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BS-2066 Lecture 11: Motor control Beyond

reflexes: swimming in a marine snail

Volko Straub Room: MSB 332

email: vs64@le.ac.uk

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Overview

From simple reflexes to fixed action patterns How

do they differ?

What are central pattern generators? How do they

work? Introduction of some theoretical models

Swimming in a marine snail An example of a real

life central pattern generator

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From simple reflexes to fixed action patterns

Simple reflexes are good for fast, stereotypic responses to external

stimuli Example: Escape behaviour

specific stimuli can also trigger more complex behaviours

Example: Egg retrieval in geese and gulls

Fixed Action Patterns

(FAPs)

Other examples:

many courtship

behaviours gaping and pecking

responses in young

birds

many more

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From simple reflexes to fixed action patterns study of FAPs is particularly linked to work by von Holst, Lorenz and Tinbergen,

which can be considered founders of field of neuroethology

study is based on observation of animal behaviour

FAPs are innate and species typical

FAPs are triggered by sign stimulus/releaser a stimulus that triggers FAP

once triggered FAPs are carried out to completion

today, the term FAP has

been widely replaced by

the term behavioural act

or behavioural pattern

Eibl-Eibesfeldt observed

many different cultures found evidence for

universal FAPs in humans

eyebrow flash

universal greeting

emotions in deaf-blind

children coyness behaviour

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Two hypotheses for the control of FAPs

Hypothesis 1: FAPs are generated by a sequence ofreflexes p Reflex chain

Also known as the peripheral control hypothesis

Reflex 1 S2 Reflex 2S1

Hypothesis 2:

The central control hypothesis

a central pattern generator

generates sequence of motor

behavioursS CPG

Component 1

Component 2

Component 3

FAP

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Peripheral vs central control

Egg retrieval: behaviour carries on after stimulus is removed

suggests that behavioural sequence is generated centrally and not by a

reflex chain

FAPs like egg retrieval are too complex for study of neuronal network

that controls behaviour

Organisation of basic locomotion is less complex, e.g.

walking: limbs move forward and backwards

flying: wings move up and down

general: locomotion involves rhythmic flexion and extension ofmuscle groups

highly repetitive, good for experimental analysis

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How can central neuronal networks

generate rhythmic activity pattern?

Pacemaker Emergent network

property

P

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Central Pattern Generators

Pacemaker model

intrinsic oscillator / pacemaker

imposes activity (rhythm) on network

To achieve two opposing phases of activity, neuron(s) that are active

whilst pacemaker is inactive require mechanism that drives their

activity, e.g.:

EF

P

P

F

E

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Central Pattern Generators

Network oscillator

How to build network oscillator?

Suggestion: Two neurons coupled by excitatory synapse

Problem: Positive feedback circuit is very unstable!

F EF

E

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Central Pattern Generators

Half-centre model

Two neurons coupled by inhibitory synapses produces stableoscillation (rhythm)

requires a mechanism that progressively reduces inhibitory effect:

fatigue, adaptation, progressive self-inhibition

Post-inhibitory rebound (PIR) can sustain oscillation without constant

drive

F E

D

F

E

D

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The sea angel Clione limacina

A simple model system

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Clione swimming behaviour

wings are modified foot of snail

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Clione swimming behaviour and CNS

swimming consists of twoalternating phases:

dorsal flexion (D-phase)

ventral flexion (V-phase)

Clione CNS few thousand neurons

clustered in a small

number of central

ganglia

cerebral

ganglia

pleuralganglion

wing

nerve

pedalganglion

intestinal

ganglion

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Location of swimming CPG

cerebral

ganglia

pleural

ganglion

wing

nerve

pedal

ganglion

intestinalganglion

electrode support

electrode

Clione

LW

RW

EMG record from left and right wing

A

pleural & intestinal ganglia removed

LW

RWB

cerebral ganglia removed

LW

RW

0.5 s

C

pedal ganglia disconnected

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Identification of swim motoneurons

backfilling makes it possible to identify

neurons with axons in a specific nerve place cut end of nerve into dye

dye is taken up by axon and

migrates to cell body

mapped neurons can be impaled with

intracellular electrodes to record theiractivity 1A

2A

~40 motoneurons in total including

2 large neurons:

1A: innervates dorsal wing side

2A: innervates ventral wing side

smaller motoneurons innervate only

certain areas of wing

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Swim motoneurons and pattern generation

inactivation of individual motoneurons does not affect overall swim

rhythm

simultaneous

recording from two

swim motoneurons

hyperpolarisation

of D-phase

motoneuron (red

box) has no effect

on V-phase

motoneuron

even photoinactivation of all motoneurons does not interrupt basic rhythm

Swim motoneurons are not involved in generation of swim rhythm!

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Swim interneurons swim interneurons have no peripheral processes can not be

identified by backfilling can only be identified by systematic search using intracellular

electrodes look for neurons that are active in phase with swim

motoneurons

swim motoneuron

swim interneuron

swim interneuron

swim motoneuron

inactivation of swim interneuronby hyperpolarisation (red box)

stops swim rhythm

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Swim interneurons and pattern generation

Clione has two groups of swim interneurons called 7 and 8

swim interneurons 7 are active during D-phase

swim interneurons 8 are active during V-phase

interneurons 7 and 8 are connected by inhibitory synapses

interneurons in the same group are electrically coupled

swim interneurons fire on rebound from inhibition(p post-inhibitory rebound)

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The Clione swim CPG

7

3 1 2 4

8

dorsal wing

muscles

ventral wing

muscles

rhythm

generation

motor

output

effector

organs

D-phase V-phase

7

8

13

2

4

D Vswim cycle

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Clione swim CPG

A half-centre oscillator with a twist

Clione swim CPG has all the elements of a half-centre oscillator rhythm generation can be fully explained by connections between different

interneuron types

What happens when swim interneurons are isolated from the swim network?

Swim interneurons possess

intrinsic bursting property!

Swim rhythm generation is

result of the combination of

intrinsic cellular properties

and network properties

before isolation

after isolation

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Summary Fixed action patterns are innate behaviours triggered by a sign

stimulus/releaser

Fixed action patterns are centrally controlled

Various models have been proposed for the central control of rhythmic

behaviours including:

o pacemaker neurons

o half-centre oscillators

Swim rhythm in the marine snail Clione is generated by a central pattern

generator with all the features of a half-centre oscillator

In addition, the interneurons of the Clione swim pattern generator also

have intrinsic bursting propertiesp so, they have the potential to function

as pacemaker neurons