The relation between extent of dorsal hippocampal kindling and delayed-match-to-place performance in the Morris water maze

Hannesson, Darren K.; Wallace, Amy E.; Pollock, Michael S.; Corley, Shannon M.; Mohapel, Paul; Corcoran, Michael E.

doi:10.1016/j.eplepsyres.2004.01.004

Cited by 10 publications

(8 citation statements)

References 30 publications

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“…Deficits in performance in the Morris water maze have been regarded as indications of hippocampal dysfunction underlying spatial memory acquisition and retention (Morris, et al 1982; Morris 1984; Hannesson, et al 2001; Hannesson, et al 2004; Sayin, et al 2004). The observed differences in PPKS vs. PPKR and outbred SD rats implicating an underlying hippocampal abnormality is potentially of interest as the PPKS strain was selected on the basis of rapid kindling rates in response to repeated stimulation of the perforant path, the major input to the hippocampus.…”

Section: Discussionmentioning

confidence: 99%

Distinct behavioral phenotypes in novel “fast” kindling-susceptible and “slow” kindling-resistant rat strains selected by stimulation of the hippocampal perforant path

Langberg

Dashek

Mulvey

et al. 2016

Neurobiology of Disease

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Kindling is a phenomenon of activity-dependent neural circuit plasticity induced by repeated seizures that results in progressive permanent increases in susceptibility to epilepsy. As the permanent structural and functional modifications induced by kindling include a diverse range of molecular, cellular, and functional alterations in neural circuits, it is of interest to determine if genetic background associated with seizure-induced plasticity might also influence plasticity in neural circuitry underlying other behaviors. Outbred Sprague-Dawley (SD) rats were selected and bred for ~15 generations for “fast’ or “slow” rates of kindling development in response to stimulation of the perforant path input to the hippocampus. After 7-8 generations of selection and breeding, consistent phenotypes of “fast” and “slow” kindling rates were observed. By the 15th generation “fast” kindling rats referred to as Perforant Path Kindling Susceptible (PPKS) rats demonstrated a kindling rate of 10.7 ± 1.1 afterdischarges (ADs) to the milestone of the first secondary generalized (Class V) seizure, which differed significantly from “slow” kindling Perforant Path Kindling Resistant (PPKR) rats requiring 25.5 ± 2.0 ADs, and outbred SD rats requiring 16.8 ± 2.5 ADs (p < 0.001, ANOVA). Seizure-naïve adult PPKS and PPKR rats from offspring of this generation and age-matched adult outbred SD rats were compared in validated behavioral measures including the open field test as a measure of exploratory activity, the Morris water maze as a measure of hippocampal spatial memory, and fear conditioning as a behavioral paradigm of associative fear learning. The PPKS (“fast” kindling) strain with increased susceptibility to seizure-induced plasticity demonstrated statistically significant increases in motor exploratory activity in the open field test and reduced spatial learning the Morris water maze, but demonstrated normal fear conditioned learning comparable to outbred SD rats and the “slow” kindling-resistant PPKR strain. These results confirm that selection and breeding on the basis of responses to repeated pathway activation by stimulation can produce enduring modification of genetic background influencing behavior. These observations also suggest that genetic background underlying susceptibility or resistance to seizure-induced plasticity in hippocampal circuitry also differentially influences distinct behaviors and learning that depend on circuitry activated by the kindling selection process, and may have implications for associations between epilepsy, comorbid behavioral conditions, and cognition.

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Section: Discussionmentioning

confidence: 99%

Distinct behavioral phenotypes in novel “fast” kindling-susceptible and “slow” kindling-resistant rat strains selected by stimulation of the hippocampal perforant path

Langberg

Dashek

Mulvey

et al. 2016

Neurobiology of Disease

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“…Previous work in the medial prefrontal cortex (mPFC) of rodents suggests that this region is important for learning associations between temporally discontiguous events (Gilmartin and Helmstetter, 2010;Gilmartin et al, 2013;Runyan et al, 2004;Takehara-Nishiuchi et al, 2005). The mPFC has also been implicated in other behaviors that rely on the temporal organization of information, including learning stimulus sequences (Barker et al, 2007;Devito and Eichenbaum, 2011;Hannesson et al, 2004a;Mitchell and Laiacona, 1998) and remembering which locations in an environment have been previously visited (Chiba et al, 1997;Hannesson et al, 2004b). At the physiological level, mPFC neurons have been found to sustain firing rates over short temporal intervals (Hattori et al, 2014;Rainer et al, 1999;Siegel, 2014;Takehara-Nishiuchi and McNaughton, 2008).…”

Section: Introductionmentioning

confidence: 97%

Enhancing Prefrontal Neuron Activity Enables Associative Learning of Temporally Disparate Events

Volle

Sun

et al. 2016

Cell Reports

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The ability to link events that are separated in time is important for extracting meaning from experiences and guiding behavior in the future. This ability likely requires the brain to continue representing events even after they have passed, a process that may involve the prefrontal cortex and takes the form of sustained, event-specific neuron activity. Here, we show that experimentally increasing the activity of excitatory neurons in the medial prefrontal cortex (mPFC) enables rats to associate two stimuli separated by a 750-ms long temporal gap. Learning is accompanied by ramping increases in prefrontal theta and beta rhythms during the interval between stimuli. This ramping activity predicts memory-related behavioral responses on a trial-by-trial basis but is not correlated with the same muscular activity during non-memory conditions. Thus, the enhancement of prefrontal neuron excitability extends the time course of evoked prefrontal network activation and facilitates the formation of associations of temporally disparate, but correlated, events.

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“…Because of the prominent role played by the hippocampus in both TLE (Engel, 1998) and memory (Squire, 1992; Aggleton & Brown, 1999), and observations that the changes in memory seen in TLE may correlate with structural or functional changes in the hippocampus (Paradiso et al ., 1995; Hermann et al ., 1997; Martin et al ., 1999; Sawrie et al ., 2000, 2001), much of the previous work on the effects of kindling on memory has employed stimulation of the dorsal hippocampus (dHPC). These studies have found that dHPC kindling produces a relatively selective and enduring disruption of spatial memory (Leung et al ., 1996; Hannesson et al ., 2001a, 2001b, 2004).…”

Section: Introductionmentioning

confidence: 99%

Anterior perirhinal cortex kindling produces long‐lasting effects on anxiety and object recognition memory

Hannesson

Howland

Pollock

et al. 2005

Eur J of Neuroscience

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Temporal lobe epilepsy (TLE) is frequently accompanied by memory impairments and, although their bases are unknown, most research has focused on the hippocampus. The present study investigated the importance of another medial temporal lobe structure, the perirhinal cortex (Prh), in changes in memory in TLE using kindling as a model. Rats were kindled twice daily with anterior Prh stimulation until three fully generalized seizures were evoked. Beginning 7 days later and on successive days, rats were tested in an elevated plus maze, a large circular open field, an open field object exploration task and a delayed-match-to-place task in a water maze in order to assess anxiety-related and exploratory behaviour, object recognition memory and spatial cognition. Kindling increased anxiety-related behaviour in both the elevated plus and open field mazes and disrupted spontaneous object recognition but spared all other behaviours tested. These results are consistent with other findings indicating a greater role for the Prh in object memory and emotional behaviour than in spatial memory and contrast with the selective disruption of spatial memory produced by dorsal hippocampal kindling. The site-selectivity of the behavioural disruptions produced by kindling indicates that such effects are probably mediated by changes particular to the site of seizure initiation rather than to changes in the characteristic circuitry activated by limbic seizure generalization. Further investigation of the behavioural effects of Prh kindling may be useful for studying the mechanisms of mnemonic and affective dysfunction associated with TLE and offer insights into bases for variability in such dysfunction across patients.

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The relation between extent of dorsal hippocampal kindling and delayed-match-to-place performance in the Morris water maze

Cited by 10 publications

References 30 publications

Distinct behavioral phenotypes in novel “fast” kindling-susceptible and “slow” kindling-resistant rat strains selected by stimulation of the hippocampal perforant path

Distinct behavioral phenotypes in novel “fast” kindling-susceptible and “slow” kindling-resistant rat strains selected by stimulation of the hippocampal perforant path

Enhancing Prefrontal Neuron Activity Enables Associative Learning of Temporally Disparate Events

Anterior perirhinal cortex kindling produces long‐lasting effects on anxiety and object recognition memory

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