Environmental conditions modulate degeneration and new dendrite growth in cerebellum of senescent rats

doi:10.1016/0006-8993(86)91437-X

Brain Research

Volume 380, Issue 1, 13 August 1986, Pages 136-143

https://doi.org/10.1016/0006-8993(86)91437-X Get rights and content

Abstract

Spiny branchlets of cerebellar Purkinje neurons, thought to be sites of synaptic efficacy change during motor learning, degenerate during aging. To examine effects of behavioral experience on degeneration, Purkinje neurons were studied in aging rats housed for 4.5 months either under complex environment conditions promoting sensory-motor activity or in pairs in standard cages. Their data were compared with those of a baseline group of rats from standard cages sacrificed at the age of onset of differential housing for the older groups. Rats housed in the complex environment had more spiny branchlets than the other groups, indicating that new branches had formed. There was a net loss of summed total spiny branchlet material per Purkinje cell in both the laboratory cage and complex environment older groups, although the complex environment group had more spiny branchlet per cell than the laboratory cage group. Thus, dendrite loss in the aging cerebellum can be partly offset by appropriate experience. There was no net loss of Purkinje cell main branch dendrite with aging, as indicated by previous studies, and there was no effect of differential housing upon main branches in the older groups. However, changes in the pattern of branching in the main dendritic field suggested that this region undergoes reorganization with aging.

References (55)

AlbusJ.S.
A theory of cerebellar function
Math. Biosci.
(1971)
ChangF.-L. et al.
Lateralized effects of monocular training on dendritic branching in adult split-brain rats
Brain Research
(1982)
ChangF.-L. et al.
Transient and enduring morphological correlates of synaptic activity and efficacy change in the rat hippocampal slice
Brain Research
(1984)
ConnorJ.R. et al.
Dendritic length in aged rats' occipital cortex: an environmentally induced response
Exp. Neurol.
(1981)
DeVoogdT.J. et al.
Distortions induced in neuronal quantification by camera lucida analysis: comparisons using a semiautomated data acquisition system
J. Neurosci. Meth.
(1981)
DiamondM.C. et al.
Plasticity in the 904-day-old male rat cerebral cortex
Exp. Neurol.
(1985)
DustmanR.E. et al.
Aerobic exercise training and improved neuropsychological function of older individuals
Neurobiol. Aging
(1984)
EcclesJ.C.
An instruction-selection theory of learning in the cerebellar cortex
Brain Research
(1977)
GilbertP.F.C. et al.
Purkinje cell activity during motor learning
Brain Research
(1977)
GlaserE.M. et al.
Analysis of thick brain sections by obverse-reverse computer microscopy: application of a new, high clarity Golgi-Nissl stain
J. Neurosci. Meth.
(1981)

GreenE.J. et al.

Effects of complex or isolated environments on cortical dendrites of middle-aged rats

Brain Research

(1983)

GreenoughW.T. et al.

Experience and the changing brain

GreenoughW.T. et al.

Effects of unilateral and bilateral training in a reaching task on dendritic branching of neurons in the rat motor-sensory forelimb cortex

Behav. Neural Biol.

(1985)

GreenoughW.T. et al.

Pattern of dendritic branching in occipital cortex of rats reared in complex environments

Exp. Neurol.

(1973)

HuntleyM.J. et al.

Effects of environmental complexity and locomotor activity on brain weight in the rat

Physiol. Behav.

(1972)

JuraskaJ.M. et al.

Plasticity in adult rat visual cortex: an examination of several cell populations after differential rearing

Behav. Neural Biol.

(1980)

McCormickD.A. et al.

Superior cerebellar peduncle lesions selectively abolish the ipsilateral classically conditioned nictitating membrane/eyelid response of the rabbit

Brain Research

(1982)

RogersJ. et al.

Senescent changes in a neurobiological model system: cerebellar Purkinje cell electrophysiology and correlative anatomy

Neurobiol. Aging

(1980)

RogersJ. et al.

Senescent microstructural changes in rat cerebellum

Brain Research

(1984)

ScheibelM.E. et al.

Progressive dendritic changes in the aging human limbic system

Exp. Neurol.

(1976)

TurnerA.M. et al.

Differential rearing effects on rat visual cortex synapses. I. Synaptic and neuronal density and synapses per neuron

Brain Research

(1985)

UylingsH.B.M. et al.

Environmental influences on neocortex in later life

YeoC.H. et al.

Discrete lesions of the cerebellar cortex abolish the classically conditioned nictitating membrane response of the rabbit

Behav. Brain Res.

(1984)

BirrenJ.E.

Psychophysiology and speed of response

Am. Psychol.

(1974)

BondareffW. et al.

Loss of synapses in the dentate gyrus of the senescent rat

Am. J. Anat.

(1976)

BrodyH.

Aging of the vertebrate brain

BuellS.J. et al.

Dendritic growth in the aged human brain and failure of growth in senile dementia

Science

(1979)

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^*: Present address: Neuroscience Laboratory Building, 1103 E. Huron, Ann Arbor, MI 48104, U.S.A.

^**: Present address: University of Illinois Medical Center, 1853 W. Polk, Rm. 112, Chicago, IL 60612, U.S.A.

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Environmental conditions modulate degeneration and new dendrite growth in cerebellum of senescent rats

Abstract

Math. Biosci.

Brain Research

Brain Research

Exp. Neurol.

J. Neurosci. Meth.

Exp. Neurol.

Neurobiol. Aging

Brain Research

Brain Research

J. Neurosci. Meth.

Brain Research

Behav. Neural Biol.

Exp. Neurol.

Physiol. Behav.

Behav. Neural Biol.

Brain Research

Neurobiol. Aging

Brain Research

Exp. Neurol.

Brain Research

Behav. Brain Res.

Psychophysiology and speed of response

Am. Psychol.

Loss of synapses in the dentate gyrus of the senescent rat

Am. J. Anat.

Aging of the vertebrate brain

Dendritic growth in the aged human brain and failure of growth in senile dementia

Science