Learning-induced modulation of the effect of neuroglial transmission on synaptic plasticity

Abstract

Training rats in a complex olfactory discrimination task results in acquisition of "rule learning" (learning how to learn), a term describing the capability to perform the task superbly. Such rule learning results in strengthening of both excitatory and inhibitory synaptic connections between neurons in the piriform cortex. Moreover, intrinsic excitability is also enhanced throughout the pyramidal neuron population. Surprisingly, the cortical network retains its stability under these long-term modifications. In particular, the susceptibility for long-term potentiation (LTP) induction, while decreased for a short time window, returns to almost its pretraining value, although significant strengthening of AMPA receptor-mediated glutamatergic transmission remains. Such network balance is essential for maintaining the single-cell modifications that underlie long-term memory while preventing hyperexcitability that would result in runaway synaptic activity. However, the mechanisms underlying the long-term maintenance of such balance have yet to be described. In this study, we explored the role of astrocyte-mediated gliotransmission in long-term maintenance of learning-induced modifications in susceptibility for LTP induction and control of the strength of synaptic inhibition. We show that blocking connexin 43 hemichannels, which form gap junctions between astrocytes, decreases significantly the ability to induce LTP by stimulating the excitatory connections between piriform cortex pyramidal neurons after learning only. In parallel, spontaneous miniature inhibitory postsynaptic current amplitude is reduced in neurons from trained rats only, to the level of prelearning. Thus gliotransmission has a key role in maintaining learning-induced cortical stability by a wide-ranged control on synaptic transmission and plasticity. NEW & NOTEWORTHY We explore the role of astrocyte-mediated gliotransmission in maintenance of olfactory discrimination learning-induced modifications. We show that blocking gap junctions between astrocytes decreases significantly the ability to induce long-term potentiation in the piriform cortex after learning only. In parallel, synaptic inhibition is reduced in neurons from trained rats only, to the level of prelearning. Thus gliotransmission has a key role in maintaining learning-induced cortical stability by a wide-ranged control on synaptic transmission and plasticity.

Immediate brain plasticity after one hour of brain–computer interface (BCI)

“…Also, the motility of synapse-associated astrocytic processes has been shown to be enhanced as early as 5 min after stimulus-induced long-term potentiation (Perez-Alvarez et al 2014). As neuroglial transmission has been shown to be fundamental in maintaining learning-induced cortical stability (long-term potentiation) (Jammal et al 2018), such rapid neuroglial processes, together with local increases in metabolism, seem likely to explain early MR-signal changes.…”

Astroglial connexins and cognition: memory formation or deterioration?

“…In contrast with the studies showing the deleterious effects of connexins on learning and memory, the role of connexin gap junctions and hemichannels in memory formation and consolidation has also been reported [13]. It has been shown that the deletion of these proteins and loss of gap junction communication results in a loss of short-term spatial memory [14,15].…”

“…There have been a number of studies documenting that connexins-associated gap junction and hemichannels are essential for normal learning and memory [13][14][15][16] (Table 1). Even the involvement of gap junction networks in the mushroom bodies in visual learning and memory in Drosophila has been reported [17,18].…”

“…Indeed, the gap junction communication is critical in inducing long-term potentiation (LTP) by stimulating the excitatory connections between piriform cortex pyramidal neurons. The blockade of connexin 43 hemichannels has been associated with a significant decrease in LTP and impairment in memory consolidation [13]. The key role of connexin 43 in learning and memory has been described in a number of studies.…”

“…There have been contrasting studies regarding the role of connexins in memory formation [13][14][15][16] and memory deterioration [31][32][33]. Careful analysis of these studies helps in elucidating that most of the studies describing the memory formation role of connexins are done with an aim to unfold the basal role/function of these proteins in normal state.…”