PSY2061

Biological Psychology

The control of action

Dr James Coxon
james.coxon@monash.edu
MEX Lab
“All mankind can do is to move things.....
whether whispering a syllable or felling a
forest”
– Dr Charles Sherrington

“We have a brain for one reason and one

reason only - and that's to produce
adaptable and complex movements….
…There can be no evolutionary advantage
to laying down memories of childhood or
perceiving the color of a rose if it doesn't
affect the way you're going to move”
- Professor Daniel Wolpert
Concepts
• Movement control poses and faces a degrees of
freedom problem
• Movement control is exerted at separate and
distinct levels
• The neural control of movement can be understood
as both hierarchical and parallel
• Neurons in primary motor cortex (M1) code for
movement direction/goal
• Neurological disorders of movement provide insight
into the function of different brain regions
Fundamentals
At birth, we have a limited behavioural repertoire
o Innate motor programs
During first ~15 years of life our motor system develops
through:
o maturation of neuronal circuitry
o observation
o learning through practising different motor activities
Fundamentals
In addition to basic motor skills we also
develop skilled motor coordination
Neural substrates expressed genetically, characteristic
of our species… Humans can do some amazing things!

https://www.youtube.com/watch?v=h6Qbwz0Uik8
Nilkolai Bernstein "It is clear that the basic difficulties
(1896-1966) for co-ordination consist precisely in
the extreme abundance of degrees
of freedom”

‘Bernstein’s problem’

Concept
Movement control poses and faces a
degrees of freedom problem
• 103 muscles spanning 102 joints
• 1011 neurons with 1014 synapses
• How is coordinated and controllable movement
even possible?

• What aspects of movement control are delegated

by an executive (the brain)?
• Does delegation simplify the control problem?
(Problem of displacement)

• Is all movement ‘controlled’ ?

• Or does movement coordination also

adhere to principles of self-organisation?
(e.g. a dynamical system with no executive)
 Concept
Movement control is exerted at separate and
distinct levels
(Components of the motor system)
 Muscles and Motoneurons
o Movement = change in joint angle
o Effected by a change in state of muscle
o Muscles = ‘Effectors’

o Motoneurons (MN) cell bodies located

along spinal cord & in brain stem
o Axon goes to to one muscle, and innervates a
number of muscle fibres
o MN + muscle fibres = a ‘motor unit’
o MNs activated by:
o Sensory afferent neurons
o Interneurons
o descending tracts from forebrain &
brainstem
o Alpha motoneurons (AMN)
o Originate in spinal cord, exit via ventral root,
terminate in muscle
Ventral
o The ‘Final common path’ (Sherrington)
o Action potential → acetylcholine
Gazzinga et al, 2009
Spinal Cord

} MNs innervate skeletal muscle

} SC is first/final point for sensorimotor
integration
} Interneurons
} Termination of descending pathways
} Direct/indirect synapses with MNs
 Primary motor cortex (M1)

• Conscious, voluntary movement

• Early stage of learning
• Distal - contralateral
• Proximal – bilateral
 Primary motor cortex (M1)

• M1 - topographical
organisation
• Cortical volume
according to precision,
not (muscle) size
• Homunculus- true only
to a point

305 Movement Neuroscience

Basal Ganglia

}receives inputs from cortex

}sends output to cortex
}no direct sensory inputs
}no direct output to spinal cord
}critical for movement control
(initiation, selection, inhibition)
 Cerebellum
• Inputs from cortex, brain stem, and
spinal cord
• Outputs to spinal cord, motor cortex,
oculomotor nuclei
• Integration
• Comparator
• efference copy from M1
• sensory consequences from periphery
• fine tuning
• Well-learned automatic
movements
Brain Stem

}physiological monitoring
} arousal
}regulates descending
commands
} sensitivity (gain)
The Motor System

cerebral cortex motor areas

Primary motor
Pre motor

thalamus where
what
basal ganglia
when
brain stem
cerebellum

muscle contraction
spinal cord and movement

sensory
receptors
Components of the motor system
(In more detail)
A Minimum Model for
Sensorimotor Integration

1) Sensory receptor
2) Afferent pathway
3) Synapse onto an alpha Motoneuron
4) Neuromuscular junction
Sensorimotor Integration in the
spinal cord
Stretch Reflex
• E.g. tendon tap
• Autogenic
• Monosynaptic

• Muscle spindle
• Ia afferent
• Synapse onto alpha MN
• Acetylcholine release
• Muscle contracts
Sensorimotor integration -
Basic motor patterns
Brainstem – spinal cord o Coordination of basic motor
patterns:
o Brainstem (medulla & midbrain):
o swallowing, chewing, breathing, saccadic
eye movements
o Spinal cord:
o protective reflexes, walking

o Central pattern generators:

o Interneurons activate and inhibit specific
groups of MNs in certain sequence
o Largely self-sustaining – via rhythmic
sensory feedback
 Descending motor pathways
Direct pathways
o Corticobulbar tract
(not shown here) o ff):
o yy
• M1 >> MNs controlling face,
head, neck muscles

o Corticospinal tract
• M1 >> spinal MNs
• Monosynaptic
• 1/3rd M1; 1/3rd PMC/SMA;
1/3rd S1
• “pyramidal decussation”
• lateral - crossed
anterior/ventral - uncrossed
• essential for goal-directed
movement! Cognitive Neuroscience, Gazzinga et al, 2009
 Descending motor pathways
Indirect pathways
o Lateral:
o ff):
• Rubrospinal o yy
• distal musculature

o Medial:
• Tectospinal
• coordination of eye and
head movements
• Vestibulospinal
• balance and posture
• Reticulospinal
• posture and reflex
modulation
Cognitive Neuroscience, Gazzinga et al, 2009
Cortical regions involved in movement

Cerebral cortex

© Cengage Learning
 Parietal and (pre)frontal cortex are
important for motor control
Apraxia
o Loss of the ability to execute or carry out learned purposeful movements
o Common after damage to L hemisphere
o Type of Apraxia depends on exact region - common in frontal & parietal cortices
o Higher order motor deficit:
o Presents bilaterally
o Motor processes in tact

o Common classification:
o Ideomotor apraxia:
o rough sense of desired action
o problem executing it!
o Ideational apraxia:
o cant determine which actions are necessary
o or their order

https://www.youtube.com/watch?v=EvOYeqM-6CE
The supplementary motor complex
(SMC)
o SMA proper, pre-SMA, SEF

o Role in planning, preparing & initiating

movement
o Monkey SMA & SEF neurons active before
movement
o Movement sequencing:
o Monkey SMA & pre-SMA neurons fire
before specific sequence
o Human fMRI – SMC active during tasks
requiring complex motor sequencing

o SMC project to ipsilateral &

contralateral motor cortex, & to the
contralatral SMC
o Bimanual coordination
© Cengage Learning
Concept 4
The neural control of
movement can be understood
as both hierarchical and
parallel
The Motor System

cerebral cortex motor areas

Primary motor
Pre motor

thalamus where
what
basal ganglia
when
brain stem
cerebellum

muscle contraction
spinal cord and movement

sensory
receptors
Hierarchical and Parallel Control
• Hierarchical:
• Spinal Cord -> pattern generation
• Brain Stem -> controller; relay
• Cortex -> controller
• Parallel:
• direct connections between Cx and basal ganglia,
cerebellum, spinal cord
• Direct and indirect connections to MNs
• Redundancy
Inside the brain of an elite athlete: the neural processes that support high achievement in sport.
Yarrow, Brown, Krakauer. Nature Reviews Neuroscience 10:585–596 (2009)
Selection of movement
Planning an action:
o Initial representation = abstract
o Translating goal into movement = competitive process

Competition driven by:

o Internal states & external sources

Cortical selection hypothesis

o All areas promote movement, but relative contribution varies as a function of task demands
o SMA = internal sources
o Lateral premotor cortex = external sources

Activation patterns in motor & premotor cortices:

o Premotor activation generally bilateral, reflects planning?
o Activation becomes lateralised over contralateral motor ctx, outcome of competition?
 Concept
Neurons in primary motor
cortex (M1) code movement
direction
 Primary motor cortex (M1)
o Provides command to drive
motoneurons to make muscles move

o Different subregions control specific

body parts

o Direction a function of summed activity

(vector) across population of neurons

o Debate over what M1 neurons code for:

o trajectory & distance to target?
o sensory motor integration?

o Motor cortex also organised for

ethologically relevant behaviour

http://www.utdallas.edu
Graziano, et al., (2007) Neuron 2:239-251
What aspects of movement does the
brain (M1) encode?
Trajectories
Experiments of Georgopoulos

n animals trained to make

pointing movements

Apparatus
 Cell Firing in Primary Motor Cortex (M1)
nFig 9-18c shows Raster Plots
of ONE M1 neuron taken
from Intracellular recordings 90
(shoulder region)
n5 movements x 8 directions =
40 trials
nNote- its almost always
180
firing. 0

nWhen does firing rate

increase?
nWhen does it decrease?

270
Neurons have a ‘Preferred
Direction’ for maximum firing

Fitted with a cosine curve: firing rate = k cos θ

Neuron Firing Rate and Movement
Direction

nEach neuron represented by a

vector
rate
ng
firi
preferred direction

nVector sum of all cells =

Population Vector
nPopulation Vector specifies
movement direction/goal!
http://motorlab.neurobio.pitt.edu/multimedia.php
http://motorlab.neurobio.pitt.edu/multimedia.php
Summary of M1 Contributions
nMovement direction and trajectories are
encoded by integration of large numbers of M1
neurons

nRedundancy

nBernstein - there can be no unambiguous

relationship between movements and the neural
signals that give rise to them!
The Cerebellum and Basal Ganglia
 FOCUS 1: The cerebellum
o Coordination of movement

o Inputs:
o Mossy fibres
o Climbing fibres

o Ongoing & planned movements

o Interacts with all of cortex

o Adjusts parameters of movement

as a function of success

o Lesion = inaccuracy, instability

Image generated by Life Science Databases(LSDB)
(www.creativecommons.org/licenses/by-sa/2.1/jp/deed.en)
 The cerebellum
Vestibulocerebellum
o Innervated by brainstem vestibular nuclei
o Controls balance, coordination of eye & body movements
o Lesions = affect reflexes essential for balance & stability

Spinocerebellum
o Innervates spinal cord & extrapyramidal system
o Lesions = difficulty with smooth movements, ataxia

Neocerebellum
o Innervated by descending ctx fibres
o Parietal & frontal ctx
o Output via thalamus to:
o M1, Lat PM, PfC
o Lesions = ataxia
The cerebellum

Nature Reviews Neuroscience 2005:6;297-311

 Function of the cerebellum
Prediction:
o Helps to predict sensory consequences of motor plans
o Determine if movement is being performed correctly
o Computes error signal between how well it predicted the
movement & the end result of that movement
o Error signal provides information on how the model can be
changed
o Explain inability to adapt to changing conditions with damage

Timing:
o Provides a clock for the timing of different events
o Information of initiation & cessation of movement for
different effectors
o Explains poor coordination of movements with damage
FOCUS 2 : Basal ganglia

o Collection of interconnected subcortical nuclei

o Interact closely with cerebral cortex, thalamus, & brainstem to

guide behaviour

o Multiple, parallel, largely segregated, cortico-cortical re-

entrant pathways

o Participate in motor, associative, & limbic functions

o Dysfunction associated with movement disorders &

neuropsychiatric disorders
BG neuroanatomy
 BG organisation

Input Cortex

(Glutamatergic): Striatum

• From layer 5 neurons in SNc

cortex (excluding primary
auditory & visual cortex)
GPe
• to striatum (putamen, Thalamus
caudate, nucleus
accumbens – ventral
striatum) STN

• From layer 5 neurons in GPi SNr

motor cortex brainstem / spinal cord PPN/SC

SC
• to STN (from motor cortex)
 BG organisation

Output
Cortex

Striatum
(GABAergic):
SNc
• From:
• GPi & SNr
GPe
• To: Thalamus
• thalamic nuclei which
project to frontal cortex STN
• superior colliculus
• pedunculopontine
nucleus GPi SNr

brainstem / spinal cord PPN/SC

 BG organisation
Cortex
o Internal connections of the
BG contain both direct and
indirect pathways from Striatum

striatum to BG output nuclei

SNc

o Indirect pathway goes via

GPe & STN GPe
Thalamus

STN

GPi SNr

brainstem / spinal cord PPN/SC

SC
BG organisation
Cortex

Direct pathway: Striatum

SNc
• Inhibitory connection from
striatum to GPi/SNr
GPe
Thalamus
• increased activation
reduces tonic inhibition of
thalamus, SC, PPN STN

• results in increased
GPi SNr
facilitation of cortex
brainstem / spinal cord PPN/SC
SC
BG organisation
Cortex

Indirect pathway:
Striatum
• Inhibitory connection from
striatum to GPe
• Inhibitory connection from SNc

GPe to STN, GPi/SNr

• Facilitatory connection from GPe
STN to GPi /SNr Thalamus

• increased activation STN

increases tonic inhibition of
thalamus, SC, PPN

• results in reduced GPi SNr

facilitation of cortex
brainstem / spinal cord PPN/SC
SC
Analogy for how the BG Pathways combine to influence thalamo-cortical projection:
 o Cortex ® striatum ® GP ® thalamus ® cortex
o Indirect pathway can suppress unwanted behaviour
o Direct pathway can facilitate wanted behaviour

o Different aspects of behaviour processed in parallel

o Same principal processing operations
o Parallel circuits
o Limbic
o Prefrontal (associative):
o Dorsolateral prefrontal

o Lateral Orbitofrontal

o Motor
o Sensory

Redgrave P,et al,. 2010. Goal-directed and habitual control in the basal ganglia: implications for Parkinson's
disease. Nature reviews Neuroscience 11:760-772.
Basal Ganglia Dysfunction
o Parkinson’s disease o Drug overdose
o Huntington’s Disease o Head injury
o Tourette Syndrome o Infection
o Hemiballismus o Liver disease
o Multiple Systems Atrophy o Metabolic problems
o Progressive Supranuclear Palsy o Side effects of certain medications
(e.g. haloperidol and risperidone)
o Dystonia
o Stroke
o Tumours
o Environmental toxins
Parkinson’s disease

• Widespread neurodegenerative disorder

• Major pathologic feature – profound loss of pigmented

dopamine neurons, mainly in SNc

• Symptoms appear when DA neuronal death reaches critical

threshold:
• 70-80% striatal nerve terminals
• 50-60% SNc perikarya

• Age of onset varies, normally around 65-70 yrs

Cho et al (2011), Movement Disorders, 26(3):713
Parkinson’s disease

o Main symptoms – tremor, rigidity, motor slowing, postural

instability
o bradykinesia , akinesia, hypokinesia
o stooped posture & impaired balance
o small, shuffling steps, poor arm swing

o Symptoms worse on one side of body

o A positive response to L-DOPA aids the diagnostic process

o Post-mortem analysis has established Parkinson’s as an

⍺-synucleinopathy (abnormal aggregation of this protein)
o No accurate biological marker or radiological imaging technique.
Other (lesser known) symptoms
o REM Sleep behavioural disorder.
o Hyposmia
o Reduced blinking, dysphagia (confusion)
o Speech:
o monotonous pitch, hypophonic (quiet), poorly enunciated (dysarthrophonia),
akinetic with festination
o Depression & anxiety symptoms
o rumination, social avoidance, associated anxiety / tension
o Volitional saccade hypometria - multi-stepping
Risk factors

o Cause is unknown
o Overlapping environmental & genetic factors?
• Exposure to toxic metals
• Bacterial toxins
• Poor diet
• Genetics
BG dysfunction in PD
Cortex

Striatum
D2 D1

SNc

GPe
Thalamus

STN

GPi SNr

PPN/SC PPN/SC
SC
https://www.youtube.com/watch?v=j86omOwx0Hk
 Treatment – 1) Pharmacotherapy

o L-DOPA (L-3,4-dihydroxyphenylalanine) - mainstay of PD

treatment
o reduces tremor, stiffness, & slowness
o improves muscle control, balance, & walking
o does not slow disease process

o “OFF - ON” motor fluctuations

o Following 5-10 years of treatment

o ­ symptoms, ­ fluctuations, ­ dyskinesias
o behavioural /cognitive changes
o primarily medication effect
Treatment – 2) Deep brain stimulation