The growth of the dendritic trees of Purkinje cells in the cerebellum of the rat

Berry, Martin; Bradley, Philip

doi:10.1016/0006-8993(76)90331-0

Cited by 167 publications

(79 citation statements)

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“…At this age, the rat cerebellum is relatively immature (15,19,20). Nevertheless, immature cerebellar neurons are capable of synaptic plasticity and increased intrinsic excitability in vitro (9)(10)(11)(12).…”

Section: Discussionmentioning

confidence: 99%

Eyeblink conditioning in 12-day-old rats using pontine stimulation as the conditioned stimulus

Campolattaro

Freeman

2008

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

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A fundamental issue in developmental science is whether ontogenetic changes in memory are caused by the development of cellular plasticity mechanisms within the brain's memory systems or maturation of sensory inputs to the memory systems. Here, we provide evidence that the development of eyeblink conditioning, a form of associative learning that depends on the cerebellum, is driven by the development of sensory inputs rather than the development of neuronal plasticity mechanisms. We find that rats as young as 12 days old show associative eyeblink conditioning when pontine stimulation is used in place of an external (e.g., a tone) conditioned stimulus. Eyeblink-conditioned responses established with pontine stimulation in 12-day-old rats were reversibly abolished by an infusion of muscimol into the cerebellar interpositus nucleus. The findings suggest that cerebellar neurons are capable of supporting associative learning-specific plasticity in vivo in very immature animals if given sufficient afferent stimulation.cerebellum ͉ eyelid conditioning ͉ learning ͉ memory I t seems reasonable to assume that the development of memory is caused by the maturation of synaptic plasticity mechanisms within the memory systems of the brain. For example, the development of declarative memory could be related to the development of long-term potentiation in the medial temporal lobe, and conditioning of discrete movements could be related to the development of cerebellar long-term depression. On the other hand, it is possible that the cerebellum and hippocampus are capable of establishing learning-related synaptic plasticity in young animals but simply do not receive sufficient sensory input during learning. We evaluated these possibilities by examining the effects of electrically stimulating a sensory input pathway to the cerebellum on eyeblink conditioning in rats that are too immature to show conditioning with external sensory stimuli.Eyeblink conditioning, a type of associative learning, typically involves the presentation of a conditioned stimulus (CS) that does not produce a blink reflex before training (e.g., a tone or light) followed by an unconditioned stimulus (US) that reliably elicits the blink reflex. Repeated presentations of the CS and US result in the acquisition of a conditioned response (CR) that precedes the onset of the US. Eyeblink conditioning emerges ontogenetically between postnatal days 17 and 24 in rats (1). Developmental changes in human eyeblink conditioning have also been documented (2).The cerebellar hemisphere that is ipsilateral to the conditioned eye is essential for acquisition and retention of eyeblink conditioning in adult and infant animals (3, 4). Neurons within the pontine nuclei (PN) are part of the mossy fiber pathway that sends CS information to the cerebellum (5-7). Cerebellar neurons are thought to develop learning-specific changes in synaptic efficacy to CS inputs, which underlies memory for the CS-US association (8). Using either cerebellar slices or cultured neurons from rodents, many ...

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Section: Discussionmentioning

confidence: 99%

Eyeblink conditioning in 12-day-old rats using pontine stimulation as the conditioned stimulus

Campolattaro

Freeman

2008

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

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“…In sagittal profile, rat Purkinje cells have three to seven parallel fiber synaptic spines per m 2 cross section of dendritic arbor (41,42,45), assuming 0.32-0.42 m of dendrite per m 2 of arbor (45). A stimulating pipette will therefore be within a 60-m radius of 40,000-80,000 spines, if this pipette is in the center of the arbor, and somewhat fewer than half this number if the pipette is at the edge of the arbor.…”

Section: Discussionmentioning

confidence: 99%

Quantification of spread of cerebellar long-term depression with chemical two-photon uncaging of glutamate

Wang

Khiroug

Augustine

2000

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

100

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Localized, chemical two-photon photolysis of caged glutamate was used to map the changes in ␣-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid-type glutamate receptors caused by long-term synaptic depression (LTD) in cerebellar Purkinje cells. LTD produced by pairing parallel fiber activity with depolarization was accompanied by a decline in the response of Purkinje cells to uncaged glutamate that accounted for both the time course and magnitude of LTD. This depression of glutamate responses was observed not only at the site of parallel fiber stimulation but also at more distant sites. The amount of LTD decreased with distance and was halfmaximal 50 m away from the site of parallel fiber activity. Estimation of the number of parallel fibers active during LTD induction indicates that LTD modified glutamate receptors not only at active synapses but also at 600 times as many inactive synapses on a single Purkinje cell. Therefore, both active and inactive parallel fiber synapses can undergo changes at a postsynaptic locus as a result of associative pre-and postsynaptic activity.synaptic plasticity ͉ glutamate receptors ͉ calcium ͉ flash photolysis U se-dependent synaptic plasticity has been proposed to serve as a mechanism for storing information in the brain (1-3). One fundamental question regarding this hypothesis is the location of the synapses that are modified. Although it has been widely assumed that individual synapses represent storage sites (2), there are now several cases where plasticity appears to extend beyond individual synapses (4-8).Here we examine the spatial range of cerebellar long-term depression (LTD), a form of plasticity that has been implicated in motor learning (9-12). LTD is associative because it arises from the coincident activity of parallel fiber (PF) and climbing fiber synapses onto Purkinje cells (9,(13)(14)(15)). The precise range of action of LTD is not yet clear. Although LTD is thought to occur only at PFs that are active during LTD induction (16-18), a nonassociative form of LTD has been reported to spread more than 100 m (18). Two unique features make it possible for us to define the range of cerebellar LTD. (i) The organized geometry of PF axons allows selective activation of PF synapses in a defined area. (ii) LTD is thought to arise from a change in the sensitivity of postsynaptic, ␣-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)-type glutamate receptors (13,19,20), allowing these receptors to serve as a read-out for the spread of LTD. By using chemical two-photon uncaging of glutamate (21) to monitor the properties of AMPA receptors, we have found that LTD affects glutamate receptors over a range of up to 60 m. Because the region of PF activation is Ϸ10 m, these results show that LTD stores information both at active PF synapses and at nearby inactive PF synapses. This spread of LTD requires a chemical signal that can move from active to inactive PF synapses on the same Purkinje cell. Materials and MethodsPatch Clamp Recordings. Whole-cell patch clamp recordings...

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“…The mean(sd) value at day 30 compares well with the 1 month outcome of 455(42) from the work of Woldenberg et al, (1993). These five data points from Berry and Bradley (1976) are drawn in Figure 7E using a linear time scale versus time-bin, such that time-bin N ϭ 500 corresponds to real time T ϭ 30 days. For the 30 days age group the optimal parameter values were found to be (B, E) ϭ (40, 0.486), and the growth curve for these parameter values has also been drawn in Figure 7E.…”

Section: Unequal Time-bin Durations (Best-model)mentioning

confidence: 97%

“…The bin durations, determined by the slope of the curve, increase with time-bin number between the 2nd and 5th data point. No assumptions have been made concerning the time of onset Berry and Bradley (1976), by using a linear time scale with bin 500 corresponding with age of 30 days. The bin numbers at which the growth curve attains similar mean values as the data points are plotted in F against the age of the groups.…”

Section: Unequal Time-bin Durations (Best-model)mentioning

confidence: 99%

Natural variability in the number of dendritic segments: Model-based inferences about branching during neurite outgrowth

1997

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A study was made of the possible basis for naturally occurring variations in the number of segments in individual dendritic trees. Distributions of the number of terminal segments have been studied in dendrites from rat, cat, and frog motoneurons, basal dendrites from rat visual cortex pyramidal and non-pyramidal neurons, in rat cerebellar Purkinje cell dendritic trees, and in human hippocampal dentate granule cells. By means of a mathematical model for dendritic branching, it was shown that the variation in the number of dendritic segments can be accounted for by assuming that new branches during neurite outgrowth are formed randomly at terminal segments. The observed terminal segment number distributions could be closely approximated by additionally assuming that branching probabilities decline with increasing number of terminal segments in growing dendrites. The pyramidal neuron group differed significantly from the other neuron groups in such a way as to suggest that this decline is stronger than in the dendrites of other types of neurons. By using literature data on the mean number of terminal segments in rat cerebellar Purkinje cells, measured at different times during early development, an estimate could be obtained of the time-course of the branching probabilities. The branching probability of a terminal segment was found to be in the order of 0.002 per hour in the first 4 weeks postnatal with a 5-fold transient increase in the second week.

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The growth of the dendritic trees of Purkinje cells in the cerebellum of the rat

Cited by 167 publications

References 50 publications

Eyeblink conditioning in 12-day-old rats using pontine stimulation as the conditioned stimulus

Eyeblink conditioning in 12-day-old rats using pontine stimulation as the conditioned stimulus

Quantification of spread of cerebellar long-term depression with chemical two-photon uncaging of glutamate

Natural variability in the number of dendritic segments: Model-based inferences about branching during neurite outgrowth

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