Activity-Dependent Increase of the AHP Amplitude in T Sensory Neurons of the Leech

Abstract

We identified a new form of activity-dependent modulation of the afterhyperpolarization (AHP) in tactile (T) sensory neurons of the leech Hirudo medicinalis. Repetitive intracellular stimulation with 30 trains of depolarizing impulses at 15-s inter-stimulus interval (ISI) led to an increase of the AHP amplitude (~60% of the control). The enhancement of AHP lasted for >/=15 min. The AHP increase was also elicited when a T neuron was activated by repetitive stimulation of its receptive field. The ISI was a critical parameter for the induction and maintenance of AHP enhancement. ISI duration had to fit within a time window with the upper limit of 20 s to make the training effective to induce an enhancement of the AHP amplitude. After recovery from potentiation, AHP amplitude could be enhanced once again by delivering another training session. The increase of AHP amplitude persisted in high Mg(2+) saline, suggesting an intrinsic cellular mechanism for its induction. Previous investigations reported that AHP of leech T neurons was mainly due to the activity of the Na(+)/K(+) ATPase and to a Ca(2+)-dependent K(+) current (I(K/Ca)). In addition, it has been demonstrated that serotonin (5HT) reduces AHP amplitude through the inhibition of the Na(+)/K(+) ATPase. By blocking the I(K/Ca) with pharmacological agents, such as cadmium and apamin, we still observed an increase of the AHP amplitude after repetitive stimulation, whereas 5HT application completely inhibited the AHP increment. These data indicate that the Na(+)/K(+) ATPase is involved in the induction and maintenance of the AHP increase after repetitive stimulation. Moreover, the AHP increase was affected by the level of serotonin in the CNS. Finally, the increase of the AHP amplitude produced a lasting depression of the synaptic connection between two T neurons, suggesting that this activity-dependent phenomenon might be involved in short-term plasticity associated with learning processes.

Nonassociative Learning in Invertebrates

“…Cite this article as Cold Spring Harb Perspect Biol 2015;7:a021675 Scuri et al 2002). The persistent increase in AHP amplitude, following low-frequency stimulation of T cells, has been attributed to increased activity of the electrogenic Na þ pump, and requires activation of phospholipase A2 (Scuri et al 2005;Zaccardi et al 2012).…”

Activity-dependent suppression of spontaneous spike generation in the Retzius neurons of the leech Hirudo medicinalis L.

“…In addition, an increased activity of the Na/K-pump also causes an increase of the pAHP amplitude in Rz neurons, while a reduction of the extracellular K + concentration has opposite effects leading to depolarization of V m and disappearance of pAHP by slowing down the Na/Kpump (Yang and Kleinhaus 1984). Long-lasting phases of spike suppression attributed to the Na/K pumping rate have been described in other identified leech neurons (Scuri et al 2002). Our preliminary observations with reduced external K + concentrations indicate that the absence of both pAHP and PSD may be related to the inhibition of the Na/K-pump.…”

Seasonal variation of long-term potentiation at a central synapse in the medicinal leech

“…Hirudo also exhibits a diurnal activity rhythm (Lotz et al, 1970). Seasonal variation has been observed in a number of behavioral and neurophysiological processes in Hirudo, including non-associative learning, serotonin content in the CNS, activity-dependent modulation of afterhyperpolarization and acetylcholine-elicited K. B. Grey and B. D. Burrell currents in the serotonergic Retzius cells (Stenzel and Neuhoff, 1976;Catarsi et al, 1990;Szczupak et al, 1993;Scuri et al, 2002).…”