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

Abstract

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...

Trace fear conditioning enhances synaptic and intrinsic plasticity in rat hippocampus

“…Thus learning-induced intrinsic and synaptic modifications of postsynaptic neurons are capable of facilitating subsequent learning. In contrast, prior training in trace eyeblink conditioning did not enhance learning of hippocampus-dependent Morris water maze; however, simultaneous training in both tasks facilitated trace eyeblink but not water maze learning (Kuo et al 2006). Additional studies will be required to determine the extent to which intrinsic and/or synaptic changes following trace fear conditioning impact learning of other hippocampusdependent learning tasks or whether learning of other tasks affects the acquisition of trace fear conditioning.…”

Intrinsic Neuronal Excitability Is Reversibly Altered by a Single Experience in Fear Conditioning

“…However, a reduction in the AHP caused by learning one task could aid in learning a second one. In fact, learning both Morris water maze and trace eyeblink conditioning reduce the AHP, and simultaneous training in the two tasks facilitates learning trace eyeblink conditioning (Kuo et al 2006). Olfactory discrimination also increases intrinsic excitability in CA1 pyramidal neurons during and on the day of learning, but not after the animal has learned the rule.…”

The N-methyl-d-aspartate receptor modulator GLYX-13 enhances learning and memory, in young adult and learning impaired aging rats

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