A Learning and Memory Area in the Octopus Brain Manifests a Vertebrate-Like Long-Term Potentiation

2003 ◽  
Vol 90 (5) ◽  
pp. 3547-3554 ◽  
Author(s):  
Binyamin Hochner ◽  
Euan R. Brown ◽  
Marina Langella ◽  
Tal Shomrat ◽  
Graziano Fiorito
Keyword(s):  
Learning And Memory ◽  
Field Potential ◽  
Long Term Potentiation ◽  
Cellular Mechanisms ◽  
Term Potentiation ◽  
Memory Area ◽  
Complex Forms ◽  
Activity Dependent ◽  
Brain Slice Preparation

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.

Learning and Memory

The Neuron ◽  
2015 ◽  
pp. 489-528
Author(s):  
Irwin B. Levitan ◽  
Leonard K. Kaczmarek
Keyword(s):  
Learning And Memory ◽  
Molecular Mechanisms ◽  
Long Term Potentiation ◽  
Memory Formation ◽  
Spike Timing ◽  
Cellular Mechanisms ◽  
Long Term Depression ◽  
Nervous Systems ◽  
Term Potentiation

Psychologists have described different kinds of learning and memory, and there is an ongoing search for the physical basis of these distinctions and for the cellular and molecular mechanisms responsible. Because of the complexity of most nervous systems, the search has focused to a large extent on animals with relatively simple nervous systems and on reduced preparations. Common themes have emerged, such as the requirement for signaling pathways linked to calcium and cyclic AMP, and the fact that pathways used in normal development continue to be used for plasticity in adults. At the same time, it is clear that there is an enormous diversity of cellular mechanisms that contribute to short-term and long-term phases of memory formation. These include long-term potentiation (LTP), long-term depression (LTD), spike-timing dependent plasticity, synaptic tagging, and synaptic scaling. Each type of synaptic connection has its own personality such that, in response to a particular pattern of stimulation, one synapse may increase its postsynaptic receptors while another may expand its presynaptic terminals.

Conditions for the induction of long-term potentiation in layer II/III horizontal connections of the rat motor cortex

1996 ◽  
Vol 75 (5) ◽  
pp. 1765-1778 ◽  
Author(s):  
G. Hess ◽  
C. D. Aizenman ◽  
J. P. Donoghue
Keyword(s):  
Motor Cortex ◽  
Field Potential ◽  
Long Term Potentiation ◽  
Receptor Activation ◽  
Intracellular Recordings ◽  
Recording Site ◽  
Horizontal Connections ◽  
Term Potentiation ◽  
Activity Dependent

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.

scholarly journals Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory

2003 ◽  
Vol 358 (1432) ◽  
pp. 773-786 ◽  
Author(s):  
R. G. M. Morris ◽  
E. I. Moser ◽  
G. Riedel ◽  
S. J. Martin ◽  
J. Sandin ◽  
...  
Keyword(s):  
Synaptic Plasticity ◽  
Long Term Potentiation ◽  
Cellular Mechanisms ◽  
Memory Processing ◽  
Functional Studies ◽  
Term Potentiation ◽  
Intermediate Storage ◽  
Activity Dependent

The hypothesis that synaptic plasticity is a critical component of the neural mechanisms underlying learning and memory is now widely accepted. In this article, we begin by outlining four criteria for evaluating the ‘synaptic plasticity and memory (SPM)’ hypothesis. We then attempt to lay the foundations for a specific neurobiological theory of hippocampal (HPC) function in which activity-dependent synaptic plasticity, such as long-term potentiation (LTP), plays a key part in the forms of memory mediated by this brain structure. HPC memory can, like other forms of memory, be divided into four processes: encoding, storage, consolidation and retrieval. We argue that synaptic plasticity is critical for the encoding and intermediate storage of memory traces that are automatically recorded in the hippocampus. These traces decay, but are sometimes retained by a process of cellular consolidation. However, we also argue that HPC synaptic plasticity is not involved in memory retrieval, and is unlikely to be involved in systems-level consolidation that depends on HPC-neocortical interactions, although neocortical synaptic plasticity does play a part. The information that has emerged from the worldwide focus on the mechanisms of induction and expression of plasticity at individual synapses has been very valuable in functional studies. Progress towards a comprehensive understanding of memory processing will also depend on the analysis of these synaptic changes within the context of a wider range of systems-level and cellular mechanisms of neuronal transmission and plasticity.

Stereotypical changes in the pattern and duration of long-term potentiation expressed at postnatal days 11 and 15 in the rat hippocampus

1993 ◽  
Vol 70 (4) ◽  
pp. 1412-1419 ◽  
Author(s):  
P. S. Jackson ◽  
T. Suppes ◽  
K. M. Harris
Keyword(s):  
Learning And Memory ◽  
Long Term Potentiation ◽  
Rat Hippocampus ◽  
Developmental Changes ◽  
Cellular Mechanisms ◽  
Adult Rat ◽  
Term Potentiation ◽  
Hippocampal Area ◽  
Pharmacological Manipulations

1. Extracellular recordings from hippocampal area CA1 lasting 2-8 h posttetanus were used to evaluate the duration of long-term potentiation (LTP) at two key developmental ages. 2. At day 11 LTP consistently endured for approximately 1 h before declining to baseline by 2.5 h posttetanus. The response could then be repotentiated, and in some cases, the repotentiation lasted longer than the original potentiation. 3. At day 15 two patterns of potentiation were observed. The first pattern was similar to that observed at day 11 in that the potentiation did not persist; however, it did endure for approximately 2-2.5 h before declining to baseline by 4 h posttetanus. In the second pattern the potentiation persisted indefinitely; these responses were monitored for 6-8 h posttetanus. 4. These patterns are similar to the temporal phases of LTP that have been revealed in adult rat hippocampus through pharmacological manipulations. They may reflect developmental changes during which the different cellular mechanisms underlying LTP become sequentially activated. 5. These findings are important for several reasons. First, because the different temporal phases of LTP seem to be added stepwise during development, animals of different ages could be used explicitly to elucidate the underlying cellular mechanisms of these phases in LTP. Second, because LTP is a candidate mechanism for some forms of learning and memory, these results have implications for sequential steps in the ontogeny of learning and memory. Finally, because studies of LTP have used animals of widely varying ages, including these two ages, it is important to consider whether differences in the developmental properties of LTP could influence experimental observations.

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
Keyword(s):  
Field Potential ◽  
Long Term Potentiation ◽  
Spontaneous Firing ◽  
Highly Active ◽  
Term Potentiation ◽  
Activity Dependent ◽  
Spontaneous Firing Rate ◽  
Theta Burst

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.

Long-term potentiation of horizontal connections provides a mechanism to reorganize cortical motor maps

1994 ◽  
Vol 71 (6) ◽  
pp. 2543-2547 ◽  
Author(s):  
G. Hess ◽  
J. P. Donoghue
Keyword(s):  
Cortical Neurons ◽  
Field Potential ◽  
Long Term Potentiation ◽  
Gamma Aminobutyric Acid ◽  
Cooperative Effects ◽  
Horizontal Connections ◽  
Term Potentiation ◽  
Gabaa Receptor Antagonist ◽  
Activity Dependent

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.

Arousing the LTP and learning debate

1997 ◽  
Vol 20 (4) ◽  
pp. 622-623 ◽  
Author(s):  
Stephen Maren
Keyword(s):  
Learning And Memory ◽  
Long Term Potentiation ◽  
Term Potentiation ◽  
Arousal Mechanism

Shors & Matzel provide compelling arguments against a role for hippocampal long-term potentiation (LTP) in mammalian learning and memory. As an alternative, they suggest that LTP is an arousal mechanism. I will argue that this view is not a satisfactory alternative to current conceptions of LTP function.

The Vertical Lobe of Cephalopods

2017 ◽  
pp. 558-574 ◽  
Author(s):  
Ana Turchetti-Maia ◽  
Tal Shomrat ◽  
Binyamin Hochner
Keyword(s):  
Complex Networks ◽  
Long Term Potentiation ◽  
Learning Networks ◽  
Neuronal Circuitry ◽  
Cellular Processes ◽  
Term Potentiation ◽  
Matrix Organization ◽  
Activity Dependent ◽  
Similar Organization

We show that the cephalopod vertical lobe (VL) is a promising system for assessing the function and organization of the neuronal circuitry mediating complex learning and memory behavior. Studies in octopus and cuttlefish VL networks suggest an independent evolutionary convergence into a matrix organization of a divergence-convergence (“fan-out fan-in”) network with activity-dependent long-term plasticity mechanisms. These studies also show, however, that the properties of the neurons, neurotransmitters, neuromodulators, and mechanisms of induction and maintenance of long-term potentiation are different from those evolved in vertebrates and other invertebrates, and even highly variable among these two cephalopod species. This suggests that complex networks may have evolved independently multiple times and that, even though memory and learning networks share similar organization and cellular processes, there are many molecular ways of constructing them.

Dopamine D-1/D-5 Receptor Activation Is Required for Long-Term Potentiation in the Rat Neostriatum In Vitro

2001 ◽  
Vol 85 (1) ◽  
pp. 117-124 ◽  
Author(s):  
J.N.D. Kerr ◽  
J. R. Wickens
Keyword(s):  
Receptor Antagonist ◽  
Learning And Memory ◽  
Sch 23390 ◽  
Long Term Potentiation ◽  
Receptor Activation ◽  
Striatal Neurons ◽  
Theoretical Understanding ◽  
Endogenous Dopamine ◽  
Term Potentiation

Dopamine and glutamate are key neurotransmitters involved in learning and memory mechanisms of the brain. These two neurotransmitter systems converge on nerve cells in the neostriatum. Dopamine modulation of activity-dependent plasticity at glutamatergic corticostriatal synapses has been proposed as a cellular mechanism for learning in the neostriatum. The present research investigated the role of specific subtypes of dopamine receptors in long-term potentiation (LTP) in the corticostriatal pathway, using intracellular recording from striatal neurons in a corticostriatal slice preparation. In agreement with previous reports, LTP could be induced reliably under Mg2+-free conditions. This Mg2+-free LTP was blocked by dopamine depletion and by the dopamine D-1/D-5 receptor antagonist SCH 23390 but was not blocked by the dopamine D-2 receptor antagonist remoxipride or the GABAA antagonist picrotoxin. In dopamine-depleted slices, the ability to induce LTP could be restored by bath application of the dopamine D-1/D-5 receptor agonist, SKF 38393. These results show that activation of dopamine D-1/D-5 receptors by either endogenous dopamine or exogenous dopamine agonists is a requirement for the induction of LTP in the corticostriatal pathway. These findings have significance for current understanding of learning and memory mechanisms of the neostriatum and for theoretical understanding of the mechanism of action of drugs used in the treatment of psychotic illnesses and Parkinson's disease.

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