Learning‐dependent plasticity of hippocampal CA1 pyramidal neuron postburst afterhyperpolarizations and increased excitability after inhibitory avoidance learning depend upon basolateral amygdala inputs

Abstract

Hippocampal pyramidal neurons in vitro exhibit transient learning-dependent reductions in the amplitude and duration of calcium-dependent postburst afterhyperpolarizations (AHPs), accompanied by other increases in excitability (i.e., increased firing rate, or reduced spike-frequency accommodation) after trace eyeblink conditioning or spatial learning, with a time-course appropriate to support consolidation of the learned tasks. Both these tasks require multiple days of training for acquisition. The hippocampus also plays a role in acquisition of single trial inhibitory avoidance learning. The current study assessed AHP plasticity in this single-trial learning task using in vitro tissue slices prepared at varying intervals posttrial using intracellular current-clamp recordings. Reduced AHPs and reduced accommodation were seen in ventral CA1 pyramidal neurons within 1 h posttraining, plasticity which persisted 24 h but was extinguished >72 h posttrial. There was also a reduction in ventral CA1 AHPs and accommodation 1 h following simple exposure to the IA apparatus (a novel context) but this change was extinguished by 24 h postexposure. Reductions in AHPs and accommodation were also seen in dorsal CA1 pyramidal neurons, but were delayed until 24 h posttrial and extinguished at >72 h posttrial. Finally, transient inactivation of the basolateral complex of the amygdala (with the local anesthetics lidocaine or bupivacaine) either immediately before or immediately posttrial blocked both learning and learning-dependent changes in excitability in the hippocampus assessed 24 h posttrial. CA3 pyramidal neurons showed no reductions in AHP peak amplitude or accommodation following IA training or context exposure.

TNF-alpha inhibition prevents cognitive decline and maintains hippocampal BDNF levels in the unpredictable chronic mild stress rat model of depression

“…Different from the MWM test, the Passive Avoidance learning was shown to involve hippocampal in addition to the amygdala function because of having contextual features in addition to fearrelated factors [35][36][37]. Relatively few studies have used Passive Avoidance Test in the chronic mild stress models.…”

Environmental enrichment modulates intrinsic cellular excitability of hippocampal CA1 pyramidal cells in a housing duration and anatomical location-dependent manner

“…Indeed, a reduction of AHP has previously been demonstrated after 30-35 days of periodic enrichment in male rats [35]. In addition, a reduction of AHP due to learning has long been established [1,8,14,38,48]. Recently, Farmer and Thompson [14] have shown that a single exposure to a novel context is sufficient to decrease both mAHP and sAHP in CA1 pyramidal neurons.…”

“…In addition, a reduction of AHP due to learning has long been established [1,8,14,38,48]. Recently, Farmer and Thompson [14] have shown that a single exposure to a novel context is sufficient to decrease both mAHP and sAHP in CA1 pyramidal neurons. Therefore, a common mechanism might increase cellular excitability through the modulation of AHP after learning and after an exposure to environment enrichment.…”

Memory-enhancing intra-basolateral amygdala clenbuterol infusion reduces post-burst afterhyperpolarizations in hippocampal CA1 pyramidal neurons following inhibitory avoidance learning

“…Similarly, 24 h after acquisition of an IA task, in which a high-intensity footshock was paired with the dark compartment, hippocampal CA1 post-burst afterhyperpolarizations (AHPs) were significantly reduced, i.e. intrinsic excitability was enhanced (Farmer & Thompson, 2012), while immediate post-trial BLA lidocaine infusions blocked this learning-dependent plasticity in CA1 AHPs. Learning-dependent reductions in CA1 neuron AHPs are a reliable and highly replicable cellular mechanism expressed in hippocampus, with a time-course appropriate to support memory consolidation (Disterhoft & Oh, 2006;Farmer & Thompson, 2012;McKay, Mathews, Oliveira, & Disterhoft, 2009;Oh, Kuo, Wu, Sametsky, & Disterhoft, 2003;Oh, Oliveira, & Disterhoft, 2010;.…”