Functional properties and cell type specific distribution of<i>I</i>h channels in leech neurons

Gerard, Ednan; Hochstrate, Peter; Dierkes, Paul Wilhelm; Coulon, Philippe

doi:10.1242/jeb.062836

Cited by 12 publications

(13 citation statements)

References 47 publications

(75 reference statements)

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“…Leech sensory cells express several different ion channels (Johansen, 1991; Kleinhaus and Angstadt, 1995; Gerard et al, 2012), most of which we did not include in our model for the sake of simplicity. Sodium-dependent K + channels as they were found in leech pressure cells (Klees et al, 2005), for example, might also affect T cell spiking in an activity dependent manner.…”

Section: Discussionmentioning

confidence: 99%

Non-synaptic Plasticity in Leech Touch Cells

2019

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The role of Na+/K+-pumps in activity-dependent synaptic plasticity has been described in both vertebrates and invertebrates. Here, we provide evidence that the Na+/K+-pump is also involved in activity-dependent non-synaptic cellular plasticity in leech sensory neurons. We show that the resting membrane potential (RMP) of T cells hyperpolarizes in response to repeated somatic current injection, while at the same time their spike count (SC) and the input resistance (IR) increase. Our Hodgkin–Huxley-type neuron model, adjusted to physiological T cell properties, suggests that repetitive action potential discharges lead to increased Na+/K+-pump activity, which then hyperpolarizes the RMP. In consequence, a slow, non-inactivating current decreases, which is presumably mediated by voltage-dependent, low-threshold potassium channels. Closing of these putative M-type channels due to hyperpolarization of the resting potential increases the IR of the cell, leading to a larger number of spikes. By this mechanism, the response behavior switches from rapidly to slowly adapting spiking. These changes in spiking behavior also effect other T cells on the same side of the ganglion, which are connected via a combination of electrical and chemical synapses. An increased SC in the presynaptic T cell results in larger postsynaptic responses (PRs) in the other T cells. However, when the number of elicited presynaptic spikes is kept constant, the PR does not change. These results suggest that T cells change their responses in an activity-dependent manner through non-synaptic rather than synaptic plasticity. These changes might act as a gain-control mechanism. Depending on the previous activity, this gain could scale the relative impacts of synaptic inputs from other mechanoreceptors, versus the spike responses to tactile skin stimulation. This multi-tasking ability, and its flexible adaptation to previous activity, might make the T cell a key player in a preparatory network, enabling the leech to perform fast behavioral reactions to skin stimulation.

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Section: Discussionmentioning

confidence: 99%

Non-synaptic Plasticity in Leech Touch Cells

2019

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“…The activation of Ih at rest in only a subset of CPG neurons (dINs) is not without precedent. For example, specific neurons of the leech heartbeat network, such as HNs and mechanosensory pressure neurons, show a prominent Ih at rest; but other neuron subtypes, such as Retzius neurons, display only a small sag potential at very hyperpolarized levels (>−70 mV) [ 40 ]. Again, the HNs in this network are the excitatory rhythm-generating interneurons, suggesting that Ih may play a common role in contributing to the rhythmicity of excitatory interneurons in phylogenetically diverse CPG networks.…”

Section: Discussionmentioning

confidence: 99%

Control of Xenopus Tadpole Locomotion via Selective Expression of Ih in Excitatory Interneurons

2018

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SummaryLocomotion relies on the coordinated activity of rhythmic neurons in the hindbrain and spinal cord and depends critically on the intrinsic properties of excitatory interneurons. Therefore, understanding how ion channels sculpt the properties of these interneurons, and the consequences for circuit function and behavior, is an important task. The hyperpolarization-activated cation current, Ih, is known to play important roles in shaping neuronal properties and for rhythm generation in many neuronal networks. We show in stage 42 Xenopus laevis frog tadpoles that Ih is strongly expressed only in excitatory descending interneurons (dINs), an important ipsilaterally projecting population that drives swimming activity. The voltage-dependent HCN channel blocker ZD7288 completely abolished a prominent depolarizing sag potential in response to hyperpolarization, the hallmark of Ih, and hyperpolarized dINs. ZD7288 also affected dIN post-inhibitory rebound firing, upon which locomotor rhythm generation relies, and disrupted locomotor output. Block of Ih also unmasked an activity-dependent ultraslow afterhyperpolarization (usAHP) in dINs following swimming, mediated by a dynamic Na/K pump current. This usAHP, unmasked in dINs by ZD7288, resulted in suprathreshold stimuli failing to evoke swimming at short inter-swim intervals, indicating an important role for Ih in maintaining swim generation capacity and in setting the post-swim refractory period of the network. Collectively, our data suggest that the selective expression of Ih in dINs determines specific dIN properties that are important for rhythm generation and counteracts an activity-dependent usAHP to ensure that dINs can maintain coordinated swimming over a wide range of inter-swim intervals.

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“…Besides a different morphology, the influence of which remains here enigmatic, mechano-sensory neurons in leech show differences in the strength of expressed ionic conductances. P cells have the strongest hyperpolarization activated conductance ( Gerard et al, 2012 ), and their delayed potassium rectifier gates faster compared to N cells ( Stewart et al, 1989 ). Both findings support the faster voltage signaling in P cells compared to N cells that we describe.…”

Section: Resultsmentioning

confidence: 99%

Intrinsic frequency response patterns in mechano-sensory neurons of the leech

Fischer¹,

Scherbarth²,

Chagnaud

et al. 2017

Biology Open

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Animals employ mechano-sensory systems to detect and explore their environment. Mechano-sensation encompasses stimuli such as constant pressure, surface movement or vibrations at various intensities that need to be segregated in the central nervous system. Besides different receptor structures, sensory filtering via intrinsic response properties could provide a convenient way to solve this problem. In leech, three major mechano-sensory cell types can be distinguished, according to their stimulus sensitivity, as nociceptive, pressure and touch cells. Using intracellular recordings, we show that the different mechano-sensory neuron classes in Hirudo medicinalis differentially respond supra-threshold to distinct frequencies of sinusoidal current injections between 0.2 and 20 Hz. Nociceptive cells responded with a low-pass filter characteristic, pressure cells as high-pass filters and touch cells as an intermediate band-pass filter. Each class of mechano-sensory neurons is thus intrinsically tuned to a specific frequency range of voltage oscillation that could help segregate mechano-sensory information centrally.

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Functional properties and cell type specific distribution ofIh channels in leech neurons

Cited by 12 publications

References 47 publications

Non-synaptic Plasticity in Leech Touch Cells

Non-synaptic Plasticity in Leech Touch Cells

Control of Xenopus Tadpole Locomotion via Selective Expression of Ih in Excitatory Interneurons

Intrinsic frequency response patterns in mechano-sensory neurons of the leech

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