior. Here we describe an operant conditioning behavioral training method developed to allow controlled psychoacoustic measurements in marmosets. We demonstrate that marmosets can be trained to consistently perform a Go/No-Go auditory task in which a subject licks at a feeding tube when it detects a sound. Correct responses result in delivery of a food reward. Crucially, this operant conditioning task generates little body movement and is well suited for pairing behavior with single-unit electrophysiology. Successful implementation of an operant conditioning behavior opens the door to a wide range of new studies in the field of auditory neuroscience using the marmoset as a model system.
Learning which stimuli (classical conditioning) or which actions (operant conditioning) predict rewards or punishments can improve chances of survival. However, the circuit mechanisms that underlie distinct types of associative learning are still not fully understood. Automated, high-throughput paradigms for studying different types of associative learning, combined with manipulation of specific neurons in freely behaving animals, can help advance this field. The Drosophila melanogaster larva is a tractable model system for studying the circuit basis of behaviour, but many forms of associative learning have not yet been demonstrated in this animal. Here, we developed a high-throughput (i.e. multi-larva) training system that combines real-time behaviour detection of freely moving larvae with targeted opto- and thermogenetic stimulation of tracked animals. Both stimuli are controlled in either open- or closed-loop, and delivered with high temporal and spatial precision. Using this tracker, we show for the first time that Drosophila larvae can perform classical conditioning with no overlap between sensory stimuli (i.e. trace conditioning). We also demonstrate that larvae are capable of operant conditioning by inducing a bend direction preference through optogenetic activation of reward-encoding serotonergic neurons. Our results extend the known associative learning capacities of Drosophila larvae. Our automated training rig will facilitate the study of many different forms of associative learning and the identification of the neural circuits that underpin them.
The honey bee has been an important model organism for studying learning and memory. More recently, the honey bee has become a valuable model to understand perception and cognition. However, the techniques used to explore psychological phenomena in honey bees have been limited to only a few primary methodologies such as the proboscis extension reflex, sting extension reflex, and free flying target discrimination-tasks. Methods to explore operant conditioning in bees and other invertebrates are not as varied as with vertebrates. This may be due to the availability of a suitable response requirement. In this manuscript we offer a new method to explore operant conditioning in honey bees: the cap pushing response (CPR). We used the CPR to test for difference in learning curves between novel auto-shaping and more traditional explicit-shaping. The CPR protocol requires bees to exhibit a novel behavior by pushing a cap to uncover a food source. Using the CPR protocol we tested the effects of both explicit-shaping and auto-shaping techniques on operant conditioning. The goodness of fit and lack of fit of these data to the Rescorla-Wagner learning-curve model, widely used in classical conditioning studies, was tested. The model fit well to both control and explicit-shaping results, but only for a limited number of trials. Learning ceased rather than continuing to asymptotically approach the physiological most accurate possible. Rate of learning differed between shaped and control bee treatments. Learning rate was about 3 times faster for shaped bees, but for all measures of proficiency control and shaped bees reached the same level. Auto-shaped bees showed one-trial learning rather than the asymptotic approach to a maximal efficiency. However, in terms of return-time, the auto-shaped bees' learning did not carry over to the covered-well test treatments.
Animal personality and individuality are intensively researched in vertebrates and both concepts are increasingly applied to behavioral science in insects. However, only few studies have looked into individuality with respect to performance in learning and memory tasks. In vertebrates, individual learning capabilities vary considerably with respect to learning speed and learning rate. Likewise, honeybees express individual learning abilities in a wide range of classical conditioning protocols. Here, we study individuality in the learning and memory performance of cockroaches, both in classical and operant conditioning tasks. We implemented a novel classical (olfactory) conditioning paradigm where the conditioned response is established in the maxilla-labia response (MLR). Operant spatial learning was investigated in a forced two-choice task using a T-maze. Our results confirm individual learning abilities in classical conditioning of cockroaches that was reported for honeybees and vertebrates but contrast long-standing reports on stochastic learning behavior in fruit flies. In our experiments, most learners expressed a correct behavior after only a single learning trial showing a consistent high performance during training and test. We can further show that individual learning differences in insects are not limited to classical conditioning but equally appear in operant conditioning of the cockroach.
Operant conditioning is a crucial tool in neuroscience research for probing brain function. While molecular, anatomical and even physiological techniques have seen radical increases in throughput, efficiency, and reproducibility in recent years, behavioural tools have somewhat lagged behind. Here we present a fully automated, high-throughput system for self-initiated conditioning of up to 25 group-housed, radio-frequency identification (RFID) tagged mice over periods of several months and >106 trials. We validate this "AutonoMouse" system in a series of olfactory behavioural tasks and show that acquired data is comparable to previous semi-manual approaches. Furthermore, we use AutonoMouse to systematically probe the impact of graded olfactory bulb lesions on olfactory behaviour, demonstrating that while odour discrimination in general is robust to even most extensive disruptions, small olfactory bulb lesions already impair odour detection. Discrimination learning of similar mixtures as well as learning speed are in turn reliably impacted by medium lesion sizes. The modular nature and open-source design of AutonoMouse should allow for similar robust and systematic assessments across neuroscience research areas.
Neuronal motor commands, whether generating real or neuroprosthetic movements, are shaped by ongoing sensory feedback from the displacement being produced. Here we asked if cortical stimulation could provide artificial feedback during operant conditioning of cortical neurons. Simultaneous two-photon imaging and real-time optogenetic stimulation were used to train mice to activate a single neuron in motor cortex (M1), while continuous feedback of its activity level was provided by proportionally stimulating somatosensory cortex. This artificial signal was necessary to rapidly learn to increase the conditioned activity, detect correct performance, and maintain the learned behavior. Population imaging in M1 revealed that learning-related activity changes are observed in the conditioned cell only, which highlights the functional potential of individual neurons in the neocortex. Our findings demonstrate the capacity of animals to use an artificially induced cortical channel in a behaviorally relevant way and reveal the remarkable speed and specificity at which this can occur.
Altered functioning of GABAergic interneurons expressing parvalbumin (PV) in the basal ganglia-thalamo-cortical circuit are likely to be involved in several human psychiatric disorders characterized by deficits in attention and sensory gating with dysfunctional decision-making behavior. However, the contribution of these interneurons in the ability to acquire demanding learning tasks remains unclear. Here, we combine an operant conditioning task with local field potentials simultaneously recorded in several nuclei involved in reward circuits of wild-type (WT) and PV-deficient (PVKO) mice, which are characterized by changes in firing activity of PV-expressing interneurons. In comparison with WT mice, PVKO animals presented significant deficits in the acquisition of the selected learning task. Recordings from prefrontal cortex, nucleus accumbens (NAc) and hippocampus showed significant decreases of the spectral power in beta and gamma bands in PVKO compared with WT mice particularly during the performance of the operant conditioning task. From the first to the last session, at all frequency bands the spectral power in NAc tended to increase in WT and to decrease in PVKO. Results indicate that PV deficiency impairs signaling necessary for instrumental learning and the recognition of natural rewards.
Reinforcement learning theories postulate that prediction error, i.e., a discrepancy between the actual and expected outcomes, drives reconsolidation and new learning, inducing an updating of the initial memory. Pavlovian studies have shown that prediction error detection is a fundamental mechanism in triggering amygdala-dependent memory updating, where the temporal relationship between stimuli plays a critical role. However, in contrast to the well-established findings in aversive situations (e.g., fear conditioning), only few studies exist on prediction error in appetitive operant conditioning, and even less with regard to the role of temporal parameters. To explore if temporal prediction error in an appetitive operant paradigm could generate an updating and consequent reconsolidation and/or new learning of temporal association, we ran four experiments in adult male rats. Experiment 1 verified whether an unexpected delay in the time of reward's availability (i.e., a negative temporal prediction error) in a single session produces an updating in long-term memory of temporal expectancy in an appetitive operant conditioning. Experiment 2 showed that negative prediction errors, either due to the temporal change or through reward omission, increased in the basolateral amygdala nucleus (BLA) the activation of a protein that is critical for memory formation. Experiment 3 revealed that the presence of a protein synthesis inhibitor (anisomycin) in the BLA during the session when the reward was delayed (Error session) affected the temporal updating. Finally, Experiment 4 showed that anisomycin, when infused immediately after the Error session, interfered with the long-term memory of the temporal updating. Together, our study demonstrated an involvement of BLA after a change in temporal and reward contingencies, and in the resulting updating in long-term memory in appetitive operant conditioning.
Extended fear training can lead to initially low fear expression that grows over time, termed fear incubation. Conversely, a single fear conditioning session typically results in high fear initially that is sustained over time. Fear expression decreases across extended training, suggesting that a fear extinction-like process might be responsible for low fear observed soon after training. Because of the prominent role medial prefrontal cortex (mPFC) plays in fear conditioning and extinction, we decided to examine Fos expression resulting from a cued fear retrieval test to gain insight into possible mechanisms involved in extended training fear incubation. Male Long-Evans rats received 1 or 10 days of tone-shock pairings or tone-only exposure (while lever-pressing for food). Two days after the end of fear training, rats received a cued fear test, with perfusions timed to visualize Fos expression during test. As expected, the limited fear conditioning group exhibited higher fear in the test than any of the other groups (as measured with conditioned suppression of lever-pressing). Interestingly, we found that extended training animals (whether they received tone-shock pairings or tone-only exposure) expressed higher levels of Fos in both prelimbic and infralimbic cortices than limited training animals. There was no association between fear expression and mPFC Fos expression. These results suggest we may have visualized Fos expression related to operant overtraining rather than conditioned fear related processes. Further research is needed to determine the neurobiological basis of extended training fear incubation and to determine processes represented by the pattern of Fos expression we observed.
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