scholarly journals Relief of Synaptic Depression Produces Long-Term Enhancement in Thalamocortical Networks

2006 ◽  
Vol 95 (4) ◽  
pp. 2479-2491 ◽  
Author(s):  
Akio Hirata ◽  
Manuel A. Castro-Alamancos

Thalamocortical synapses may be able to undergo activity-dependent long-term changes in efficacy, such as long-term potentiation. Indeed, studies conducted in vivo have found that theta-burst stimulation (TBS) of the thalamus induces a long-term enhancement (LTE) of field potential responses evoked in the neocortex of adult rodents. Because the thalamus and neocortex form a complex interconnected network that is highly active in vivo, it is possible that a change in thalamic excitability would be reflected in the neocortex. To test this possibility, we recorded from barrel neocortex and applied TBS to the thalamic radiation while the somatosensory thalamus was inactivated with muscimol. Thalamocortical LTE was absent when the thalamus was inactivated, suggesting that changes in thalamic excitability are involved. Single-unit recordings from thalamocortical cells revealed that TBS causes a significant reduction in the spontaneous firing rate of thalamocortical cells. Reducing the spontaneous firing of thalamocortical cells directly enhances the efficacy of the thalamocortical pathway because it relieves the tonic depression of the thalamocortical connection caused by thalamocortical activity. Because these changes in thalamic excitability are triggered by corticothalamic activity, this may be a useful top-down mechanism to regulate afferent sensory input to the neocortex during behavior as a function of experience.

1996 ◽  
Vol 75 (5) ◽  
pp. 1765-1778 ◽  
Author(s):  
G. Hess ◽  
C. D. Aizenman ◽  
J. P. Donoghue

1. The present studies investigated conditions for the induction of long-term potentiation (LTP) in the local horizontal pathways of layers II/III in the primary motor cortex (MI) of the adult rat. Field potential and intracellular recordings demonstrated synaptic interactions across the superficial layers within MI that could be enhanced transiently by focal application of the gamma-aminobuturic acid-A receptor antagonist bicuculline methiodide (Bic) at the recording site. 2. Field potentials evoked in the superficial MI horizontal pathways increased in amplitude after tetanizing, theta burst stimulation (TBS), but only when Bic was applied transiently at the recording site immediately before TBS. In the absence of Bic, TBS failed to produce long-lasting increases in horizontally evoked field responses. By contrast, TBS delivery during focal Bic application increased field potential amplitudes by 25-35% when measured 25-30 min after stimulation. The amount of potentiation was greater when two converging horizontal inputs were stimulated together but was not increased with higher intensity stimulation. Persistent effects of Bic application alone were evident. However, these effects were small unless Bic application continued until evoked field potential amplitude increase exceeded 200% of baseline. 3. The synaptic nature of field potential increases were confirmed using intracellular recordings of layer II/III neurons located near field potential electrodes. 4. LTP also could be induced without Bic application by cotetanization of vertical pathways simultaneously with horizontal activation. Vertical conditioning alone at 2 Hz, which affects inhibitory efficacy, was shown to transiently relieve depression of successive responses that ordinarily occurs during a burst of three horizontal stimuli. These results suggest that LTP of horizontal pathways may be regulated by spatiotemporal interactions between horizontal and vertical pathways. 5. Horizontal LTP was blocked reversibly by bath application of the N-methyl-D-aspartate (NMDA) antagonist 2-amino-5-phosphonovaleric acid, thereby implicating NMDA-receptor activation in LTP induction for these pathways. 6. The results confirm and extend our previous finding that the potential for activity-dependent modification of synaptic connections exists within the intrinsic horizontal connections of the superficial cortical layers. Synaptic modification across horizontally connected neurons appears to be regulated both by the arrangement of intrinsic circuitry and by the availability of mechanisms for modification at individual synapses. The properties of horizontal connections indicate that they form a spatial substrate and provide an activity-dependent mechanism for plasticity of adult cortical representations.


2003 ◽  
Vol 90 (5) ◽  
pp. 3547-3554 ◽  
Author(s):  
Binyamin Hochner ◽  
Euan R. Brown ◽  
Marina Langella ◽  
Tal Shomrat ◽  
Graziano Fiorito

Cellular mechanisms underlying learning and memory were investigated in the octopus using a brain slice preparation of the vertical lobe, an area of the octopus brain involved in learning and memory. Field potential recordings revealed long-term potentiation (LTP) of glutamatergic synaptic field potentials similar to that in vertebrates. These findings suggest that convergent evolution has led to the selection of similar activity-dependent synaptic processes that mediate complex forms of learning and memory in vertebrates and invertebrates.


2005 ◽  
Vol 93 (5) ◽  
pp. 3001-3006 ◽  
Author(s):  
Chaoying Li ◽  
Donna L. Maier ◽  
Ben Cross ◽  
James J. Doherty ◽  
Edward P. Christian

Although bilateral fimbria-fornix (FF) lesioning impairs spatial performance in animals, the literature is equivocal regarding its effects on hippocampal long-term potentiation (LTP). We examined the effects of FF lesioning on LTP induction in the Schaffer collateral–CA1 pathway in vivo with a protocol that delivered theta burst stimulation (TBS) trains of increasing length until a sufficient length was reached to induce LTP of the monosynaptic field excitatory postsynaptic potential (fEPSP). Experiments were performed in urethan-anesthetized Long-Evans rats either 4 or 12–16 wk after lesioning. In sham-operated controls, TBS trains ranging from 4 to 12 bursts were sufficient to induce robust LTP [170 ± 10% (mean ± SF) of control fEPSP slope; n = 8]. Four-week post -FF-lesioned animals also displayed clear LTP (167 ± 12% of control fEPSP slope; n = 4) that did not differ from the shams ( P > 0.05). In contrast, animals in the 12- to 16-wk post-lesion group showed a highly significant deficit in LTP induction (95 ± 3% of control fEPSP slope; n = 8; ≤28 burst TBS trains tested; P < 0.001 vs. sham- and 4-wk post-FF-lesion groups). Other quantitative measures of synaptic excitability (i.e., baseline fEPSP slope and input-output relation) did not differ between the sham- and the 12- to 16-wk post-FF-lesion groups. These results indicate that the FF lesion leads to an enduring defect in hippocampal long-term synaptic plasticity that may relate mechanistically to the cognitive deficits characterized in this model.


2013 ◽  
Vol 110 (9) ◽  
pp. 2027-2036 ◽  
Author(s):  
Sarah L. Hawes ◽  
Fawad Gillani ◽  
Rebekah C. Evans ◽  
Elizabeth A. Benkert ◽  
Kim T. Blackwell

Long-term potentiation (LTP) of excitatory afferents to the dorsal striatum likely occurs with learning to encode new skills and habits, yet corticostriatal LTP is challenging to evoke reliably in brain slice under physiological conditions. Here we test the hypothesis that stimulating striatal afferents with theta-burst timing, similar to recently reported in vivo temporal patterns corresponding to learning, evokes LTP. Recording from adult mouse brain slice extracellularly in 1 mM Mg2+, we find LTP in dorsomedial and dorsolateral striatum is preferentially evoked by certain theta-burst patterns. In particular, we demonstrate that greater LTP is produced using moderate intraburst and high theta-range frequencies, and that pauses separating bursts of stimuli are critical for LTP induction. By altering temporal pattern alone, we illustrate the importance of burst-patterning for LTP induction and demonstrate that corticostriatal long-term depression is evoked in the same preparation. In accord with prior studies, LTP is greatest in dorsomedial striatum and relies on N-methyl-d-aspartate receptors. We also demonstrate a requirement for both Gq- and Gs/olf-coupled pathways, as well as several kinases associated with memory storage: PKC, PKA, and ERK. Our data build on previous reports of activity-directed plasticity by identifying effective values for distinct temporal parameters in variants of theta-burst LTP induction paradigms. We conclude that those variants which best match reports of striatal activity during learning behavior are most successful in evoking dorsal striatal LTP in adult brain slice without altering artificial cerebrospinal fluid. Future application of this approach will enable diverse investigations of plasticity serving striatal-based learning.


1994 ◽  
Vol 71 (6) ◽  
pp. 2543-2547 ◽  
Author(s):  
G. Hess ◽  
J. P. Donoghue

1. Field potential recordings were used in rat motor cortex (MI) slice preparations to investigate the potential for activity-dependent modifications in the effectiveness of synaptic connections formed by layer II/III horizontal projections. 2. Long-term potentiation (LTP) of synaptic efficacy in MI horizontal pathways could be produced at short (0.5 mm) and long (1.0 mm) distances by theta burst stimulation (TBS), but only during local, transient application of the gamma-aminobutyric acid-A (GABAA) receptor antagonist, bicuculline methiodide (bic) immediately before TBS. Mean increase of the field potential amplitude measured 25–35 min after LTP induction ranged between 24 and 34%. Cooperative effects of conjoint TBS of two horizontal pathways on LTP induction were observed. 3. These results demonstrate that persistent changes in the functional interactions of cortical neurons can arise by activity-dependent mechanisms within the local horizontal connections and suggest a likely mechanism to recognize cortical representation patterns.


Hippocampus ◽  
2009 ◽  
Vol 19 (2) ◽  
pp. 130-140 ◽  
Author(s):  
Peter Jedlicka ◽  
Stephan W. Schwarzacher ◽  
Raphael Winkels ◽  
Friederike Kienzler ◽  
Michael Frotscher ◽  
...  

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