Journal club: Phylogenic plasticity of crustacean stomatogastric circuits

by Pierre Meyrand and Maurice Moulins

J. exp. Biol. 138, 107-132, 133-153 (1988)

This old twin papers describe a neural network that has a very similar designs to that of related species but produces distinct patterns of output. They concluded that the differences in the pattern of motor output depend more on the action of the extrinsic neuromodulation onto individual neurons than the synaptic architecture of the network.

I. Pyloric patterns and pyloric circuit of the shrimp Palaemon serratus
http://jeb.biologists.org/content/138/1/107

To find the general rules of neural circuit function, direct comparison of different circuits may be useful. Finding a common principle or 'building blocks' may help understanding the fundamental mechanisms underlying rhythmic pattern generation. In this study, the authors investigated the stomatogastric nervous system of a shrimp and compared it with those of larger crustaceans such as lobster and crab. They found that pyloric networks are very similar between this shrimp and large crustaceans.

The pattern of their rhythmic outputs are quite different.  In large decapods, the pyrolic circuit generate triphasic rhythm. The pacemaker AB fire in antiphase with the constrictor motoneurones (LP and PY). In shrimp, AB fires in phase with the constrictor neurones because of electrical connection; endogenous oscillatory property was only found in LP.

II. Pyloric patterns and pyloric circuit of the shrimp Palaemon serratus

http://jeb.biologists.org/content/138/1/133

The previous study (above) showed that the fundamental network architectures are almost identical between large decapods and the shrimp. This study investigate how extrinsic modulatory inputs contribut to produce the motor outputs of different patterns.

They found that the shrimp neurons responded differently to muscarinic agonist and dopamin than those in large decapods. For example, oxotremorine activated PY, while dopamine activated PD. In large decapods, muscarinic agnonist causes oscillation in PDs while inhibit PDs. In shrimp, AB neuron is driven by and returns an inhibitory feedback to the commissural pyrolic oscillator. In large decapods, AB is the conditional oscillator and act as the pacemaker.

   Altogether, the phylogenetic plasticity in motor pattern production does not derive from structural differences in the corresponding central neuronal circuits themselves. Rather it is due to the difference in the modulatory system controlling these circuits. 

Journal club: Recent Clione papers

Arshavsky published a series of studies on the Clione swim CPG. Those papers are "must read" for researchers who work on CPG. I pay the highest respect to them.They were published in late 80's and now can be categorized as classical papers.
   More recently, there came a series of papers performing more detailed(?) analyses on this system. The following are my impressions with regard to those recent Clione papers.

2004
"Cellular mechanisms underlying swim acceleration in the pteropod mollusk Clione limacina"
by Pirtle and Satterlie
Integr. Comp. Biol. (2004) 44 (1): 37-46. doi: 10.1093/icb/44.1.37

Clione can swim faster when attacking a prey. It had been suggested that 5-HT mediates the acceleration of the swim motor pattern. In this study, the authors examined what membrane current components were modified by 5-HT.
   It seems to me that the experiments were not well designed. The way they compared the effects of drugs seems problematic (e.g., Fig. 7D). Figures were not well arranged. A control swim activity was not presented in Fig. 2 but then shown in Fig. 3. The authors called ion channel blockers as "antagonists." Antagonists are for receptors. No description of what neurons they used. The introduction was great, though.


2006
"The contribution of the pleural type 12 interneuron to swim acceleration in Clione limacina"
by Pirtle and Satterlie
Invert Neurosci (2006) 6:161–168. DOI 10.1007/s10158-006-0029-8

In this paper, the authors examined the role of type-12 neurons in the swim acceleration.
   Type-12 neuron is recruited into the type7/8 half-center network when the CPG gets into the fast swim mode. Arshavsky et al. (1985) suggested that this neuron plays an important role in the swim acceleration by rewiring the circuit. It turned out that activation of type-12 had only a transient effect on the swim cycle frequency. They suggested that type 12 has rather minor roles in maintaining the fast swim mode. Its function may be bilateral coordination or to increase the stability of the network. Despite negative results, this paper is more interesting than the other two.


2010
"A hyperpolarization-activated inward current alters swim frequency of the pteropod mollusk Clione limacina"
Pirtle, Willingham, and Satterlie
Comparative Biochemistry and Physiology, Part A 157 (2010) 319–327. DOI:10.1016/j.cbpa.2010.07.025

I don't see much difference between this and the previous 2004 paper. The only change was that they now show ZD7288 data instead of CsCl. In Fig. 5E. They stated ZD7288 blocked the 5-HT effect. I cannot agree with that. If compared with Fig. 4D data, I see that 5-HT still increases the swim cycle frequency even in the presence of ZD7288. Oh and again they were still calling ZD7288 as an "antagonist" for Ih current.

Journal club: Development of the nervous system in Solenogastres (Mollusca) reveals putative ancestral spiralian features

Redl et al. EvoDevo 2014 5:48
DOI: 10.1186/2041-9139-5-48

Background: The evolutionary emergence of the Mollusca is unclear.  Some have proposed that molluscs stem from unsegmented organisms, while others say they stem from a segmented annelid-like ancestor. 

   In this study, the authors investigated the development of the nervous system in two species of solenogasters to describe the larval nervous system and also to test the hypotheses on segmented or unsegmented ancestry of molluscs. 

Observations: During the embryonic development, first neurons appear at the apical and abapical pole; the flask-shaped cells of the apical organ and the large cells associated with the suprarectal commissure are lost.

   The neuropile beneath the apical organ develops into the cerebral commissure. The cellular posterior connection of the lateral neurite bundles becomes the suprarectal commissure.

   Interestingly early nervous system development in the polychaetes shows strong similarity to the mode of neural development described here for solenogasters. They both develop apical organ with flask-shaped cells, and a single pair of longitudinal neurite bundles. Similarity in the pattern of serotonin-like immunoreactivity, and formation of the CNS from anterior and posterior ends. 

Conclusions: This study supports a nonsegmented ancestry of molluscs, but there is similarities between solenogasters and polychaetes during early nervous system development, such as the formation of the nervous system from an apical and abapical neurogenic domain.
   The authors suggest that they share neural features descent from the last common ancestor, which had no segmentation.  Segmentation may have evolved only along the line leading to the annelids.

Journal club: Evolution of highly diverse forms of behavior in molluscs

Current Biology 26, R965-71 (2016)
Binyamin Hochner and David L. Glanzman
DOI: http://dx.doi.org/10.1016/j.cub.2016.08.047

This short review paper starts off with the comparative anatomy of the nervous system.  The authors discuss the diversity of the nervous system and its co-evolution with body plan by showing a variety of nervous systems from Solenogastres to cephalopods. Then, cellular mechanisms of synaptic plasticity underlying learning in the gastropod Aplysia and the cephalopod Octopus were discussed.

The first part was fun to read.
Comparative anatomy of the nervous system is a good reminder that the molluscan nervous system, or the medullary cord, is organized in a ladder-like fashion. The loss of collinear pattern of gene expression may explain their simple body plans. The supremacy of Octopus in the motor and cognitive abilities can be due to the high expansion of two developmentally important gene families, extensive transposable element activity, and genome rearrangements.

The second part was somewhat boring.
The title says the diversity of behavior, but this part actually covers just synaptic plasticity in Aplysia (serotonin-mediated long-term facilitation) and Octopus (long-term potentiation). The mechanisms underlying the serotonergic enhancement of synaptic strength has already been described five hundred times elsewhere.  Plus, I don't think this is a valid comparison to discuss about the evolutional process, because the gill-withdrawal reflex and the higher-order learning are completely different brain functions. Such comparison merely shows different types of learning regardless of species, not actually explains the species-dependent differences or the evolution. This is like comparing the spinal reflex and motor learning in two different vertebrate species. No wonder they are different; synaptic plasticity has little to do with the diversity of behavioral expressions.

No bubble?

Experimental procedures often have lots of superstitions.
Even in electrophysiological techniques there are plenty of those.
Superstitions often make one comfortable while doing stressful experiments; however, it looks silly when you see someone following a superstition that you don't believe in.

Here's an example: the bubbles in a glass capillary microelectrode.
I know some people seriously worry about those bubbles. They let the electrode sit in a tube filled with 3M KCl solution for a few minutes. It looks as if some sort of Buddhist ceremony with an insence standing up in front of an altar.

I don't believe that religion and here's why.
Here is a microelectrodes with ugly bubbles.

I let the silver wire not to penetrate through these bubbles.

And the resistance was...

The voltage drop was -38mV with no bridge when -1nA was passed. 

So the electrode resistance was 38 MΩ.

Then, I let the bubble go out. 

Yes it took me a few minutes to get rid of all tiny bubbles.

And the resistance was...

It was reduced by 1 MΩ. 
So, those ugly stupid bubbles costed me 1 MΩ!

1 MΩ, Oh well...
Tell you what, when you play with 6 electrodes simultaneously poking around neurons looking for Si2 or Si3 or whatever cells, 1 MΩ drift is nothing.  The electrode resistance will change anyway by tens of MΩ when you poke around the brain looking for cells. It is no worth spending a good few minutes just to get rid of those stupid 1 MΩ bubbles. Just go for a poke with it and replace it when clogged. Think about the efficiency of your labor. Don't worry about the bubbles. 

The recovery paper has come out

Finally, my "recovery paper" came out:

Recruitment of polysynaptic connections underlies functional recovery of a neural circuit after lesion.

Akira Sakurai, Arianna N. Tamvacakis, Paul S. Katz

DOI: 10.1523/ENEURO.0056-16.2016

This paper shows that, when a neural circuit failed by losing one of its synapses within, functional recovery can occur through reorganization of the remaining neural circuitry. We show that a molluscan neural circuit recruits additional neurons in response to a lesion. The extent of recruitment predicts the extent of behavioral recovery. 

Even in a well-defined (sort of) invertebrate neural circuit, there are indirect, polysynaptic pathways that provide compensatory function or flexibility to the circuit. Such individual variability appears to be hidden under normal conditions but becomes relevant when challenged by neural injury.

This paper is a sequel of two preceding papers:

Functional Recovery after Lesion of a Central Pattern Generator (2009)

Hidden synaptic differences in a neural circuit underlie differential behavioral susceptibility to a neural injury (2014)

A simple half-center network oscillator with a twist

My latest paper came out from J Neurophys:

The central pattern generator underlying swimming in Dendronotus iris: A simple half-center network oscillator with a twist  

by Akira Sakurai and Paul S. Katz

DOI: 10.1152/jn.00150.2016

This paper describes the central oscillatory circuit underlying rhythmic swimming of a nudibranch sea slug, Dendronotus iris.

Dendronotus iris swims by rhythmically flexing its body to left and right.

The Dendronotus brain is a cluster of lobes or "ganglia." The neurons that produce the rhythmic motor output for swimming have their cell bodies in the pedal ganglia. They all project the axons toward the other side of the brain to synapse with their contralateral counterparts.  

The circuit is a typical "half-center oscillator" that consists of only two bilateral pairs of neurons. The paired neurons each inhibit their contralateral counterparts.  The circuit has a “twisted” organization; that is, a neuron in one pair is excitatory-coupled contralaterally to a neuron in the other pair.

The Dendronotus swim CPG is a half-center oscillator.  The left illustration shows actual synaptic connections. The left Si3 (L-Si3) neuron forms an excitatory synapse and electrical connection onto the right Si2 (R-Si2), forming a twisted configuration. A modified version is shown on the right. Coupled Si2 and Si3 neurons form a functional unit that works as a half-center to produce rhythmic bursting.

The half-center oscillator is the simplest design of a network oscillator, in which two neuronal elements with no endogenous rhythmicity form reciprocally inhibititory synapses. The half-center theory was first proposed by T. Graham Brown in 1911 after the historical experiment with a walking cat with transected spinal cord.

In addition to the reciprocal inhibition, each functional unit of the half-center oscillator generally contains the excitatory neurons that provide rhythmic excitatory drive onto the mutually-inhibitory neurons (eg., Clione, tadpole, lamprey, zebrafish, and mice). Because of high complexity with so many neurons involved, the role of the excitatory neurons have not been clearly understood.  Here, we found that the Dendronotus swim circuit consists of only 4 neurons. By using "Dynamic Clamping" technique, we manipulated the strength of the excitatory synapse and found that they play crucial roles for the circuit to function as the half-center oscillator.  To our knowledge, this is probably the simplest half-center oscillator described to date. Because of such simplicity, this circuit is also highly manipulable, and hence may provide a good system to study the fundamental properties of a network oscillator.