17-­‐02-­‐18

BPK 415
Neural Control of Movement

Dan Marigold, PhD

Section 4

Locomotion and
Spatial Navigation

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Section Outline
• Gait initiation

• Central pattern generators (CPG)

• Hip proprioception and load information

– Role of sensory feedback in controlling step cycle

• H-reflexes and cutaneous reflexes

• Interlimb co-ordination
• Supraspinal control
– Optic flow and heading direction
– Obstacle avoidance and precision stepping
– Role of motor cortex, PPC, and cerebellum

• Spatial navigation

Section Learning Outcomes

• By the end of this section, you should be able to…

– Describe through the use of specific research examples how the

nervous system initiates and regulates the basic walking pattern
via central pattern generators
– Explain the concepts of phase-, task-, and context-dependent
reflex modulation
– Illustrate how visual, vestibular, and somatosensory systems
contribute to walking
– Describe the contribution of the posterior parietal cortex,
cerebellum, and primary motor cortex in the planning and
execution of gait modifications
– Outline the neural mechanisms allowing for spatial navigation
– Propose experiments to determine the role of sensory feedback
and contribution of select brain areas in the regulation of walking

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Locomotor Step Cycle

Inman et al. 1981

Tresilian 2012

Locomotor Step Cycle: Muscle Activity

Tresilian 2012 Lacquaniti et al. 2012

Arrows departing from the COM denote the resultant module contributions to the
horizontal and vertical ground reaction forces that accelerate the COM providing
body support and forward propulsion. Net energy flow by each module to the trunk
or leg is denoted by a + or – for energy increases or decreases, respectively

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Dynamic Stability
• A primary concern of the CNS is to maintain
dynamic stability during walking
– This feat is particularly challenging on unstable
terrain

• Dynamic stability during walking is the control

of the center of mass within a changing base
of support
– Requires effective proactive and reactive
recovery response strategies when exposed to
perturbations
Patla 2003

Techniques to Study Neural

Control of Stepping/Locomotion
• Perturbation studies
– Loading/unloading
– Stretch/shortening
– Unexpected support removal
– Unstable ground terrain
– Physical contact

• Adaptive locomotion & behavioural studies

– Obstacle avoidance
– Precision stepping tasks
– Split-belt treadmill walking

• Animal studies
– Single-unit recordings
– Various preparations

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Preparations Used to Study Neural

Control of Stepping/Locomotion
• Decorticate
– Cerebral cortex removed and connections to thalamus are severed
– Basal ganglia intact

• Decerebrate
– Pre-mammillary
– Post-mammillary (mesencephalic)

• Spinal
– Acute versus chronic

• Immobilized preparations (fictive locomotion)

– Motor neurons to flexor and extensor muscles fire but no movement
takes place

• Intact cat
– Restrained
– Unrestrained
Kandel et al. 2000

Initiation of Locomotion by
Supraspinal Regions

Kandel et al. 2013

Role of mesencephalic locomotor

region (MLR) Tresilian 2012

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Mesencephalic and Subthalamic

Locomotor Regions
• Stimulation of the MLR and SLR results in
activation of reticulospinal neurons (RS)
– Unilateral stimulation elicits bilateral activity
– Occurs in reduced and intact preparations
– Destruction of one region doesn’t influence ability
of the other region to produce locomotion

• RS pathway is necessary for MLR-evoked

locomotion
– Inactivation by cooling of the medial reticular
formation blocks MLR locomotion

MLR Initiates Locomotion and

Regulates Speed

Tresilian 2012

• Increasing MLR
stimulation results in
increased propulsive
force and transition from
walk à trot à gallop
Orlovsky et al. 1999

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Control of Postural Tone for

Locomotion
• Two brainstem regions located in the pons
involved:
– Dorsal tegmental field (DTF)
• Exerts inhibitory action on muscle tone in all limbs

– Ventral tegmental field (VTF)

• Exerts excitatory action on muscle tone in all limbs

Control of Postural Tone for

Locomotion
• Stimulation of DTF alters
standing postural tone

• Stimulation of DTF during

locomotion terminates the
activity

• Stimulation of VTF during

locomotion enhances
locomotor activity
Orlovsky et al. 1999

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Three Fundamental Principles of

Neural Control of Walking
• #1: Walking utilizes a combination of
feedforward and feedback control

• #2: Feedback control integrates visual,

vestibular, proprioceptive, and cutaneous
information

• #3: Strength and sign of feedback

pathways are task- and phase-dependent
Donelan & Pearson 2004

Three Fundamental Principles of

Neural Control of Walking
• #1: Walking utilizes a combination of
feedforward and feedback control

– Feedback control
• Current state of animal and external environment to modify
muscle activity
• Compensates for perturbations

– Feedforward control
• Modifies muscle activity independent of animals sensed state
• Reduces the effect of a decline in performance when sensory
information is imprecise
• CPG in spinal cord provides this locomotor drive

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Central Pattern Generator (CPG)

• A CPG is a neuronal network
capable of generating a
rhythmic pattern of motor
activity in the absence of
sensory input
– Isolated spinal cord can
generate rhythmic bursts of
reciprocal activity in flexor
and extensor motor neurons

– Two systems mutually inhibit

each other

– Sensory input and

descending commands can
modify basic pattern
produced by CPG
• So in normal situations CPG
doesn’t work alone

Kandel et al. 2000

Central Pattern Generator (CPG)

Kandel et al. 2013

Electrical stimulation of human spinal cord also shows these

patterns (Dimitrijevic et al.. 1998)
Goulding 2009

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Human Epidural Spinal Cord Stimulation

Evokes Rhythmic Muscle Activity

Danner et al. 2015

Proposed Two-level CPG Organization

• MLR initiates locomotion via tonic

excitatory input to rhythm
generator (RG) and pattern
formation (PF) neuronal
populations

• Locomotor rhythm and durations of

flexor and extensor phases are
determined by the RG network

• RG network controls the activity of

the PF network

• PF population activity produces

phase-specific activations of
appropriate groups of synergist
motoneuron pools
– Thus, activating specific muscles

McCrea & Rybak 2008; Rybak et al. 2015

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CPG Functions
• Supplies motoneurons with rhythmical input
– Producing motor pattern of stepping and scratching
• Informs other limb controllers about its activity
– Important for interlimb coordination
• Informs different brain regions about its activity
– Important for descending control/interaction with CPG
• Modulates its own sensitivity to descending
signals
• Modulates the efficiency of transmission of signals
in different spinal pathways in a phase-dependent
manner

Locomotor Modules & Primitives

• Locomotor module
– Functional unit
– In neuronal network of spinal cord (e.g., CPG)
– Produces a specific motor output by imposing spatiotemporal structure
to muscle activations

• Locomotion can be explained by a few basic patterns independent

of mode, direction, speed, and body support

• Locomotor primitives
– Are the basic patterns described above
– Building blocks from which locomotor activities are constructed

• Recent evidence suggests that two basic patterns of stepping

neonates are retained through development, whereby two new
patterns emerge starting in toddlers
– Common pattern observed across species as well
Dominici et al. 2011; Lacquaniti et al. 2012

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Locomotor Primitives and

Development of Walking Patterns
• Compared
locomotor output of:
– Neonates
– Toddlers
– Preschoolers
– Adults
– Even other animals

• Recorded up to 24
muscles using EMG
Dominici et al. 2011

Locomotor Primitives and

Development of Walking Patterns
• 2 patterns found in neonates
• 4 patterns in toddlers, preschoolers, and adults
– 2 patterns in neonates conserved
• As person ages, the peak of the pattern shifts to more adult-like
stepping

Dominici et al. 2011

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Three Fundamental Principles of

Neural Control of Walking
• #2: Feedback control integrates visual,
vestibular, proprioceptive, and cutaneous
information

– Control of the step cycle will be examined first

(based mostly on cat research)
• Hip proprioception and extensor load information

– Then we will look at how sensory feedback is

used to assist in stance phase muscle activity
(based on human research)

Hip Proprioception Helps Trigger

Swing Phase of Locomotion
• Stretch of hip flexor muscle
causes shift to swing phase
(based on muscle spindle input
via Ia afferents)

• Top and middle:

– Oscillate limb to alternate flexion
and extension
– Note EMG activity

• Bottom:
– Sudden stretch of hip flexors (as
would occur during hip extension)
– Note change in EMG activity

Kandel et al. 2013

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Hip Proprioception Helps Trigger

Swing Phase of Locomotion
• Note changes when ipsilateral limb is held
and thus maintaining a relatively constant
hip angle

Extensor
Flexor

Grillner and Rossignol 1978

Entrainment of Locomotor Rhythm

by Ankle Extensor Stretch
• Saw-tooth and ramp-and-hold
stretches showed flexor bursts
after 200 ms following stretch
release
• Same entrainment seen when
electrically stimulate group I
afferents
– Control experiments showed most
likely due to Ib involvement

Pearson et al. 1992

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Extensor Load Information Helps

Maintain Stance Phase of Locomotion

Ib afferents from extensor

muscles respond to load and
enhance extensor muscle activity

Stimulation of Ib afferents
prolongs extensor activity

Whelan et al. 1995 in: Kandel et al. 2013

Extensor Load Information –

Loss of Ground Support

Gorassini et al. 1994

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Extensor Load Information –

Loss of Ground Support
• Peg on walkway suddenly
lowered

• Extensor muscle EMG is

reduced early
– Peg accelerating
downward and thus
reduced GRF

• Increase in extensor
muscle activity later
– Peg decelerating and thus
increased GRF
Donelan and Pearson 2004

Extensor Load Information –

Loss of Ground Support
• Loading ankle
extensor
muscles during
foot-in-hole trials
increases
extensor muscle
activity

Hiebert and Pearson 1999

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Extensor Load Information –

Loss of Ground Support
• Absence of normal load
(signaled via group I
afferents) is responsible
for the corrective
response to a loss of
ground support
– Electrical stimulation of
group I afferents when
paw in hole delays
response
Hiebert et al. 1995

Hip Position and Leg Load –

Infant Stepping Evidence
• Stance phase is
prolonged and swing
phase delayed when
infant hip is flexed and
the load is increased

• Stance phase is
shortened and swing
phase is earlier if hip
is extended and load
is decreased

Pang and Yang 2000

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Ongoing Muscle Activity During

Stance Phase
• Unloading of ankle plantar flexors
– Normal lengthening contraction in plantar
flexors is prevented and thus unloaded

• Reduction in EMG is seen

Sinkjaer et al. 2000

IN: Donelan and Pearson 2004

Ongoing Muscle Activity During

Stance Phase
• Could be stretch in ankle dorsiflexors?
– Control experiments blocking afferent
transmission via lidocaine around CPN
shows no effects

• Could be cutaneous afferents from

perturbation?
– Lidocaine around cutaneous nerves
shows no effects

• Could be group I afferents?

– Ischaemia of leg (cuff above knee)
decreased group I (mainly Ia)
transmission and no effect of decreased
EMG

• Could be group II afferents

– May still be Ib afferents (less sensitive to
ischaemia) but should see increased
EMG in later stance when force increases
– Later work argues more for Ib afferents

Sinkjaer et al. 2000 IN: Nielsen 2002

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Role of Load Feedback in the Ongoing

Muscle Activity During Stance Phase

• Sudden drop in
surface during walking
– I.e., Reduced load

• Decreased soleus muscle activity

• Ankle foot orthosis (AFO) restricting ankle movement

(and hence muscle length properties) had no effect on
the response to the drop in surface in late stance
– Muscle length properties not involved in SOL depression

• Suggests load feedback is important and that group Ib

afferents involved
af Klint et al. 2009

Role of Load or Muscle Length Feedback in the

Ongoing Muscle Activity During Stance Phase

• Altered body-weight support (BWS) to

change load information (5% or 30% body-
weight lifted off ground, which equates to
95% or 70% load on ground, respectively)
• Gave dorsiflexor (eliciting stretch reflex) and
plantarflexor (eliciting unload response)
perturbations when the load was changed

af Klint et al. 2010

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Role of Load or Muscle Length Feedback in the

Ongoing Muscle Activity During Stance Phase
• More weight on ground, greater decrease in EMG
with plantarflexion perturbation
– Magnitude of unload response greater

• Suppression of group II afferents with tizanidine had

no effect on the unload response

• Suggests unload response mainly Ib afferents

• MLR was modulated based on BWS

– MLR decreased with less load applied to ground (i.e., 30%
BWS condition)

• Suppression of group II afferents did, however, effect

the MLR

• Suggests that load/force- (i.e., Ib afferents) related

feedback contributes to both ongoing background
muscle activity and MLR whereas length-related
feedback (group II) contributes to the MLR only
af Klint et al. 2010

New Approach to Recover Voluntary

Control of Locomotion after SCI
• Adult rats received a left lateral • Rats were trained with usual
hemisection at T7 and a right treadmill approach and with new
lateral hemisection at T10 robotic postural interface
(overground training)
• Tonic electrical stimulation of the
spinal cord was applied, along
with serotonin and dopamine
receptor agonists

Van den Brand et al. 2012

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New Approach to Recover Voluntary

Control of Locomotion after SCI
• After training, all rats were able to
initiate full weight-bearing locomotion of
hindlimbs

• However, only rats trained with the

robotic postural interface were able to
initiate locomotion overground

• These rats were also able to go up

stairs and over obstacles after 2-3 more
weeks of training

• Training protocol encouraged animals to

actively initiate locomotion and engage
cortical neurons, and thus promoted
remodeling of descending pathways
Van den Brand et al,
Van den Brand et al. 2012 2012

Brain-spine Interface to Reduce Gait

Deficits after Spinal Cord Injury
• Microelectrode array
implanted into the leg area
of the motor cortex

• Decoded neural activity

and used to drive an
implanted pulse generator
that caused epidural
electrical stimulation to
targeted dorsal roots of the
lumbar spinal cord during
locomotion
Capogrosso et al. 2016

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Brain-spine Interface to Reduce Gait

Deficits after Spinal Cord Injury
• Figure on right:
– Brain-controlled leg flexion and
extension compared to normal
control
– Step height can be controlled based
on brain signals
– Note: this figure shows the results in
an intact monkey

• Figure below:
– Brain control of flexion/extension in
spinal cord injured monkey

Capogrosso et al. 2016

Role of Cutaneous Input in

Controlling Locomotion
• Cutaneous afferents provide valuable information for foot
placement during walking
• Plantar surface provides information on load, facilitates the
control of the centre of pressure, can detect slippage, etc.
• Dorsal surface provides information regarding contact with
obstacles
• Techniques to study the role of cutaneous input
– Denervation
• Lesion of nerve (animal models) or sensory neuropathy (humans)
– Cooling
• Ice bath
– Electrical stimulation
• Train of pulses applied to nerve through skin

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Sources of Cutaneous
Information from the Foot
• Tibial nerve
– Transmits info
from plantar
surface of foot

• Superficial peroneal
nerve
– Transmits info
from dorsal foot
surface

• Sural nerve
– Transmits info Figures from: http://emedicine.medscape.com; WebMD LLC, 2017
from lateral side of
foot

Role of Cutaneous Input in

Precision Walking

• Denervation of cutaneous nerves in hindlimb of cat

– Ladder walking impaired but minimal deficit seen for
normal treadmill locomotion
Bouyer & Rossignol 2003

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Role of Cutaneous Input for Gait

Termination
• Plantar surface of foot
was submersed in ice
water to reduce
cutaneous sensation

• Task was to terminate

gait when cued

• Measured relationship
between centre of
pressure (COP), centre
of mass (COM), and
base of support (BOS)

Perry et al. 2001

Role of Cutaneous Input for Gait

Termination
• Resulted in:
– Increased step length
of second step (A)
– COM closer to BOS (B)
– Increase variability in
step length (C)
– Increase in loading rate
at foot contact (D)

Perry et al. 2001

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Role of Cutaneous Input in

Recovering from Gait Perturbations
• Medial-lateral perturbations
during walking in the cat

• Before and after cutaneous

denervation of the hindlimb

• After denervation, cats made

larger lateral steps and required
greater # of steps to recover

• Muscle responses to
perturbations were reduced in
amplitude

• Suggests role in scaling recovery

responses
Bolton & Misiaszek 2009

Summary of the Effects of Somatosensory

Feedback on Human Muscle Activity
• Group Ia
– Role in SLR
– Important for altering muscle activity in response to small variations in
ground conditions

• Group Ib
– Positive force feedback during walking (i.e., load-related) à ongoing
muscle activity
– Converges with group II afferents to contribute to MLR

• Group II
– Major contributor to the MLR
– Likely also plays some role in positive force feedback

• Cutaneous afferents (groups I, II, and III)

– Load-related information
– Detection of COP and BOS
– Role in triggering response to trips
– Role in scaling recovery responses

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Local Spinal Circuitry Summary

Rossignol et al. 2006

Role of Vestibular System in

Controlling Locomotion
• APA = anticipatory
postural adjustment
• TO = toe-off
• HC = heel contact

• GVS used to stimulate

vestibular system

• Head roll increases as

task transitions into
dynamic phase and
remains equal
throughout gait cycle

Bent et al. 2005

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Role of Vestibular System in

Controlling Locomotion
• Differences in
vestibular
contribution between
upper and lower limb

• Lower limb changes

reflected by
modifications in M-L
foot placement
– Phase-dependent
modulation seen
with greatest
contribution at HC

Bent et al. 2005

Role of Vestibular System in

Controlling Locomotion
• GVS applied during walking with eyes
closed

• Note staggered foot placement on left

(to side of anode)
– Balance responses show large trunk tilt

• Note deviation of trajectory on right

(towards anode)
– No balance responses seen

• These balance and orientation

responses depend on head position
during the GVS walking

St. George and Fitzpatrick 2011

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1b afferents come on
during walking during
Three Fundamental Principles of the swing phase will
have enhanced activity.
Neural Control of Walking During the stance phase,
1b afferents have an
• #3: Strength and sign of opposite, inhibitory
feedback pathways are task- effect.
and phase-dependent Depending on the task,
the nervous system will
– Task-dependent activity either activate or
• Reflexes (e.g., cutaneous & H-
reflexes) suppress activity.
• Force-sensitive afferents that Depending on the phase
facilitate increase in extensor activity of the swing cycle, you
during walking have opposite effect
during standing get feedback that has a
different effect on
– Phase-dependent activity muscle activity.
• H-reflex (Capaday & Stein 1986)
• Cutaneous reflexes (Zehr & Stein 1999)
• This relates to CPG Kandel et al. 2013

These two graphs show

the exact same thing The
H-reflex Modulation figure on the left shows
the H reflex on the 3rd
(Phase-dependent) one down. On the right
it's the 4th one down.
• H-reflex greatest during The right graph show the
late stance phase hip and knee angle.
What you're seeing here
is the TA activity, but
• H-reflex the H reflex is done off
the soleus muscle.
smallest If you look at the figure
during swing on the left and r9ght,
what you can see is that
phase the H reflex is greatest
during the late stance
phase. This facilitates
plantar flexion for the to
off phase. During swing
Capaday and Stein 1986 Rossignol et al. 2006
phase, do you want a
plantar flexion? NO
H reflex is least sensitive
during swing phase to
ensure plantar flexion
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doesn't happen.
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The larger the slope

Y intercept of the
the more sensitive the
relationship. The Y
intercept is going to be circuit is. Walking, the
0. Duirng the walking H-Reflex Modulation slope is largest, as you
have to accommodate
task. At this condition
this is swing phase. As
(Task-dependent) changes in the terrain.
This allows for greater
you go into stance • H-reflex amplitude is
modulated based on task (see compensatory
phase, and the muscle
figure on right) responses for irregular
acitiyt in th esoleus
– Standing condition – maintained terrain. The sensitivity
increases, you go into a contractions of various levels of the h reflex changes
larger H reflex. In a – Larger slope = higher reflex
standing case, you have from standing to
sensitivity walking to running.
minimal muscle activity – Y-intercept differences too The H reflex si reduced
in your legs. Any
walking on a balance
stretch of the muscle is
beam.
going to have a large • H-reflex is reduced by ~40% H reflex is reduced in
repsonse. The swaying during walking on beam
compared to walking on the running because there
of the stance phase will
ground (Llewellyn et al. 1990) is less contact with the
cause a small stretch
with a large muscle ground as there is less
toe off.
response to counter the Stein and Capaday 1988
sway.

Local sign means each

nerve has a different These grpahs show a
rrefelxive response for a Cutaneous Reflex Modulation stimulated trial vs a
non-stimulated trial
given phase. Right
figure shows 4 muscles (Phase-dependent) such that a positive
number means
in the leg. IIn each
panel, you have the Local Sign activation and a
cutaneous reflex negative number means
response when you inhibition. If you
stimulate the superficial, stimulate the nerve
sural, and TA nerve. during stance phase,
What you see, you get no response. If
dpeneidng on the nerve you stimulate during
you stimulate, you'll get swing phase, you get a
a different response. respnose. If you
Phase dependency: 16 stimulate in the swing
phase step cycle: they're to stance transition, you
depicting stance phase get a suppressed
and swing phase. From response. This prevents
phase 1-9 is stance a large dorsiflexion
phase, and after that is Zehr and Stein 1999 Van Wezel et al. 1997 action during a normal
swing phase. landing of the foot.

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How cutaneous
amplitude is modified
for a placement
precision task. See how
Cutaneous Reflex Modulation gait is changed for
(Task- or Context-dependent)
Ladder Experiment
Ladder Condition visual input of the task.
Walk on the rungs of a
horizontal ladder.
• Modification of cutaneous reflex gain when foot
71 cm

Raised vs flat rungs and

Stimulation Range:
Right Toe-off to Right Toe-off 122 cm

placement precision is increased and/or there

3.5 cm

Overground Condition
10 cm

small vs large rungs.

are changes in ground terrain What happened?
Stimulation Range:
Right Toe-off to Right Toe-off

Ladder Experiment
Stepping Stone Experiment
Ladder Condition Narrow Target Condition

71 cm
71 cm

Stimulation Range: Stimulation Range: 30 cm

Right Toe-off to Right Toe-off 122 cm Right Toe-off to Right Toe-off

3.5 cm 10 cm

10 cm
Large Target Condition
Overground Condition

65 cm
15 cm
Stimulation Range:
Stimulation Range: Right Toe-off to Right Toe-off 30 cm
Right Toe-off to Right Toe-off

Stepping Stone Experiment

Narrow Target Condition

Ruff, Miller, Delva,Figure

Lajoie,
1 & Marigold 2014

71 cm

Stimulation Range: 30 cm
Right Toe-off to Right Toe-off

10 cm
Large Target Condition

I will not ask you to If you have an

memorize this figure, unexptected contact
Cutaneous Reflex Modulation on (cutaneous feedback),
65 cm

just understand the

15 cm
Stimulation Range:
Right Toe-off to Right Toe-off 30 cm

summary. Just look at you will have a differnt

the black bars (high the Basis of Visual Feedback Figure 1
respnse in order to
precision condition) and A
Tibial Nerve Stimulation - Ladder Experiment
B A
Tibial Nerve Stimulation - Stepping Stone Experiment
B
maintian your position.
1.4
iTA 1.4 iMG iTA iMG * *

grey bars are low

1.2 1.2 + +
1.2 1.2 1.0 * * 1.0 +
+ + +
1.0 1.0 * 0.8
Normalized EMG Amplitude

Normalized EMG Amplitude

0.8
Normalized EMG Amplitude

+
Normalized EMG Amplitude

* * *

precision conditions.
0.8 * + 0.8 * 0.6 0.6
+ + + +
0.6 * 0.6 0.4 0.4
* + +
0.4 + 0.4 0.2 0.2
+

The amplitude of these

0.2 0.2 0 0

0 0 -0.2 -0.2

-0.2 1 2 3 4 5 6 7 8 9 10 -0.2 -0.4 -0.4

bars were modified -0.4

-0.6
iSwing

Phase (Bin #)
iStance
-0.4

-0.6
1 2 3 4 5

Phase (Bin #)
6 7 8 9 10 -0.6

-0.8
1 2 3
iSwing
4 5 6

Phase (Bin #)
7

iStance
8 9 10 -0.6

-0.8
1 2 3 4 5

Phase (Bin #)
6 7 8 9 10

during a very narrow

Ladder (Reflex / Background) * = Ladder vs. overground: Reflex (p<0.05) Narrow Targets (Reflex / Background) * = Narrow vs. large targets: Reflex (p<0.05)
Overground (Reflex / Background) + = Ladder vs. overground: Background EMG (p<0.05) Large Targets (Reflex / Background) + = Narrow vs. large targets: Background EMG (p<0.05)

C C D

range, like in late swing

phase of the limb. In
this phase, you are
precisely guiding your
foot to the surface, and
this is where the
nervous system uses
cutaneous feedback the • Change in reflex amplitude during late swing phase (when precision paramount)
most. Ruff, Miller, Delva, Lajoie, & Marigold 2014

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Summary slide. Use this During the stance phase,

to study and help with Functional Reflexes cutaneous informatino
is providing ystability.
the integrative question.
Swing phase, stance (or Functional Responses) During the STS, the
muslces are involved in
phase. During swing
phase, there unloading and the
is a response called cutaneous input is
stumble correction involved in withdrawal
(you've hit something, of the surface
dumb dumb). During
swing phase, muslce
feedback is being
used to stabilize the
limb. During the S-T-S
transition: lowering
strategy (fall with style).

Zehr and Stein 1999

arm swing plays a role

in walking. There are
proposed CPG circuits
Interlimb Co-ordination for each one of our
limbs. Each CPG is
connected to the other in
• Interlimb coordination order to facilitate
(maintenance of reciprocal, communication and
out of phase motions of the movement. THe blue
errors represent
limbs) is critical for stable descending
walking modifications. The red
arrows are propriospinal
pathways.
• Different forms of interlimb
coordination are used for
various forms of locomotion
(walking, running, swimming)
Marigold & Misiaszek 2009

31  
 17-­‐02-­‐18  

Big fancy complicated

slides to stay a simple
point.
Neural Coupling between Upper & Lower If you stimulate
electrically in the foot,
Limbs – Interlimb Co-ordination or stimulate in the arm,
you get responses from
ALL the limbs,
suggesting there must be
this communication
circuit.

Zehr 2001; Haridas & Zehr 2003

Bilateral coordination. If you shift belt speed,

How CPG's work. How
we can use this Interlimb Coordination: what happens is you see
this large asymmetrical
techniqe for rehab
purposes. Split-belt Treadmill Walking walking pattern, then a
gradual adaptation, then
You can set the speeds • Treadmill belts able to run at different they tie the belts back
of each leg speeds
to the same speeds and
independently. This • Must couple lower limbs according to you see this after effect
creates an initial limb, different belt speeds
in the opposite direction
which you recover § People react to the speed
from, and then develop perturbations by scaling the stance
and swing times of each leg
an after-effect if you independently to maintain an
match both belt speeds. alternating walk pattern

§ Interlimb parameters gradually adapt

during split-belt walking and parallel
the behavioral observations:
§ Limp in early adaptation,
§ Reduced limp in late adaptation,
§ Opposite limp post-adaptation (after
training)

Malone and Bastian 2010

32  
 17-­‐02-­‐18  

Then they jumped on the

Understand direction
bi-speed treadmill.
dependent storage. How
You can see they are
people adapt, and what Interlimb Coordination: Split-belt relatively symmetrical
we can infer from CPG
control. Locomotion (Direction-dependent Storage) during forwards in
backwards. When we
Forward, backward, and
• Split-belt manipulate speed you
variable speed
– Forward walking see a large change in
condition. Look at the – Backward walking symmetry. Early on they
bottom row. What – Baseline: tied belts are asymmetric, and
they're measuring is – Adaptation: one limb then they adapt. Then
phase ( the relationship faster than other (2:1
ratio) they walk backwards
between the 2 lgs).
and they're symmetrical.
Point 5 phase represents • Measured phase Then they walk
perfect symmetry. The relationship between
legs forwards again and
green represents
there's an aftereffect
backwards, the blue • Aftereffects indicate that's opposite to their
represents forwards. storage of adaptation
adaptation. It's direction
Group walks backwards
• Walking directions adapt specific (this only
for 2 minutes, then separately and don’t occurs in the forward
forward for 2 minutes. interfere with each other
Choi and Bastian 2007 moving condition).

There is a CPG involved in forward walking, and theres a different circuit in backwards walking

HYBRID WALKING -
Interlimb Coordination: Split-belt ONE BELT MOVES
FORWARD, ONE
Locomotion (Limb-specific Storage) BELT MOVES
• Hybrid walking (HW): one leg forward, one leg backward (-1:1 BACKWARDS! What
ratio) they found an after
• Adaptation in hybrid walking (-1:2 ratio) effect for the forward
• Aftereffect seen in leg moving forward (for FW tied belts) and walking, and an after
leg moving backward (for BW tied belts) effect for the backward
walking for each leg
during the hybrid
condition. THIS
MEANS THERE IS A
SEPARATE CPG FOR
EACH LEG THAT
REMEMBERS THE
ADAPTATION.

Choi and Bastian 2007

33  
 17-­‐02-­‐18  

Adaptation and Transfer of

Learning in Stroke Rehabilitation
• People with stroke can
adapt to split-belt
locomotion
• The ability transfers to
overground walking
– Step length and double
support measures

Reisman et al. 2009

‘‘…vision evolved in animals, not to enable them to

‘see’ the world, but to guide their movements
through it.’’ (pg. 183, Goodale & Humphrey 1998)

Visual Input Regarding the

Environment is Critical for Movement

34  
 17-­‐02-­‐18  

How is Vision Used During Walking?

• Vision plays an essential role in guiding locomotion
– Implementing avoidance strategies
– Accommodating different ground terrain
– Navigation

• Many details are captured and processed by the visual system as

we move in our environment including:
– Layout of the environment
– Identification and characteristics of objects and surfaces
– Self-motion information

• Vision is able to provide necessary information for successful

locomotion at a distance
• Vision provides information about the body relative to the
environment (i.e., visual exproprioception)
• Vision also affords information on environmental characteristics
such as obstacle height (i.e., visual exteroception)

Studying Visuomotor Control

During Walking
• Optic flow and heading direction

• Precision stepping tasks

– Irregularly spaced targets
– Horizontal ladder

• Obstacle avoidance
– Stationary obstacles to avoid (i.e., step over)
– Moving obstacles to avoid

• Deficits associated with visual impairment

– Simulated
– Actual

35  
 17-­‐02-­‐18  

relative optic flow values of

greater than one give the
ipresson of moving faster
Optic Flow and Locomotion through their environment
and so they slow down.

• Walking velocity
(WV) is regulated
by relative optic flow
(rOF)

• Note that they are

inversely related
Prokop et al. 1997
– E.g. rOF > 1 means
subjects have
impression of being
propelled faster than
normal (and thus
slow down)

The way we visually sampe

the worl d dpeends on the
When is Vision Information Used environmeent and the task
we're doing. People tend to
During Walking? look one to two steps in
advance. If it's the hallway,
• Visual sampling depends on environment and people will look far ahead. If
the hallway is cluttered with
task bullshit, you will be fixating
at the ground.
Feedback from vision plans a
• People fixate ~1-2 steps ahead on task- feedforward movement.
relevant features under demanding situations
and when foot placement is constrained

• Thus, vision may be used in a feedforward

manner

Hollands and Marple-Horvat 2001; Marigold and Patla 2007; Patla 1997; Patla and Vickers 2003

36  
 17-­‐02-­‐18  

Study with LCD goggles:

They could go opaque or
translucent. What
When is Vision Information Used experimenters did was give
control to the subject.
During Walking? They could turn the
goggles translucent at will.
• Intermittent visual sampling So the question was how
much time to people need
paradigm to sample a task? Visual
– Subject-controlled sampling with sampling is used about
LCD goggles 30% of the time when
environment is more
difficult.
• Visual sampling of the
environment with no visually
demanding requirement
– 10% of travel time

• Visual sampling when foot

placement is constrained
– 30% of travel time
Patla 1997

you look at the obstacle

during your approach phase.
When is Vision Used? Visual Sampling When you actually step over
the obstacle, you have no
During Obstacle Avoidance fixations.

• Gaze fixations
made to obstacle
during approach
phase

• Essentially no
fixations made to
obstacle during
step over obstacle
phase

• Travel gaze Patla and Vickers 1997

fixations are
common
Obstacle height varied from 1 to 30 cm

37  
 17-­‐02-­‐18  

When is Vision Information Used?

Precision Walking When pick a target with our
ipsilateral foot when our
contralateral foot is planted.
• Walking across irregularly-spaced
stepping stones
– 68% of saccades made to next footfall target
(i.e., target acquired) while the stepping foot
was still in contact with ground (i.e., end of
stance phase)

– Remaining saccades completed in 1st 300 ms

of swing phase
Hollands et al. 1995

targets are LED lights that lit

When is Vision Information Used? up and denoted where to step.
Even in the dark, they were
Precision Walking wable to accurately step on
the target despite not seeing
their limbs. Target location
• Walking across irregularly-spaced stepping stones alone is enough to guide limb
without ambient lighting (LEDs as targets) movement.
– Intermittent visual denial of targets resulted in increased
stance duration (only sometimes)
– Saccades still made in dark

• Target location alone is sufficient to guide eye/limb

movements

• Continual on-line visual information not necessary

(argues for feedforward control)

• However, many others argue for importance of on-line

guidance (see upcoming slides)
Hollands and Marple-Horvat 1996

38  
 17-­‐02-­‐18  

In order to guide that left leg

to the target, i can use two
When is Vision Information Used things.
During Walking? In order to use that visual
feedbac in a feedborward
manner, I need to get that
• Gathering visual info to allow me to adjust.
information by mid-
stance of the previous
single-support phase
allows person to:
– Modify the mechanics of
the body to step to the
target in a way that is
most energetically
efficient

• Can alter push-off force

and/or change position
of plant leg to re-direct
COM and lower limb
Matthis et al. 2015

As soon as the foot is off the

On-line (Feedback) Control of ground, they remove vision

and so they don't see step off
or swing phase.
Stepping
• Rapid step to a target

• Vision either available

or removed at foot lift-
off

• Notice variability of the

foot placement
Reynolds and Day 2005

39  
 17-­‐02-­‐18  

Goggles that blocked

their lower visual field.
Peripheral Visual Cues and On-line They would need to pitch
Control on Multi-surface Terrain their head down to see
their visual field.
So THEY DID!
WOW! SCIENCE!
Older adults had to pitch
their head more than
young adults.
This is evidence that says
we use peripheral vision
ot perform the task.

Marigold and Patla 2008, In: Marigold 2008

Its hard to see where they've

position the foot in this
obstacle. If you don't step on
Peripheral Visual Cues During the obstacle in the
apporopritate spot they will
Obstacle Avoidance trip. They're usin g
peripheral vision durin ght e
movement online and in the
• Lower visual field feedforward manner.
(LVF) was blocked To put this into context, if
with goggles anyone has done their own
laundry, you have to see
around your giant ass laudry
• Toe clearance, toe basket when walking down
clearance variability, the stairs. You have a higher
and position of foot incidence of falling with
before obstacle bifocals on, so have a pair of
showed main effects r eading glasses instead.
We use a combinatino of
of vision Patla 1998 central and peripheral visual
– With goggles cues.
measures were all What are the implications of the use of
increased peripheral visual cues from the lower
visual field for older adults?

40  
 17-­‐02-­‐18  

When is Vision Information Used During

Walking? Summary
• As the terrain becomes more challenging and the environment
more cluttered, people fixate closer to where they are about to
step

• There might be a critical phase when visual information about

an upcoming foot placement is essential
– After this period, continual visual input may not be needed
– In other words, the step itself may be ballistic

• However, peripheral visual cues (from the lower and upper

visual field, depending on the point of fixation) are normally
used to monitor leg trajectory, foot placement accuracy, and
changes in the environment that dictate sudden gait
modifications (or corrections)

Macular degeneration. More

people have AMD than AD,
PD, and MS combined.

Visual Impairments
• Age-related macular degeneration (AMD)
– Loss of central visual field due to damage of the
macula
– A leading cause of blindness in Western society
(CNIB 2010)

• Cataracts
– Clouding of the eye’s lens that impairs the
passage of light
– Very treatable through surgery

• Glaucoma
– Loss of peripheral visual field due to a collection
of conditions resulting in damage to the optic
nerve
– ~60 million people thought to have glaucoma
worldwide (Quigley & Broman 2006)

• Retinitis pigmentosa (RP)

– Loss of peripheral vision
– Due to progressive degeneration of the retina

41  
 17-­‐02-­‐18  

Different degrees of these

impairement but you have
Symptoms of Visual Impairment decreased contrast sesnitivity
and visual acuity.

• Visual field loss

• Decreased visual acuity

• Reduced contrast sensitivity

• Reduced motion sensitivity

• Falls and collisions with

objects are a major problem
for those with visual
impairment

Brabyn et al. 2004

curve negotiation task.

Effects of Ambient Lighting and Macular Manipulated the lighting
Degeneration on Curb Negotiation and conditino. Dont worry about
lux. 0.7 lux is a moonlit
Precision Walking night.
• Goals: Switched lighting rapidly
– To guide environmental design
• Hospitals, community centres, long-term care centres
– To develop mobility measures suitable to determine the
effectiveness of future drug interventions or mobility aid devices to
treat or combat AMD

• Two mobility tasks:

– Curb negotiation (ascent and descent)
– Precision walking
• Controlling foot placement accuracy to step on irregularly spaced targets

• Three lighting conditions:

– Normal (600 lux)
– Dim (0.7 lux)
– Sudden reduction (600 to 0.7 lux)
Alexander, Lajoie, Neima, Strath, Robinovitch, & Marigold 2014a,b

42  
 17-­‐02-­‐18  

Both groups were affected

by the lighting. In the norla
lighting conditino there is no
Effects of Ambient Lighting and Macular difference between the tow
groups. What we started to
Degeneration on Curb Negotiation notice are differerences
where we dim the lights.
The dim condition ws a
situation was they sat in the
dark for adaptation. There
was also a sudden light
switch.
Some MD pateints take
several minutes before they
start and when they do they
shuffle.
• Both groups were affected by
changes in ambient lighting when
negotiating the curb

• Striking changes were observed in

the condition with a sudden
reduction in light

Alexander, Lajoie, Neima, Strath, Robinovitch, & Marigold 2014

The exapme esubject is

nowhere near the targets
Impact of Ambient Lighting and Macular Degeneration The accuracy severely
on the Ability to Control Foot Placement decreased.
One more application before
we move on. PD disease
• Performance patients have trouble
walking.
worse with
reduced lighting
– Primarily in older
adults with AMD

Alexander, Lajoie, Neima, Strath, Robinovitch, & Marigold 2014.

43  
 17-­‐02-­‐18  

Just having the laser light no

longer help PD patients with
Using Visual Cues to Help in PD their walking. Because there
are proprioceptive deficits,
Rehabilitation visual feedback is critical for
accomplishing this step.
• Recall bradykinesia with PD Visual and auditory cues help
parkinsons patients regulate
– Shuffling gait and shorter step length walking.
• Increased risk of falls

• Lines on ground improve walking in PD

– Targets to step onto
– Increased optic flow information

• However, effect most prevalent when vision

of lower limb is also available
Lebold and Almeida 2011

Supraspinal Control of Locomotion

• Visual input is processed in visual cortex

• Visual information is sent to PPC, which integrates it with other

incoming sensory information regarding body position, etc.
– This signal must be sent to motor areas to execute desired movement

• Key brain regions involved in visually guided walking

– Extrastriate visual areas (e.g., MST)

– Posterior parietal cortex (PPC)

– Cerebellum

– Motor cortex (M1)

44  
 17-­‐02-­‐18  

PPC Neurons Contribute to Planning As it sounds, the ramp up

of action potentials occurs
of Gait Modifications before the cat steps over
obstacles. We know the
• Some PPC neurons vast majority of these
discharge 1 – 3 steps in neurons are not related to
advance of the step over In: Kandel et al. 2013
muscle activity.
an approaching obstacle
– Activity of the majority of
these neurons does not These neural firing does not
correlate with muscle correlate with size/shape of
activity or obstacle size the postion, but the relation
between the two.
• Other PPC neurons discharge
when an obstacle passes
between the forelimbs and
hindlimbs

• Lesions disrupt paw placement

and lead to collisions

Top right. Top two

forelimbs, bot two
The figure on the left is hindlimbs.
Greatest firing at first limb
showing you how cats Planning & PPC Neurons: Estimating steps over the obstacle.
perform in the dark. They
adapt to the dark the same Obstacle Position Relative to Body/limb State Then second forelimb goes
rate we do. a 900 ms period to over. Stutter step at
adapt is not enough time for hindlimbs. Then hindlimbs
cats or humans. In over 50% step over. The number
of the neurons in this regin, green number show the
they maintain their discharge order which the legs step
activity while occluded. If over the obstacle.
these neurons were being
guided strcitly by visual info, Forelimb
then knocking out the vision Forelimb
• Discharge in ~50% of step-advanced PPC extra step from back legs
would cause these neurons to
neurons was unaffected by visual occlusion Hindlimb
be inhibted. There is some • Role in high-order planning
higher order planning or Hindlimb
proprioception going on. • Discharge of PPC neurons that are active
When the object is between when obstacle is between fore- & hind-
the forellimb/backlimb, the limbs is modified when order of stepping
neurons fire most. They limbs changes
• Signal related to estimating obstacle
encode the relationship
position relative to body/limb state
between the cat and the
obstacle.

45  
 17-­‐02-­‐18  

Cat still has to coordinate

the hindlimbs once both
PPC & Maintaining Internal Representation it's forelimbs cross.
Stutter step?
(or Memory) of Obstacle-Body Relationship

Role of Cerebellum
in Walking
• Cerebellar neurons are active during ladder
walking in cats (Marple-Horvat & Criado 1999)
– Active at different phases of step cycle
– Lateral cerebellar neurons respond to flash of
visual stimulus, ladder rung movement, saccade-
related activity (Marple-Horvat et al. 1998)
• Suggests role in visually guided walking

• Cerebellar lesions result in ataxia

• Majority of dorsal spinocerebellar tract

neurons discharge during both ipsilateral and
contralateral limb movements (Poppele et al. 2003)
– Encode orientation angle of the limb axis and limb
load during active treadmill walking (Bosco et al. 2006)

• Ventral spinocerebellar tract neurons signal

info related to CPG, and receive signals from
reticulospinal tract neurons (Hammar et al. 2011)

Kiehn and Dougherty 2013

46  
 17-­‐02-­‐18  

Role of Motor Cortex During

Visually-guided Locomotion
• Inactivation of small
regions of the motor
cortex with the GABA
agonist, muscimol, results
in changes in the limb
trajectory so that cats hit
an obstacle instead of
stepping over it as they
do normally
• Lesions to corticospinal
tract also result in
difficulties
Drew et al. 1996

Role of Motor Cortex in

Locomotion
• Primary motor cortex
neurons increase
activity during a step
over an obstacle
– Associated with
enhanced activity in
muscles

Drew 1988 in: Kandel et al. 2013

47  
 17-­‐02-­‐18  

Role of Motor Cortex during

Locomotion
• MC neurons discharge during visually-guided walking

Beloozerova and Sirota 1993

Motor Cortex Neurons are Particularly

Active During Gait Modifications
• Different cells in the MC
discharge at different
times during the gait
modification and control
different groups of
muscles

• Discharge is like a
sequence of muscle
activation as movement
unfolds to guide limb over
obstacle
Drew et al. 1996

48  
 17-­‐02-­‐18  

Motor Cortex Neurons are Particularly

Active During Gait Modifications

Drew et al. 1996

• Discharge related to controlling timing and amplitude of

muscle activity for stepping over the obstacle
• Shape of obstacle dictates MC neuron discharge
– What does this mean?

Cortical Control Summary

Drew and Marigold 2015

49  
 17-­‐02-­‐18  

Dorsal Visual Stream and Movement

• Composed of three separate visual
pathways:
– Parieto-prefrontal pathway
• Involved in spatial working memory
• Involved in the control of eye
movements

– Parieto-premotor pathway
• Involved in visually guided action
• Subregions maintain the continuously
aligned representations of visual
coordinates relative to the location of
body parts that are necessary for
visually guided action in peripersonal
space

– Parieto-medial temporal pathway

• Involved in spatial navigation
Kravitz et al. 2011

These regions have neurons

that seem to discharge in
particularr places and
Parieto-medial Temporal Pathway regions. Discharge at an initla
posiotn based on their
rleevant during the starting
• Some medial parietal region neurons position.
(such as precuneus, PCC, RSC) Posterior cingulate cortex _
show place/route-selective responses again the nurons resond to
(Sato et al. 2010)
– Neurons show varying responses stimulation/learning.
based on starting position or
destination in a virtual maze
navigation task in monkeys
• Discharge can vary based on context of
the environment

• Posterior cingulate cortex (PCC)

– In monkeys, neurons respond to
particular places
– Inactivation can lead to deficits in
following previously learned routes
– In humans, active in simulated optic
flow environments that mimic walking
forward
Kravitz et al. 2011

50  
 17-­‐02-­‐18  

Parieto-medial Temporal Pathway: PCC

There are preferences in
• Monkeys fixated the centre of the screen, allocentric vs
after which a target appeared in one of egocentric
ten positions across the upper visual field
– After a delay, the central fixation cross
disappeared and monkeys made an eye
movement to the target

• To determine whether a neuron encoded

the position of the target in allocentric or
egocentric coordinates, monkeys’ heads
were rotated
– What does this do?

• PCC neuron encoding shown in bottom

panel

Kravitz et al. 2011

Lesions in the retrosplenial

cortex, you have this
topogrpahic disorientation.
Parieto-medial Temporal Pathway: RSC These patients can recognize
landmarks, but they cannot
use those landmarks to get
• Retrosplenial cortex (RSC) home. Some patients can
– Involved in coordinating and translating between draw detailed maps of these
egocentric and allocentric reference frames (with PCC?), environments.
enabling individuals to orient themselves with respect to
their environment

– RSC lesions lead to heading disorientation, a form of

topographic disorientation in which patients are unable to
orient themselves with respect to landmarks in the
environment
• These patients are able to recognize landmarks, but cannot
extract directional information from them (for example, turn right
at the light)
• In some cases, patients can draw detailed maps of familiar
locations, but still cannot describe routes through those maps
Kravitz et al. 2011

51  
 17-­‐02-­‐18  

PPC is egocentric. RSC is

allocentric.

Parieto-medial Temporal Pathway: RSC

• Patients with lesions of the RSC were tested

for their ability to coordinate allocentric and
egocentric representations

• Patients placed in the middle of a 3 x 3 grid

with three objects arrayed around them
– After a study period, the patients closed their
eyes, the objects were removed and the
patients then had to recreate the array
(middle panel)

– When patients were rotated before recreating

the array, their performance was significantly
impaired compared with the control situation
(bottom panel)

• What does this suggest about role of RSC?

Kravitz et al. 2011

Testing for Navigation Cells

The Nobel Prize in Physiology or Medicine 2014

John O’Keefe discovered, in 1971, that certain nerve cells ‘Firing Field’
in the brain were activated when a rat assumed a particular
place in the environment. Other nerve cells were activated at
other places. He proposed that these “place cells” build up
Map
an inner map of the environment. Place cells are located in a
part of the brain called the hippocampus.

Fig. 1

May-Britt och Edvard I. Moser discovered in 2005 that other nerve cells in
a nearby part of the brain, the entorhinal cortex, were activated when the rat
passed certain locations. Together, these locations formed a hexagonal grid,
each “grid cell” reacting in a unique spatial pattern. Collectively, these grid cells
form a coordinate system that allows for spatial navigation.
Fig. 2

Grid cells, together with other cells in the entorhinal cortex that recognize the
direction of the head of the animal and the border of the room, form networks with
the place cells in the hippocampus. This circuitry constitutes a comprehensive
positioning system, an inner GPS, in the brain. The positioning system in the
In: Kandel et al. 2013; www.nobelprize.org
Fig. 3
human brain appears to have similar components as those of the rat brain.

© 2014 The Nobel Committee for Physiology or Medicine Illustration and layout: Mattias Karlén
The Nobel Prize® and the Nobel Prize® medal design mark are registered trademarks of the Nobel Foundation

52  
 The Nobel Prize in Physiology or Medicine 2014 17-­‐02-­‐18  

John O’Keefe discovered, in 1971, that certain nerve cells

in the brain were activated when a rat assumed a particular
place in the environment. Other nerve cells were activated at
other places. He proposed that these “place cells” build up
an inner map of the environment. Place cells are located in a
part of the brain called the hippocampus.

Neurons in the Brain Associated Fig. 1

with Spatial Navigation

May-Britt och Edvard I. Moser discovered in 2005 that other nerve cells in
a nearby part of the brain, the entorhinal cortex, were activated when the rat
passed certain locations. Together, these locations formed a hexagonal grid,
Place Cell each “grid cell” reacting in a unique spatial pattern. Collectively, these grid cells
form a coordinate system that allows for spatial navigation. Grid Cell Fig. 2

Grid cells, together with other cells in the entorhinal cortex that recognize the
direction of the head of the animal and the border of the room, form networks with
the place cells in the hippocampus. This circuitry constitutes a comprehensive
positioning system, an inner GPS, in the brain. The positioning system in the
Fig. 3
human brain appears to have similar components as those of the rat brain.

© 2014 The Nobel Committee for Physiology or Medicine Illustration and layout: Mattias Karlén
The Nobel Prize® and the Nobel Prize® medal design mark are registered trademarks of the Nobel Foundation

Head-direction Cell Boundary Vector Cell

Hartley et al. 2014; Burgess 2014; www.nobelprize.org

Place and Grid Cells –

Basis for Cognitive Map

Place Cell Grid Cell

- Cells in brain that become - Cells in brain that are active in
active whenever the animal is many different parts of the
in, or transits through, a certain environment
part of the environment - Active areas form a grid pattern
- Located in hippocampus - Located in entorhinal cortex
Moser et al. 2008

53  
 17-­‐02-­‐18  

Place Cell Properties

Nakazawa et al. 2004

• Cognitive map: place cells

maintain an up-to-date
representation of space and the
animal’s location in that space

• Place fields expand, maintain a

relationship to environment
boundaries, and are anchored to
environmental visual cues
Bush et al. 2014

Theta Phase Precession & Place Cells

• Theta phase precession
– Ongoing theta rhythm of LFP
– When animal moves through
firing field, the place cell
discharges short bursts whose
phase relative to theta rhythm
shifts systematically from later
to earlier phases (Jeewajee et al. 2014)

• Time of firing and firing rate are

dissociable, and can represent
two independent variables:
– Respectively:
• Animal’s location within the
place field
• Its speed of movement through
the field

Huxter et al. 2003

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 17-­‐02-­‐18  

Theta Phase Precession & Place Cells

• Travel distances
between peaks of
firing on two
overlapping place
cells can be
computed by the
time lag between the
two cells with respect
to their relationship
to the phase of the
underlying theta
rhythm
Diba & Buzsaki 2008 In: Buzsaki & Moser 2013

Characteristics of Grid Cells

• ‘Firing fields’ form a grid of repeating
equilateral triangles across
environment
• Defined by:
– Spacing between ‘firing fields’
– Field size
– Orientation
– Phase

• Grid cells in same region share

common spacing, size, & orientation

Buzsáki & Moser 2013; Hafting et al. 2005; Moser et al. 2014

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 17-­‐02-­‐18  

Characteristics of Grid Cells

• Grid cells in close
proximity have
different phases
– Note firing fields of
three different grid
cells (top figure)
– Cover entire
environment

• Grid cell patterns

can be anchored to
environment cues

Hafting et al. 2005

Head-direction Cells
• Discharge whenever
animal’s head is facing a
particular direction
– Independent of animal’s
location in environment
– Contrast with place cells

• Located in several parts of

brain
– Anterior thalamus,
presubiculum, and
entorhinal cortex

• Integrate information from

vestibular signals

Taube 2007

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Linear speed is directly

Speed Cells in the Medial proportional to AP firing rte
of speed cells.
Entorhinal Cortex
• A group of cells in the MEC discharge linearly in
relation to running speed (part b)
– Respond to acceleration and deceleration (part c)
– Different cells have different firing rates (part e)

Kropff et al. 2015

Speed Cells in the Medial

Entorhinal Cortex
• When rats forage in
open field, there
are large variations
in running speed
– Discharge activity
of speed cells co-
varies with speed
• Speed code is context-invariant
– Speed cells have same discharge-
speed relation in different environments
(part b: left)

• Can use discharge-speed relation to

train a computer algorithm, that can
then predict running speed in
different rooms (part d: left)
• Note: other cells in the MEC can also
be modulated by speed, but ‘speed
cells’ form a separate population
Kropff et al. 2015

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Try to think of movement before adding the finer details.
Subective marks based on organization and flow. We need at least 50 check marks

17-­‐02-­‐18  

Section Summary
• Brainstem centers can initiate walking
• Sensory feedback from muscle spindles, GTOs,
and cutaneous receptors in foot modulate activity of
spinal cord circuitry (e.g., CPG) to control step
cycle
• Vision heavily involved in guiding walking (in an
intermittent manner) for both planning and on-line
control
• Multiple limbs are coordinated (& separately
controlled)
• Motor cortex, PPC, and cerebellum involved (as
task demand increases) and related to execution
and planning of gait modifications

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