Neuronal Substrate of Classical Conditioning in the Hippocampus

Berger, Theodore W.; Alger, Bradley E.; Thompson, Richard F.

doi:10.1126/science.1257783

Cited by 515 publications

(233 citation statements)

References 25 publications

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“…A closer examination revealed that the theta-related differences emerged very early in training and were significant on day 1 [F(1,8) ϭ 5.52, P ϭ 0.047 (Fig. 4)], a result consistent with other data implicating the hippocampus in the earliest stages of acquisition (7,8,16,(25)(26)(27)(37)(38)(39)(40). The groups of behavioral control animals that were assigned trials per day and ITIs matching those of the experimental groups did not differ in learning rate from each other [F(1,8) ϭ 0.01, P ϭ 0.92], indicating that the difference observed between Tϩ and TϪ groups was a result of the experimental manipulation (i.e., triggering trials on theta or non-theta states).…”

Section: Resultssupporting

confidence: 74%

Oscillatory brain states and learning: Impact of hippocampal theta-contingent training

Seager

Johnson

Chabot

et al. 2002

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

184

185

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Eyeblink classical conditioning is a relatively simple form of associative learning that has become an invaluable tool in our understanding of the neural mechanisms of learning. When studying rabbits in this paradigm, we observed a dramatic modification of learning rate by conducting training during episodes of either hippocampal theta or hippocampal non-theta activity as determined by on-line slow-wave spectral analysis. Specifically, if animals were given trials only when a computer analysis verified a predominance of slow-wave oscillations at theta frequencies (3-8 Hz), they learned in half as many trials as animals trained during non-theta hippocampal activity (58 vs. 115). This finding provides important evidence from awake, behaving animals that supports recent advances in our knowledge of (i) brain sites and neurobiological mechanisms of learning and memory, specifically hippocampus and theta oscillations, (ii) the biological plausibility of current models of hippocampal function that posit important roles for oscillatory potentials, and (iii) the design of interfaces between biological and cybernetic (electronic) systems that can optimize cognitive processes and performance.

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Section: Resultssupporting

confidence: 74%

Oscillatory brain states and learning: Impact of hippocampal theta-contingent training

Seager

Johnson

Chabot

et al. 2002

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

184

185

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“…Although their findings differ from ours because such cells were found following trial outcome, and not preceding it, they provide important evidence that the hippocampus has information about the trial outcome. Our results are in accordance with previous reports showing that different hippocampal cells can code for different sensory and behavioral features of events (Ranck 1973;Berger et al 1976;Wiener et al 1989;Wood et al 1999). In our data set, we found that early in training some cells did not present spatial coding, other cells exhibited pure spatial coding, while others coded for both position and behavioral responses.…”

Section: Discussionsupporting

confidence: 83%

“…Starting with Ranck (1973), several experiments have identified firing patterns of hippocampal neurons related to nonspatial stimuli, as well as cognitive and behavioral events (Ranck 1973;Berger et al 1976;Wiener et al 1989;Wood et al 1999). Among the clearest of these are single hippocampal neurons that fire predicting eye-blink responses in a classical conditioning paradigm (Berger et al 1983).…”

Section: Discussionmentioning

confidence: 99%

A mechanism for the formation of hippocampal neuronal firing patterns that represent what happens where

Tort¹,

Komorowski²,

Eichenbaum³

2011

Learn. Mem.

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The association of specific events with the context in which they occur is a fundamental feature of episodic memory. However, the underlying network mechanisms generating what-where associations are poorly understood. Recently we reported that some hippocampal principal neurons develop representations of specific events occurring in particular locations (item-position cells). Here, we investigate the emergence of item-position selectivity as rats learn new associations for reward and find that before the animal's performance rises above chance in the task, neurons that will later become itemposition cells have a strong selective bias toward one of two behavioral responses, which the animal will subsequently make to that stimulus. This response bias results in an asymmetry of neural activity on correct and error trials that could drive the emergence of particular item specificities based on a simple reward-driven synaptic plasticity mechanism.The hippocampus is critically involved in the acquisition of new episodic memories (Scoville and Milner 1957;Eichenbaum 2000). In particular, the formation of associations between events and the context where they occur, a fundamental feature of episodic memory, depends on hippocampal function (Manns and Eichenbaum 2006;Eichenbaum et al. 2007).We have recently shown that some hippocampal principal neurons develop representations of specific events occurring in particular locations (Komorowski et al. 2009). In this study, animals learned which of two stimulus items (what) was rewarded depending on the environmental context (where) in which the items were presented (Rajji et al. 2006;Manns and Eichenbaum 2009). On each trial, a rat initially explored one of the two contexts, after which the two stimulus items were placed into different positions (corners) of the context (Fig. 1A); the animal then investigated the items (scented flower pots), and should learn to dig (Go response) for a buried food reward in the appropriate pot for that context or not dig (NoGo) at pots where no reward was buried. All animals performed at no better than chance (50%) for the first 30 trials, then acquired the what-where associations, reaching an average accuracy of 86% in the last 30 trials of the training session (Fig. 1B).In this paradigm, we previously indentified principal neurons showing differential firing during the sampling of one of the two stimulus items when located in the same position (Fig. 1C, left), which we called as item-position (IP) cells (Komorowski et al. 2009). IP cell responses did not distinguish the items during the first 30 trials of the learning session, but did fire during item sampling at particular locations. Subsequently, we showed that many IP cells increased firing during the sampling of an item-position combination in parallel with learning (Fig. 1C, left). Importantly, we observed approximately equivalent selectivity for rewarded and nonrewarded item-position combinations (Fig. 1C, middle). We also identified principal neurons that were active during item sampl...

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“…No effect was seen on acquisition for either task when using the consecutive training design. Taken together, these findings provide insight into how the hippocampus processes information when animals learn multiple hippocampus-dependent tasks.The importance of the hippocampus in learning is well established (Berger et al 1976;Berger and Thompson 1978;Disterhoft et al 1999). A number of studies have demonstrated the necessity of the hippocampus in learning spatial and nonspatial tasks, as well as those requiring the association of temporally remote events (Morris et al 1982;Moyer Jr. et al 1990;Davidson and Jarrard 1993;McEchron et al 1998;Bannerman et al 1999;Weiss et al 1999a).…”

mentioning

confidence: 99%

Simultaneous training on two hippocampus-dependent tasks facilitates acquisition of trace eyeblink conditioning

Kuo¹,

Lee²,

Disterhoft³

2006

Learn. Mem.

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A common cellular alteration, reduced post-burst afterhyperpolarization (AHP) in CA1 neurons, is associated with acquisition of the hippocampus-dependent tasks trace eyeblink conditioning and the Morris water maze. As a similar increase in excitability is correlated with these two learning paradigms, we sought to determine the interactive behavioral effects of training animals on both tasks by using either a consecutive or simultaneous training design. In the consecutive design, animals were trained first on either the trace eyeblink conditioning task for six sessions, followed by training on the water maze task for six sessions, or vice versa. The simultaneous design consisted of six or 11 training days; animals received one session/day of both trace eyeblink conditioning and water maze training. Separate groups were used for consecutive and simultaneous training. Animals trained on both tasks simultaneously were significantly facilitated in their ability to acquire the trace eyeblink conditioning task; no effect of simultaneous training was seen on the water maze task. No effect was seen on acquisition for either task when using the consecutive training design. Taken together, these findings provide insight into how the hippocampus processes information when animals learn multiple hippocampus-dependent tasks.The importance of the hippocampus in learning is well established (Berger et al. 1976;Berger and Thompson 1978;Disterhoft et al. 1999). A number of studies have demonstrated the necessity of the hippocampus in learning spatial and nonspatial tasks, as well as those requiring the association of temporally remote events (Morris et al. 1982;Moyer Jr. et al. 1990;Davidson and Jarrard 1993;McEchron et al. 1998;Bannerman et al. 1999;Weiss et al. 1999a). Two such tasks are trace eyeblink conditioning (EBC) and Morris water maze (WMZ).A common cellular mechanism that underlies learning, increased membrane excitability, has been observed by several investigators. This mechanism is conserved across species, tasks, and brain regions. Trains of action potentials in both hippocampal and cortical neurons are followed by a prolonged post-burst afterhyperpolarization (AHP), which decreases neuronal excitability and inhibits further firing to a sustained depolarizing input (Schwindt et al. 1988;Storm 1990). A reduction in the AHP occurred in both rat and rabbit CA1 pyramidal neurons after acquisition of trace EBC (Moyer Jr. et al. 1996;Kuo et al. 2004). This reduction also occurred in rat CA1 pyramidal neurons after acquisition of another type of hippocampus-dependent task, the spatial Morris WMZ (Oh et al. 2003). Alterations in the AHP with learning have also been observed in rat piriform cortical neurons after acquisition of an odor discrimination task (Saar et al. 1998). In both hippocampus and piriform cortex, the reduced AHP followed a similar time course after learning, with a maximal reduction 24 h after task acquisition and a return to baseline within 7 d of acquisition (Moyer Jr. et al. 1996;Saar et al. 1998).In a...

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Neuronal Substrate of Classical Conditioning in the Hippocampus

Cited by 515 publications

References 25 publications

Oscillatory brain states and learning: Impact of hippocampal theta-contingent training

Oscillatory brain states and learning: Impact of hippocampal theta-contingent training

A mechanism for the formation of hippocampal neuronal firing patterns that represent what happens where

Simultaneous training on two hippocampus-dependent tasks facilitates acquisition of trace eyeblink conditioning

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