Reduction of restricted repetitive behavior by environmental enrichment: Potential neurobiological mechanisms

Farmer, Anna L.; Lewis, Mark H.

doi:10.1016/j.neubiorev.2023.105291

Cited by 5 publications

(3 citation statements)

References 267 publications

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“…In the past decade, few studies investigated the role epigenetics in the regulation of physiological and maladaptive habitual behaviors ( Langen et al, 2011 ; Shiflett and Balleine, 2011 ; Malvaez et al, 2018 ). While extensive evidence has been gathered about the development of maladaptive habit formation upon drug abuse and its effect on synaptic plasticity ( Ostlund and Balleine, 2008 ; Corbit et al, 2014 ; Nestler, 2014 ; Nestler and Lüscher, 2019 ), less information is available concerning repetitive behaviors ( Farmer and Lewis, 2023 ). Epigenetic modifications of chromatin offer a mechanistic link between the genome and environmental experiences given their ability to alter the chromatin landscape, promptly adapting the molecular and cellular substrates to the requests of everyday life.…”

Section: Beyond Genetics: Epigenetic Players In Pathological Repetiti...mentioning

confidence: 99%

Striatal insights: a cellular and molecular perspective on repetitive behaviors in pathology

Burton,

Longaretti,

Zlatanovic

et al. 2024

Front. Cell. Neurosci.

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Animals often behave repetitively and predictably. These repetitive behaviors can have a component that is learned and ingrained as habits, which can be evolutionarily advantageous as they reduce cognitive load and the expenditure of attentional resources. Repetitive behaviors can also be conscious and deliberate, and may occur in the absence of habit formation, typically when they are a feature of normal development in children, or neuropsychiatric disorders. They can be considered pathological when they interfere with social relationships and daily activities. For instance, people affected by obsessive-compulsive disorder, autism spectrum disorder, Huntington’s disease and Gilles de la Tourette syndrome can display a wide range of symptoms like compulsive, stereotyped and ritualistic behaviors. The striatum nucleus of the basal ganglia is proposed to act as a master regulator of these repetitive behaviors through its circuit connections with sensorimotor, associative, and limbic areas of the cortex. However, the precise mechanisms within the striatum, detailing its compartmental organization, cellular specificity, and the intricacies of its downstream connections, remain an area of active research. In this review, we summarize evidence across multiple scales, including circuit-level, cellular, and molecular dimensions, to elucidate the striatal mechanisms underpinning repetitive behaviors and offer perspectives on the implicated disorders. We consider the close relationship between behavioral output and transcriptional changes, and thereby structural and circuit alterations, including those occurring through epigenetic processes.

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Section: Beyond Genetics: Epigenetic Players In Pathological Repetiti...mentioning

confidence: 99%

Striatal insights: a cellular and molecular perspective on repetitive behaviors in pathology

Burton,

Longaretti,

Zlatanovic

et al. 2024

Front. Cell. Neurosci.

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“…Although numerous studies have documented brain changes after exposure to EE, the specific alterations responsible for EE’s attenuation of RRB are largely unknown [reviewed by 14]. Of the few studies that have examined the neural mechanisms behind EE’s reduction of stereotypies, most suggest that EE may prevent RRB development by increasing neurotrophin levels and synaptic plasticity within the indirect basal ganglia pathway and other basal ganglia regions [ 14 – 17 ]. For example, Lewis et al [ 15 ] observed that C58 mice, an animal model of RRB, raised in EE displayed greater dendritic spine density and increased expression of genes associated with synaptic plasticity in the subthalamic nucleus than standard-housed (SH) control animals.…”

Section: Introductionmentioning

confidence: 99%

“…RRB reduction in enriched environments has also been connected to increases in BDNF in the striatum of deer mice, as well as in the prefrontal cortex and hippocampus of Fmr1 knockout mice, a rodent model of fragile X syndrome [ 17 , 19 ]. However, the current understanding of how EE reduces RRB remains poorly understood and is limited by the relatively few brain regions and neurocellular mechanisms investigated to date [ 14 ].…”

Section: Introductionmentioning

confidence: 99%

Environmental enrichment reduces restricted repetitive behavior by altering gray matter microstructure

Farmer,

Febo,

Wilkes

et al. 2024

PLoS ONE

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Restricted, repetitive behaviors are common symptoms in neurodevelopmental disorders including autism spectrum disorder. Despite being associated with poor developmental outcomes, repetitive behaviors remain poorly understood and have limited treatment options. Environmental enrichment attenuates the development of repetitive behaviors, but the exact mechanisms remain obscure. Using the C58 mouse model of repetitive behavior, we performed diffusion tensor imaging to examine microstructural alterations associated with the development of repetitive behavior and its attenuation by environmental enrichment. The C57BL/6 mouse strain, which displays little or no repetitive behavior, was used as a control group. We observed widespread differences in diffusion metrics between C58 mice and C57BL/6 mice. In juvenile C58 mice, repetitive motor behavior displayed strong negative correlations with fractional anisotropy in multiple gray matter regions, whereas in young adult C58 mice, high repetitive motor behavior was most strongly associated with lower fractional anisotropy and higher radial diffusivity in the striatum. Environmental enrichment increased fractional anisotropy and axial diffusivity throughout gray matter regions in the brains of juvenile C58 mice and overlapped predominantly with cerebellar and sensory regions associated with repetitive behavior. Our results suggest environmental enrichment reduces repetitive behavior development by altering gray matter microstructure in the cerebellum, medial entorhinal cortex, and sensory processing regions in juvenile C58 mice. Under standard laboratory conditions, early pathology in these regions appears to contribute to later striatal and white matter dysfunction in adult C58 mice. Future studies should examine the role these regions play in the development of repetitive behavior and the relationship between sensory processing and cerebellar deficits and repetitive behavior.

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Oral stereotypic behaviors in farm animals and their causes

Li,

2024

Animal Research and One Health

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High stocking density and suboptimal conditions limit animal behaviors in modern livestock farming. This is particularly evident in captive animals, in which the motivation for foraging behavior is often thwarted. Oral stereotypic behaviors are common in farm animals. Ruminants (e.g., cattle and sheep) show oral stereotypic behaviors such as tongue‐rolling, self‐sucking, and inter‐sucking. Captive pigs exhibit oral stereotypic behaviors such as bar‐biting, sham‐chewing, and ear‐biting. Chickens peck at drinkers, feeders, and pens. Stereotypic behavior in livestock can be reduced by selecting a specific diet composition that prolongs their eating time and increases their satiety. Furthermore, reducing stocking density and enriching the farming environment encourage livestock to explore and reduce stereotypic behavior. It is important to note that stereotypic behavior is also influenced by organismal physiology. Stereotypic behavior was considered an indicator of poor animal welfare. However, recent research has revealed that animals engage in stereotypic behavior as a response to external stimuli, aiming to alleviate the negative impact of these stimuli on their well‐being. Animals that frequently show stereotypic behavior may have higher levels of stress. Certain stress indicators also affect the expression of stereotypic behavior, such as 5‐hydroxytryptamine and dopamine. Consequently, further investigation is necessary to understand how stereotypic behaviors affect the physiological state and metabolic processes of animals. This paper discusses the research progress on the oral stereotypic behaviors of farm animals. The objective is to establish a foundation for enhancing livestock feeding conditions and optimizing feeding practices, ultimately reducing stereotypic behaviors.

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Reduction of restricted repetitive behavior by environmental enrichment: Potential neurobiological mechanisms

Cited by 5 publications

References 267 publications

Striatal insights: a cellular and molecular perspective on repetitive behaviors in pathology

Striatal insights: a cellular and molecular perspective on repetitive behaviors in pathology

Environmental enrichment reduces restricted repetitive behavior by altering gray matter microstructure

Oral stereotypic behaviors in farm animals and their causes

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