Experience of a First, “Whisker-Dependent,” Skill Affects the Induction of c-Fos Expression in Somatosensory Cortex Barrel Field Neurons in Rats on Training to a Second Skill (original) (raw)
Related papers
Frontiers in Behavioral Neuroscience, 2013
Learning is known to be accompanied by induction of c-Fos expression in cortical neurons. However, not all neurons are involved in this process. What the c-Fos expression pattern depends on is still unknown. In the present work we studied whether and to what degree previous animal experience about Task 1 (the first phase of an instrumental learning) influenced neuronal c-Fos expression in the retrosplenial cortex during acquisition of Task 2 (the second phase of an instrumental learning). Animals were progressively shaped across days to bar-press for food at the left side of the experimental chamber (Task 1). This appetitive bar-pressing behavior was shaped by nine stages ("9 stages" group), five stages ("5 stages" group) or one intermediate stage ("1 stage" group). After all animals acquired the first skill and practiced it for five days, the bar and feeder on the left, familiar side of the chamber were inactivated, and the animals were allowed to learn a similar instrumental task at the opposite side of the chamber using another pair of a bar and a feeder (Task 2). The highest number of c-Fos positive neurons was found in the retrosplenial cortex of "1 stage" animals as compared to the other groups. The number of c-Fos positive neurons in "5 stages" group animals was significantly lower than in "1 stage" animals and significantly higher than in "9 stages" animals. The number of c-Fos positive neurons in the cortex of "9 stages" animals was significantly higher than in home caged control animals. At the same time, there were no significant differences between groups in such behavioral variables as the number of entrees into the feeder or bar zones during Task 2 learning. Our results suggest that c-Fos expression in the retrosplenial cortex during Task 2 acquisition was influenced by the previous learning history.
Fos expression and task-related neuronal activity in rat cerebral cortex after instrumental learning
Neuroscience, 2005
Learning has been shown to induce changes in neuronal gene expression and to produce development of task-specific neuronal activity. The connection between these two features of neuronal plasticity remains of a great interest. To address this issue we compared distribution of c-Fos expressing and task-related neurons in the rat cerebral cortex following instrumental learning of appetitive leverpress task. The number of Fos-positive neurons was determined immunohistochemically in the retrosplenial and the motor cortex of naive ("control" group), newly trained ("acquisition" group) and overtrained ("performance" group) animals. A significant activation of c-Fos expression was observed in the neurons of the retrosplenial but not motor cortex in the "acquisition" group rats, as compared with the "control" and "performance" groups. In accordance with this c-Fos expression difference, the retrosplenial cortex of the trained animals contained significantly more neurons with lever-press-related activity than the motor cortex. Therefore, the two examined cortical areas showed a parallel between experience-dependent induction of c-Fos and development of task-related neuronal activity. These data support a notion that learning-induced activation of c-Fos is associated with long-term neurophysiological changes produced by training.
Journal of Behavioral and Brain Science, 2015
To address the issue of how hippocampal neurons are involved into learning progress, we studied c-Fos expression in rat hippocampal subfields at different stages of appetitive instrumental learning. To model the first stage of learning, we pre-trained animals to approach the lever to obtain the food, and then made this behavior ineffective by not reinforcing it during the last session ("mismatch" group). Another group just acquired lever-pressing behavior at that day ("acquisition" group). Animals of the third group performed this well-trained behavior ("performance" group). The number of Fos-positive neurons in all hippocampal regions of the "mismatch" group animals was higher than in the ones of the home cage control group animals. The number of Fos-positive neurons was increased in CA1 and CA3 areas, but not in the dentate gyrus of both the "acquisition" and "performance" group animals as compared with the control group. We also found segmented c-Fos expression, which was more evident in "acquisition" group animals. Thus, our results suggest that during the first (mismatch) stage of learning hippocampal neurons are activated in an equally distributed manner. The following clustered pattern of activated CA1 neurons during the acquisition stage may reflect specialization of these neurons in respect to the specific lever-pressing behavior.
Although it is generally assumed that brain circuits are modified by new experiences, the question of which changes in synaptic efficacy take place in cortical and subcortical circuits across the learning process remains unanswered. Rats were trained in the acquisition of an operant conditioning in a Skinner box provided with light beams to detect animals' approaches to lever and feeder. Behaviors such as pressing the lever, eating, exploring, and grooming were also recorded. Animals were chronically implanted with stimulating and recording electrodes in hippocampal, prefrontal, and subcortical sites relevant to the task. Field synaptic potentials were evoked during the performance of the above-mentioned behaviors and before, during, and after the acquisition process. Afferent pathways to the hippocampus and the intrinsic hippocampal circuit were slightly modified in synaptic strength during the performance of those behaviors. In contrast, afferent and efferent circuits of the medial prefrontal cortex were significantly modified in synaptic strength across training sessions, mostly at the moment of the largest change in the learning curve. Performance of behaviors nondirectly related to the acquisition process (exploring, grooming) also evoked changes in synaptic strength across training. This study helps to understand when and where learning is being engraved in the brain.
Learning & Memory, 2007
The role of the primary motor cortex in the acquisition of new motor skills was evaluated during classical conditioning of vibrissal protraction responses in behaving mice, using a trace paradigm. Conditioned stimulus (CS) presentation elicited a characteristic field potential in the vibrissal motor cortex, which was dependent on the synchronized firing of layer V pyramidal cells. CS-evoked and other event-related potentials were particular cases of a motor cortex oscillatory state related to the increased firing of pyramidal neurons and to vibrissal activities. Along conditioning sessions, but not during pseudoconditioning, CS-evoked field potentials and unitary pyramidal cell responses grew with a time-course similar to the percentage of vibrissal conditioned responses (CRs), and correlated significantly with CR parameters. High-frequency stimulation of barrel cortex afferents to the vibrissal motor cortex mimicked CS-related potentials growth, suggesting that the latter process was due to a learning-dependent potentiation of cortico-cortical synaptic inputs. This potentiation seemed to enhance the efficiency of cortical commands to whisker-pad intrinsic muscles, enabling the generation of acquired motor responses.
Nature Communications, 2019
Previous studies indicate that the dorsolateral striatum (DLS) integrates sensorimotor information from cortical and thalamic regions to learn and execute motor habits. However, the exact contribution of sensory representations to this process is still unknown. Here we explore the role of the forelimb somatosensory flow in the DLS during the learning and execution of motor habits. First, we compare rhythmic somesthetic representations in the DLS and primary somatosensory cortex in anesthetized rats, and find that sequential and temporal stimuli contents are more strongly represented in the DLS. Then, using a behavioral protocol in which rats developed a stereotyped motor sequence, functional disconnection experiments, and pharmacologic and optogenetic manipulations in apprentice and expert animals, we reveal that somatosensory thalamic- and cortical-striatal pathways are indispensable for the temporal component of execution. Our results indicate that the somatosensory flow in the DL...
Distribution of tactile learning and its neural basis
Proceedings of The National Academy of Sciences, 1999
The brain's sensory processing systems are modified during perceptual learning. To learn more about the spatial organization of learning-related modifications, we trained rats to utilize the sensory signal from a single intact whisker to carry out a behavioral task. Once a rat had mastered the task, we clipped its ''trained'' whisker and attached a ''prosthetic'' one to a different whisker stub. We then tested the rat to determine how quickly it could relearn the task by using the new whisker. We observed that rats were immediately able to use the prosthetic whisker if it were attached to the stub of the trained whisker but not if it were attached to a different stub. Indeed, the greater the distance between the trained and prosthetic whisker, the more trials were needed to relearn the task. We hypothesized that this ''transfer'' of learning between whiskers might depend on how much the representations of individual whiskers overlap in primary somatosensory cortex. Testing this hypothesis by using 100-electrode cortical recordings, we found that the overlap between the cortical response patterns of two whiskers accounted well for the transfer of learning between them: The correlation between the electrophysiological and behavioral data was very high (r ؍ 0.98). These findings suggest that a topographically distributed memory trace for sensory-perceptual learning may reside in primary sensory cortex.
Pathway-specific reorganization of projection neurons in somatosensory cortex during learning
Nature neuroscience, 2015
In the mammalian brain, sensory cortices exhibit plasticity during task learning, but how this alters information transferred between connected cortical areas remains unknown. We found that divergent subpopulations of cortico-cortical neurons in mouse whisker primary somatosensory cortex (S1) undergo functional changes reflecting learned behavior. We chronically imaged activity of S1 neurons projecting to secondary somatosensory (S2) or primary motor (M1) cortex in mice learning a texture discrimination task. Mice adopted an active whisking strategy that enhanced texture-related whisker kinematics, correlating with task performance. M1-projecting neurons reliably encoded basic kinematics features, and an additional subset of touch-related neurons was recruited that persisted past training. The number of S2-projecting touch neurons remained constant, but improved their discrimination of trial types through reorganization while developing activity patterns capable of discriminating th...
Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill
Nature …, 2009
The learning of new skills is characterized by an initial phase of rapid improvement in performance and a phase of more gradual improvements as skills are automatized and performance asymptotes. Using in vivo striatal recordings, we observed region-specific changes in neural activity during the different phases of skill learning, with the associative or dorsomedial striatum being preferentially engaged early in training and the sensorimotor or dorsolateral striatum being engaged later in training. Ex vivo recordings from medium spiny striatal neurons in brain slices of trained mice revealed that the changes observed in vivo corresponded to regionaland training-specific changes in excitatory synaptic transmission in the striatum. Furthermore, the potentiation of glutamatergic transmission observed in dorsolateral striatum after extensive training was preferentially expressed in striatopallidal neurons, rather than striatonigral neurons. These findings demonstrate that region-and pathway-specific plasticity sculpts the circuits involved in the performance of the skill as it becomes automatized.
A cellular mechanism of reward-related learning
Nature, 2001
Positive reinforcement helps to control the acquisition of learned behaviours. Here we report a cellular mechanism in the brain that may underlie the behavioural effects of positive reinforcement. We used intracranial self-stimulation (ICSS) as a model of reinforcement learning, in which each rat learns to press a lever that applies reinforcing electrical stimulation to its own substantia nigra. The outputs from neurons of the substantia nigra terminate on neurons in the striatum in close proximity to inputs from the cerebral cortex on the same striatal neurons. We measured the effect of substantia nigra stimulation on these inputs from the cortex to striatal neurons and also on how quickly the rats learned to press the lever. We found that stimulation of the substantia nigra (with the optimal parameters for lever-pressing behaviour) induced potentiation of synapses between the cortex and the striatum, which required activation of dopamine receptors. The degree of potentiation within ten minutes of the ICSS trains was correlated with the time taken by the rats to learn ICSS behaviour. We propose that stimulation of the substantia nigra when the lever is pressed induces a similar potentiation of cortical inputs to the striatum, positively reinforcing the learning of the behaviour by the rats.