Dorsal-ventral differentiation of short-term synaptic plasticity in rat CA1 hippocampal region

Papatheodoropoulos, Costas; Kostopoulos, George

doi:10.1016/s0304-3940(00)01084-3

Cited by 89 publications

(76 citation statements)

References 28 publications

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“…In contrast to the traditional PIFF studies 8,19,26 our results suggest that long intervals induce inhibition under continuous stimulation leading to a balance between excitation and inhibition. These results parallel findings by Fuhrman et al 13 indicating that depressing and excitatory synapses are optimized in the 0.5-5 Hz and 9-70 Hz frequency range, respectively.…”

Section: Discussioncontrasting

confidence: 99%

“…1,5,12,14,18 The weight of evidence for neural encoding points to the temporal relationship of the cell output (firing frequency, EPSP, Population Spike) to its presynaptic input (synaptic current evoked by the impingement of electrical impulses [action potentials] on the nerve terminal). 27,11,24,28,29 This relationship has been traditionally investigated using paired impulse stimulation of variable interimpulse intervals 8,19,26 and short impulse trains at fixed frequencies. 5,4,7,25 The paired impulse approach is based on two-impulse stimuli separated in time by a variable time interval while the short impulse train approach uses impulse sequences at fixed interimpulse intervals.…”

Section: Introductionmentioning

confidence: 99%

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Nonlinear Dynamic Model of CA1 Short-Term Plasticity using Random Impulse Train Stimulation

et al. 2007

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A comprehensive, quantitative description of the nonlinear dynamic characteristics of the short-term plasticity (STP) in the CA1 hippocampal region is presented. It is based on the Volterra-Poisson modeling approach using random impulse train (RIT) stimuli. In vitro hippocampal slice preparations were used from adult rats. RIT stimuli were applied at the Schaffer collaterals and population spike responses were recorded at the CA1 cell body layer. The computed STP descriptors that capture the nonlinear dynamics of the underlying STP mechanisms were the Volterra-Poisson kernels. The kernels quantified the presence of facilitatory and inhibitory STP behavior in magnitude and duration. A third order Volterra-Poisson STP model was introduced that accurately predicted in-sample and out-of-sample system responses. The proposed model could also accurately predict impulse pair and short impulse train system responses.

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Section: Discussioncontrasting

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Nonlinear Dynamic Model of CA1 Short-Term Plasticity using Random Impulse Train Stimulation

et al. 2007

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“…There were also very strong correlations between the responses of different slices from the same animal, suggesting that there are not significant differences in short-term plasticity in different parts of the hippocampus. All of our recordings were from dorsal hippocampus, however, and differences in paired-pulse facilitation between dorsal and ventral hippocampus have been reported (Papatheodoropoulos and Kostopoulos, 2000). In light of the wide variation of the properties of individual synapses, the strong similarity of the average properties of synapses suggests that there is a coordinated mechanism for regulating the population of synapses in the CA1 region as a whole.…”

Section: Discussionmentioning

confidence: 92%

Responses of excitatory hippocampal synapses to natural stimulus patterns reveal a decrease in short‐term facilitation and increase in short‐term depression during postnatal development

et al. 2005

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Schaffer collateral excitatory synapses onto CA1 pyramidal cells are subject to significant modulation by short-term plasticity. This presynaptic, history-dependent modulation of neurotransmitter release causes synaptic transmission to be sensitive to the frequency of the input. As a result, temporally irregular input patterns, such as those observed in vivo, produce synaptic responses over a very wide dynamic range that reflect a balance of short-term facilitation and short-term depression. The neonatal period is an important developmental period in the hippocampus, when functional representations of an animal's environment are being established through exploratory behavior. The strength of excitatory synapses and their modulation by short-term plasticity are critical to this process. One form of short-term plasticity, paired-pulse facilitation, has been shown to decrease as juvenile rats mature into young adults. However, little is known about the neonatal modulation of other forms of short-term plasticity, including the responses to temporally complex stimuli. We examined developmental modulation of the short-term dynamics of Schaffer collateral excitatory synapses onto CA1 pyramidal cells in acute hippocampal slices, using both constant frequency stimuli and natural stimulus patterns that were taken from in vivo recording of spike patterns of hippocampal cells. In response to constant frequency stimulation, synapses in slices from young adult rats (P28-P35) showed less short-term depression than did those in slices from juveniles (P12-P18). However, when the natural stimulus pattern (containing a wide mix of frequencies) was used, synapses from young adults instead showed more short-term depression and less short-term facilitation than did juveniles. Comparing the natural stimulus pattern responses with constant frequency stimulation of a similar frequency, we found that the average responses were similar in young adults (both showed modest depression). However, in juveniles, the natural pattern produced robust facilitation while constant frequency stimulation caused a large short-term depression. Our results reveal that there are developmental changes both in individual forms of short-term plasticity and in the relative balance between short-term facilitation and short-term depression that will alter the signal transfer characteristics of these synapses.

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“…Divergent topography of the HC afferents and massive systems of DG and CA3 associational projections between the transversal HC segments (Amaral and Witter, 1989;Ishizuka et al, 1990;Li et al, 1994;Burwell and Amaral, 1998;Dolorfo and Amaral, 1998;Burwell, 2000) may underlie two main clusters of learning-specific activity localized in the central parts of the dorsal and ventral HC; however, rostrocaudal differences in pattern and magnitude of Arc mRNA expression, place cell parameters (Jung et al, 1994;Poucet et al, 1994), and synaptic plasticity (Papatheodoropoulos and Kostopoulos, 2000) may underlie differences in mechanisms of the dorsal and ventral HC in spatial memory recall. Persistent activation of the dorsal but not ventral HC during both recent and remote memory tasks supports the hypothesis that the dorsal HC is more involved in spatial memory than the ventral HC (Moser et al, 1995;Moser and Moser, 1998b;Bannerman et al, 1999Bannerman et al, , 2004.…”

Section: Discussionmentioning

confidence: 99%

Topography of Arc/Arg3.1 mRNA Expression in the Dorsal and Ventral Hippocampus Induced by Recent and Remote Spatial Memory Recall: Dissociation of CA3 and CA1 Activation

Gusev¹,

Cui²,

Alkon³

et al. 2005

J. Neurosci.

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The understanding of the mechanisms of memory retrieval and its deficits, and the detection of memory underlying neuronal plasticity, is greatly impeded by a lack of precise knowledge of the brain circuitry that underlies the functions of memory. The specific roles of anatomically distinct hippocampal subdivisions in recent and long-term memory retention and recall are essentially unknown. To address these questions, we mapped the expression of Arc/Arg 3.1 mRNA, a neuronal activity marker, in memory retention at multiple rostrocaudal levels of the dentate gyrus, CA3, CA1, subiculum, and lateral and medial entorhinal cortices after a platform search in a water-maze spatial task at 24 h and 1 month compared with swim and naive controls. We found that the entorhinohippocampal neuronal activity underlying the recall of recent and remote spatial memory has an anatomically distributed and time-dependent organization throughout both the dorsal and ventral hippocampus that is subdivision specific. We found a dissociation in the activity of the entorhinal cortex, CA3, and CA1 over a period of memory consolidation. Although CA3, the dorsal hippocampus, and the entorhinal cortex demonstrated the most persistent learning-specific signal during both recent and long-term memory recall, CA1 and the ventral hippocampus displayed the most dramatic signal decline. We determined the coordinates of activity clusters in the hippocampal subdivisions during the platform search and their dynamics over time. Our mapping data suggest that although the level of corticohippocampal interaction is similar during the retrieval of recent and remote spatial memories, the mnemonic function of the hippocampus may have changed, and the activity underlying remote spatial memory could be anatomically segregated within hippocampal subdivisions in small segments.

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Dorsal-ventral differentiation of short-term synaptic plasticity in rat CA1 hippocampal region

Cited by 89 publications

References 28 publications

Nonlinear Dynamic Model of CA1 Short-Term Plasticity using Random Impulse Train Stimulation

Nonlinear Dynamic Model of CA1 Short-Term Plasticity using Random Impulse Train Stimulation

Responses of excitatory hippocampal synapses to natural stimulus patterns reveal a decrease in short‐term facilitation and increase in short‐term depression during postnatal development

Topography of Arc/Arg3.1 mRNA Expression in the Dorsal and Ventral Hippocampus Induced by Recent and Remote Spatial Memory Recall: Dissociation of CA3 and CA1 Activation

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