Learning-Dependent Dendritic Hypertrophy of Cerebellar Stellate Cells: Plasticity of Local Circuit Neurons

Kleim, Jeffrey A.; Swain, Rodney A.; Czerlanis, Cheryl; Kelly, Jennifer L.; Pipitone, Michelle A.; Greenough, William T.

doi:10.1006/nlme.1996.3742

Cited by 70 publications

(38 citation statements)

References 7 publications

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“…In particular, environmental enrichment, but not physical exercise on a treadmill, augmented the number of synapses per Purkinje cell in rats (Black, Isaacs, Anderson, Alcantara, & Greenough, 1990). Moreover, running a complex obstacle course, but not forced exercise on a treadmill, augmented the number of parallel fiber and climbing fiber synapses per Purkinje cell (Anderson, Alcantara, & Greenough, 1996) and the dendritic arborization of stellate cells (Kleim et al, 1997) in rats. The morphological effects of environmental enrichment are due to the different experiences of the animals.…”

Section: Discussionmentioning

confidence: 94%

“…In our own study of a genetically lesioned animal, the improvement of motor and water maze performance may have been caused by several factors, including (a) slowing of the degenerative process in the olivocerebellar system,(b) plasticity of the remaining cells in the olivocerebellar system, and (c) plasticity of extracerebellar regions taking over from lost cerebellar function. The experiments by Greenough and colleagues (Anderson et al, 1996;Black et al, 1990;Kleim et al, 1997) indicate that plastic changes occur in the cerebellum after exposure to environmental enrichment or to a complex obstacle course requiring sensorimotor learning. Similar processes may occur in cerebellar-damaged animals exposed to complex stimuli.…”

Section: Discussionmentioning

confidence: 99%

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Role of an enriched environment on the restoration of behavioral deficits in Lurcher mutant mice

et al. 1999

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Section: Discussionmentioning

confidence: 94%

Section: Discussionmentioning

confidence: 99%

Role of an enriched environment on the restoration of behavioral deficits in Lurcher mutant mice

et al. 1999

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“…Behavioral training can lead to an increase in cortical volume that is primarily attributable to dendritic Kleim et al, 1997b), glial (Sirevaag et al, 1991;Anderson et al, 1994), and vascular hypertrophy (Black et al, 1990). Because of this volume increase, measures of synapse density alone may not reveal changes in synapse number.…”

Section: Methodsmentioning

confidence: 99%

Cortical Synaptogenesis and Motor Map Reorganization Occur during Late, But Not Early, Phase of Motor Skill Learning

et al. 2004

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Extensive motor skill training induces reorganization of movement representations and synaptogenesis within adult motor cortex. Motor skill does not, however, develop uniformly across training sessions. It is characterized by an initial fast phase, followed by a later slow phase of learning. How cortical plasticity emerges during these phases is unknown. Here, we examine motor map topography and synapse number within rat motor cortex during the early and late phases of motor learning. Adult rats were placed in either a skilled or unskilled reaching condition (SRC and URC, respectively) for 3, 7, or 10 d. Intracortical microstimulation of layer V was used to determine the topography of forelimb movement representations within caudal forelimb area of motor cortex contralateral to the trained paw. Quantitative electron microscopy was used to measure the number of synapses per neuron within layer V. SRC animals showed significant increases in reaching accuracy after 3, 7, and 10 d of training. In comparison with URC animals, SRC animals had significantly larger distal forelimb representations after 10 d of training only. Furthermore, SRC animals had significantly more synapses per neuron than URC animals after 7 and 10 d of training. These results show that both motor map reorganization and synapse formation occur during the late phase of skill learning. Furthermore, synaptogenesis precedes map reorganization. We propose that motor map reorganization and synapse formation do not contribute to the initial acquisition of motor skills but represent the consolidation of motor skill that occurs during late stages of training.

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“…Behavioral training can lead to an increase in neuropil volume resulting from dendritic (13,14) and glial (15) hypertrophy. Because of this potential volume increase, measures of synapse density alone may not reveal changes in synapse number.…”

Section: Methodsmentioning

confidence: 99%

Synapse formation is associated with memory storage in the cerebellum

Kleim

Freeman

Bruneau

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

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164

124

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The idea that memory is encoded by means of synaptic growth is not new. However, this idea has been difficult to demonstrate in the mammalian brain because of both the complexity of mammalian behavior and the neural circuitry by which it is supported. Here we examine how eyeblink classical conditioning affects synapse number within the cerebellum; the brain region essential for long-term retention of the conditioned response. Results showed eyeblink-conditioned rats to have significantly more synapses per neuron within the cerebellar interpositus nucleus than both explicitly unpaired and untrained controls. Further analysis showed that the increase was caused by the addition of excitatory rather than inhibitory synapses. Thus, development of the conditioned eyeblink response is associated with a strengthening of inputs from precerebellar nuclei rather than from cerebellar cortex. These results demonstrate that the modifications of specific neural pathways by means of synaptogenesis contributes to formation of a specific memory within the mammalian brain.For every act of memory, every exercise of bodily aptitude, every habit, recollection, train of ideas, there is a specific neural grouping, or co-ordination, of sensations and movement, by virtue of specific growths in cell junctions (1).T he neural circuits critical for the acquisition and performance of the conditioned eyeblink response are localized to the cerebellum (2). Information regarding the unconditioned stimulus (US) and conditioned stimulus (CS) converge within both the cerebellar cortex and the interpositus nucleus. CS information is relayed via ponto-cerebellar projections, whereas US information is relayed via the olivo-cerebellar pathway (2, 3). Although the cerebellar cortex is involved in modulating some aspects of the conditioned response (CR) (4, 5), the interpositus nucleus is the critical brain structure supporting long-term retention of the CR (2, 6, 7). Neuronal activity within the interpositus nucleus is highly correlated with development of the CR (5, 7), and inactivation of the interpositus prevents both CR acquisition and performance (8).Although the locus of the memory trace is clear, the cellular mechanisms underlying the formation of the CS͞US association are poorly understood. Several mechanisms have been proposed, including increases in the intrinsic excitability of interpositus neurons and reduced inhibition via depression of Purkinje cell activity (9). The fact that inhibition of specific synaptic enzymes (10) and neurotransmitter receptors (11) within the interpositus nucleus impair learning suggests that changes in synaptic function are involved. Transient changes in enzyme or receptor activity, however, would seem incapable of supporting the long-term encoding of the CS͞US association. Recent work has shown that microinjections of a protein synthesis inhibitor into the interpositus nucleus impairs the acquisition but not the expression of the CR (12). This finding suggests that strengthening of the CS pathway may involve more...

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Learning-Dependent Dendritic Hypertrophy of Cerebellar Stellate Cells: Plasticity of Local Circuit Neurons

Cited by 70 publications

References 7 publications

Role of an enriched environment on the restoration of behavioral deficits in Lurcher mutant mice

Role of an enriched environment on the restoration of behavioral deficits in Lurcher mutant mice

Cortical Synaptogenesis and Motor Map Reorganization Occur during Late, But Not Early, Phase of Motor Skill Learning

Synapse formation is associated with memory storage in the cerebellum

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