Effects of Early Hippocampal Lesions on Trace, Delay, and Long-Delay Eyeblink Conditioning in Developing Rats

Ivkovich, Dragana; Stanton, Mark E.

doi:10.1006/nlme.2001.4027

Cited by 66 publications

(94 citation statements)

References 37 publications

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“…It has been hypothesized that a hippocampal-dependent short-term memory system is necessary to create and maintain a representation of the CS during the trace interval, allowing for the integration of the temporally discontiguous CS and US events (Rodriguez & Levy, 2001;Wallenstein, Eichenbaum, & Hasselmo, 1998). If the late ontogenetic emergence of trace conditioning is due to hippocampal immaturity, as has previously been suggested (Ivkovich & Stanton, 2001;Moye & Rudy, 1987), and delay conditioning is not hippocampal dependent, it remains unanswered why long-delay conditioning would also be developmentally delayed (like trace conditioning) and, furthermore, why long-delay and trace conditioning would emerge at the same time.…”

Section: Discussionmentioning

confidence: 99%

“…Some studies have been performed to specifically examine a possible role for the hippocampus in long-delay conditioning, and the results have confirmed that hippocampal lesions selectively impact trace, but not long-delay, conditioning, at least with eyeblink preparations (Beylin, Gandhi, Wood, Talk, Matzel, & Shors, 2001;Ivkovich & Stanton, 2001). Interestingly, however, Beylin et al did report that lesions of the hippocampus had detrimental effects on acquisition of the eyeblink response in a delay group that was trained with a "very long" duration CS.…”

Section: Discussionmentioning

confidence: 99%

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Trace and long-delay fear conditioning in the developing rat

Barnet

Hunt

2005

Learning & Behavior

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Trace and long-delay fear conditioning in the developing rat

Barnet

Hunt

2005

Learning & Behavior

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“…To equate the interstimulus interval (ISI) (750 ms) between the CS and US in the delay versus trace paradigms, an 850 ms CS that overlapped and coterminated with a 100 ms US was used during delay conditioning. Thus, this version of delay conditioning differs from the standard delay procedure, which typically incorporates a shorter CS and ISI (Solomon and Groccia-Ellison, 1996;Gould et al, 1999;Ivkovich and Stanton, 2001). During very long delay conditioning, the ISI was extended to 1400 ms such that a CS of 1500 ms overlapped and coterminated with a 100 ms US.…”

Section: Methodsmentioning

confidence: 99%

Temporal Discontiguity Is neither Necessary nor Sufficient for Learning-Induced Effects on Adult Neurogenesis

Leuner¹,

Waddell²,

Gould³

et al. 2006

J. Neurosci.

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Some, but not all, types of learning and memory can influence neurogenesis in the adult hippocampus. Trace eyeblink conditioning has been shown to enhance the survival of new neurons, whereas delay eyeblink conditioning has no such effect. The key difference between the two training procedures is that the conditioning stimuli are separated in time during trace but not delay conditioning. These findings raise the question of whether temporal discontiguity is necessary for enhancing the survival of new neurons. Here we used two approaches to test this hypothesis. First, we examined the influence of a delay conditioning task in which the duration of the conditioned stimulus (CS) was increased nearly twofold, a procedure that critically engages the hippocampus. Although the CS and unconditioned stimulus are contiguous, this very long delay conditioning procedure increased the number of new neurons that survived. Second, we examined the influence of learning the trace conditioned response (CR) after having acquired the CR during delay conditioning, a procedure that renders trace conditioning hippocampal-independent. In this case, trace conditioning did not enhance the survival of new neurons. Together, these results demonstrate that associative learning increases the survival of new neurons in the adult hippocampus, regardless of temporal contiguity.

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“…For example, CS preexposure attenuates CR-related hippocampal CA1 activation during subsequent conditioning (Katz, Rogers, & Steinmetz, 2002). Given the fact that large hippocampal lesions impair trace eyeblink conditioning (Ivkovich & Stanton, 2001;Kishimoto et al, 2006;Moyer et al, 1990;Solomon et al, 1986;Tseng et al, 2004;Weiss et al, 1999) but not delay eyeblink conditioning (Akase et al, 1989;Lee & Kim, 2004;Port et al 1985;Schmaltz & Theios, 1972;Solomon & Moore, 1975), even when delay and trace are matched for CS-US interval (Beylin et al, 2001;Ivkovich & Stanton, 2001), it might be expected that the development and pattern of hippocampal activation during trace conditioning would appear different from the development and pattern of hippocampal activation during delay conditioning when they are matched for CS-US interval. Resolution of this issue might provide further clues as to the type of information that the hippocampus is communicating to the cerebellum (or vice versa) during different phases of training which allows trace conditioning to occur but which is not necessary for delay conditioning.…”

Section: The Involvement Of the Hippocampal Ca1 Field In Trace Conditmentioning

confidence: 99%

“…Trace eyeblink conditioning appears to require the same brainstem-cerebellar circuit for acquisition and retention as delay eyeblink conditioning (Takehara, Kawahara, & Kirino, 2003;Woodruff-Pak, Lavond, & Thompson, 1985) but, when the stimulus-free trace period is long enough (250-ms for rodents; Tseng, Guan, Disterhoft, & Weiss, 2004;Weiss, Bouwmeester, Power, & Disterhoft 1999; 500-ms for rabbits, Moyer, Deyo, & Disterhoft, 1990) the hippocampus is required as well. Lesion studies have indicated that the hippocampal formation is necessary for normal acquisition and/ or proper timing of trace eyeblink CRs (Beylin et al 2001;Ivkovich & Stanton, 2001;James, Hardiman, & Yeo, 1987;Kishimoto, Nakazawa, Tonegawa, Kirino, & Kano, 2006;Moyer et al, 1990;Port, Romano, Steinmetz, Mikhail, & Patterson, 1986;Solomon, Vander Schaaf, Thompson, & Weisz, 1986;Takehara et al, 2003;Tseng et al, 2004;Weiss et al, 1999) and for short-term retention (perhaps up to several weeks; Kim, Clark, & Thompson, 1995;Takehara, Kawahara, Takatsuki, & Kirino, 2002;Takehara et al, 2003) of trace eyeblink conditioning. However, recording studies of CA1 unit activity during trace eyeblink conditioning have yielded somewhat inconsistent results.…”

Section: Introductionmentioning

confidence: 99%

Hippocampal and cerebellar single-unit activity during delay and trace eyeblink conditioning in the rat

Green

Arenos

2007

Neurobiology of Learning and Memory

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In delay eyeblink conditioning, the CS overlaps with the US and only a brainstem-cerebellar circuit is necessary for learning. In trace eyeblink conditioning, the CS ends before the US is delivered and several forebrain structures, including the hippocampus, are required for learning, in addition to a brainstem-cerebellar circuit. The interstimulus interval (ISI) between CS onset and US onset is perhaps the most important factor in classical conditioning, but studies comparing delay and trace conditioning have typically not matched these procedures in this crucial factor, so it is often difficult to determine whether results are due to differences between delay and trace or to differences in ISI.In the current study, we employed a 580-ms CS-US interval for both delay and trace conditioning and compared hippocampal CA1 activity and cerebellar interpositus nucleus activity in order to determine whether a unique signature of trace conditioning exists in patterns of single-unit activity in either structure. Long-Evans rats were chronically implanted in either CA1 or interpositus with microwire electrodes and underwent either delay eyeblink conditioning, or trace eyeblink conditioning with a 300-ms trace period between CS offset and US onset. On trials with a CR in delay conditioning, CA1 pyramidal cells showed increases in activation (relative to a pre-CS baseline) during the CS-US period in sessions 1-4 that was attenuated by sessions 5-6. In contrast, on trials with a CR in trace conditioning, CA1 pyramidal cells did not show increases in activation during the CS-US period until sessions 5-6. In sessions 5-6, increases in activation were present only to the CS and not during the trace period. For rats with interpositus electrodes, activation of interpositus neurons on CR trials was present in all sessions in both delay and trace conditioning. However, activation was greater in trace compared to delay conditioning in the first half of the CS-US interval (during the trace CS) during early sessions of conditioning and, in later sessions of conditioning, activation was greater in the second half of the CS-US interval (during the trace interval). These results suggest that the pattern of hippocampal activation that differentiates trace from delay eyeblink conditioning is a slow buildup of activation to the CS, possibly representing encoding of CS duration or discrimination of the CS from the background context. Interpositus nucleus neurons show strong modeling of the eyeblink CR regardless of paradigm but show a changing pattern across conditioning that may be due to the necessary contributions of forebrain processing to trace conditioning.

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Effects of Early Hippocampal Lesions on Trace, Delay, and Long-Delay Eyeblink Conditioning in Developing Rats

Cited by 66 publications

References 37 publications

Trace and long-delay fear conditioning in the developing rat

Trace and long-delay fear conditioning in the developing rat

Temporal Discontiguity Is neither Necessary nor Sufficient for Learning-Induced Effects on Adult Neurogenesis

Hippocampal and cerebellar single-unit activity during delay and trace eyeblink conditioning in the rat

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