The motirod: a novel physical skill task that enhances motivation to learn and thereby increases neurogenesis especially in the female hippocampus

DiFeo, Gina; Curlik, Daniel M.; Shors, Tracey J.

doi:10.1016/j.brainres.2014.11.045

Cited by 7 publications

(5 citation statements)

References 50 publications

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“…If cognitive improvement requires synaptic as well as dendritic arbor re-organization in the CA1, then this type of change may very well require more than 3-4 days, since synapses in CA1 are removed from those in the dentate gyrus by at least two synaptic relays. (Curlik 2nd, Difeo, & Shors, 2014;DiFeo, Curlik 2nd, & Shors, 2015). Perhaps it is only at the highest levels of wheel activity that BDNF is released at levels that are sufficiently high to augment neurogenesis beyond the basal levels that are already characteristically high during adolescence.…”

Section: Food Restriction Results In Improvement Of Cognitive Functmentioning

confidence: 99%

Effects of adolescent experience of food restriction and exercise on spatial learning and open field exploration of female rats

2020

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The hippocampus carries out multiple functions: spatial cognition dorsally (DH) and regulation of emotionality-driven behavior ventrally (VH). Previously, we showed that dendrites of DH and VH pyramidal neurons of female rats are still developing robustly during adolescence and are altered by the experience of food restriction and voluntary exercise on a wheel. We tested whether such anatomical changes during adolescence impact anxiety-like behavior and spatial cognition. Four groups of female rats were evaluated for these behaviors: those with wheel access in its cage from postnatal day (P) 36-44 (EX); those with food access restricted to 1 hr per day, from P40 to 44 (FR); those with EX from P36 to 44, combined with FR from P40 to 44, which we will refer to as EX + FR; and controls, CON (no EX, no FR). Open field test for anxiety-like behavior and active place avoidance test for spatial cognition were conducted at P47-49, the age when food restricted animals have restored body weight, or at P54-56, to identify more enduring effects. Anxiety-like behavior was elevated for the EX and FR groups at P47-49 but not for the EX + FR group. By P54-56, the EX + FR and EX groups exhibited less anxiety-like behavior, indicating a beneficial delayed main effect of exercise. There was a beneficial main effect of food restriction upon cognition, as the FR group showed cognition superior to CONs' at P44-46 and P54-56, while the EX + FR animals also showed enhanced spatial learning at P54-56. EX + FR animals with best adaptation to the feeding schedule showed the best spatial learning performance but with a delay. The EX group exhibited only a transient improvement. These findings indicate that FR, EX, and EX + FR in midadolescence are all beneficial in reducing anxiety-like behavior and improving spatial cognition but with subtle differences in the timing of their manifestation, possibly reflecting the protracted maturation of the hippocampus.

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Section: Food Restriction Results In Improvement Of Cognitive Functmentioning

confidence: 99%

Effects of adolescent experience of food restriction and exercise on spatial learning and open field exploration of female rats

2020

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“…However, several additional studies have revealed that other forms of learning can also prevent the death of these cells. For example, acquisition of social transmission of food preference (Olariu, Cleaver, Shore, Brewer, & Cameron, 2005) and learning a new motor skill (Curlik et al, 2013; DiFeo et al, 2015) also prevent cell death. The present study extends this literature by revealing that acquisition of an easy-to-perform appetitive conditioning task can also prevent the death of adult-born hippocampal cells.…”

Section: Discussionmentioning

confidence: 99%

“…Moreover, acquisition of operant procedures has been shown to activate hippocampal circuitry (Jurado-Parras et al, 2013; Rapanelli, Frick, & Zanutto, 2009; Rapanelli, Lew, Frick, & Zanutto, 2010), and this hippocampal activation may increase the number of surviving cells in the dentate gyrus. Furthermore, myriad studies have revealed that both hippocampal-dependent and hippocampal-independent forms of learning can prevent the death of these adult-born cells (Curlik et al, 2013; Dalla, Bangasser, Edgecomb, & Shors, 2007; DiFeo, Curlik, & Shors, 2015). Therefore, acquisition of a reward-dependent operant procedure may also influence the number of surviving hippocampal cells, regardless of whether the hippocampus is necessary for that form of learning.…”

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confidence: 99%

Operant conditioning prevents cell death in the adult rat dentate gyrus.

Huggins¹,

Curlik²

2019

Behavioral Neuroscience

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Thousands of new neurons are produced each day in the dentate gyrus of the adult mammalian hippocampus. However, the majority of those cells die within weeks of their birth. The most effective way to prevent this cell death is through effortful and successful learning. Myriad studies have revealed that classical conditioning and spatial learning can prevent this cell death. However, little research has examined whether acquisition of an operant conditioning task with an appetitive reward also increases the number of surviving cells. Therefore, the current study was conducted to determine whether conditioning with an operant procedure would prevent the death of adult-born hippocampal cells. Adult male rats were trained with 50 trials of an operant discrimination procedure per day for four consecutive days. In order to motivate animals to perform the task, they were food restricted prior to conditioning, and food pellets were used as an appetitive reward during training. Additional control animals were food restricted but not trained, or not food restricted and not trained. In order to ensure that exposure to food reward pellets did not alter cell survival, all animals received equal exposure to the food pellets. Stereological analysis conducted approximately two weeks after training revealed that food restriction decreased the number of surviving cells in the dentate gyrus (p < .05). However, training with the operant task prevented that decrease (p < .05). Together, these results indicate that food restriction decreased the number of surviving cells in the dentate gyrus, and training with an operant procedure was sufficient to attenuate that decrease.

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“…In contrast, neuroimaging approaches have shown that the hippocampus displays higher rates of micro-structural changes in rotarod-trained mice compared with untrained controls and, accordingly, this brain region is larger in the best performers (Scholz et al, 2015). Furthermore, the accelerating rotarod task induces Fos expression (a marker of neural activation) labeling (Nagai et al, 2017), mTOR and cAMP-dependent protein kinase expression (Bergeron et al, 2014;Chagniel et al, 2014), and neurogenesis (DiFeo et al, 2015) in the hippocampus. These observations indicate that the hippocampus is recruited and likely to play a role in the modulation of motor skills learning.…”

Section: Introductionmentioning

confidence: 99%

Hippocampal Egr1-Dependent Neuronal Ensembles Negatively Regulate Motor Learning

et al. 2022

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Motor skills learning is classically associated with brain regions including cerebral and cerebellar cortices and basal ganglia nuclei. Less is known about the role of the hippocampus in the acquisition and storage of motor skills. Here, we show that mice receiving a long-term training in the accelerating rotarod display marked hippocampal transcriptional changes and reduced pyramidal neurons activity in the CA1 region when compared with naive mice. Then, we use mice in which neural ensembles are permanently labeled in an Egr1 activity-dependent fashion. Using these mice, we identify a subpopulation of Egr1-expressing pyramidal neurons in CA1 activated in short-term (STT) and long-term (LTT) trained mice in the rotarod task. When Egr1 is downregulated in the CA1 or these neuronal ensembles are depleted, motor learning is improved whereas their chemogenetic stimulation impairs motor learning performance. Thus, Egr1 organizes specific CA1 neuronal ensembles during the accelerating rotarod task that limit motor learning. These evidences highlight the role of the hippocampus in the control of this type of learning and we provide a possible underlying mechanism.

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The motirod: a novel physical skill task that enhances motivation to learn and thereby increases neurogenesis especially in the female hippocampus

Cited by 7 publications

References 50 publications

Effects of adolescent experience of food restriction and exercise on spatial learning and open field exploration of female rats

Effects of adolescent experience of food restriction and exercise on spatial learning and open field exploration of female rats

Operant conditioning prevents cell death in the adult rat dentate gyrus.

Hippocampal Egr1-Dependent Neuronal Ensembles Negatively Regulate Motor Learning

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