10/26/2011

Reading

L35.SensoryMotorIntegration
TheCorollaryDischargeintheAnimal
Kingdom
October26,2011
C.D.Hopkins

1. Craspe,T.B.andSommer,M.A.(2008).Corollary
dischargeacrosstheanimalkingdom.Nature
ReviewsNeuroscience9,587600.
2. Poulet,J.F.A.(2005).Corollarydischargeinhibition
andauditioninthestridulatingcricket.J.Comp.
g
p
Physiol.A.191,979986.
3. Poulet,J.F.andHedwig,B.(2006).Thecellularbasis
ofacorollarydischarge.Science311,51822.

SensoryMotorIntegration
Much of sensory processing involves the generation of expectations or predictions
about sensory input, and subsequent removal of such expectations from the sensory
inflow.
Bell, C (1997) Brain, Behavior, Evolution 50 (suppl.) 17-31.

Dronefly,Eristalis igives anoptomotor responsetoa

movingstripeddrum.

normaloptomotor

reversedoptomotor

Eristalis
normal

headturned180

Inresponsetoanyselfmovement,thenormalflyignoresthestationarystripeddrum
whileaheadreversedflyoscillatesbackandforthinresponsetoselfinitiated
movements.

newtwithnormalretina,A,above
newtwithretinaBandD(below)
Holst E.vonand Mittelstaedt H.(1950)DasReafferenzprincip.Naturwissenschaften37,464476.

retinaAabove
retinaBandCbelow

Sperry,R.W.(1956).Theeyeandthebrain. ScientificAmerican

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CorollaryDischargeandEfferenceCopy
ErichvonHolst andHorstMittlesteadt (1950)
RogerSperry(1950)

Konrad Lorenz

Holst E.vonand Mittelstaedt H.(1950)

DasReafferenzprincip.
Naturwissenschaften37,464476.

ExpectedSensoryInputandtheReafference
Principle
Principle:everymotoractcauses
somesortofsensoryresponse
thatcanbeusedbyanimalto
controlsubsequentactions.
Sensoryfeedbackfrommotoract
can be useful evenvital
canbeuseful
even vital to
to
animalsperformance.
Sensoryfeedbackthatdiffers
fromexpectedcanbeusedto
controlsubsequentaction.

Erich von Holst

Erich von Holst , 1908-1962

Sperry,R.W.(1950).Neuralbasisofthe
spontaneousoptokinetic responseproduced
byvisualinversion. JournalofComparativeand
PhysiologicalPsychology 43:483489.

E.vonHolstandH.Mittelstaedt

Moveeyesorhead.
Retinalimageshifts

TheReafferencePrinciple:
interactionbetweenthecentral
nervoussystemandperiphery
(1950).

Expectedshift:thingsare
normal.
Unexpectedintput:thevisual
worldisshifting,takeaction.

Higherbraincenter,Zhasconnections
forbothmotoroutput(efference)and
(
)
sensoryresponses(afferences).
Whenamotorcommandarisesfroma
highercenter,theafferentfeedbackis
calledreafference.
Simultaneouswiththeefference,there
isasecond,internal,efference copy(EK).

Reafference

Comparedtoreafference,and
appropriatelydelayed,itservestotell
whethersensoryfeedbackisas
expected.

Holst E.vonand Mittelstaedt H.(1950)

Da;.Reafferenzprincip.
Naturwissenschaften37,464476. 10

IllustrationoftheReafference Principle:
a)Reafference circuitforthecontrolofeyemovements.
Zn=highervisualcenter
Z1=lowervisualcenter
E=efference (outputtomuscles)
A=reafference (visualmotion)
a)Theimmobilizedeyereceivesacommandtoturn
theeyetotheright.Theeyemusclesareimmobilized
bycurare:theefference copyispresentinthelower
center,Z1(anegativeimageoftheexpected
reafference).Thevisualworldappearstomovetothe
left.

11

b)

Theobjectmovestotheright;theimageontheretina
movesfrom1to2causingafference.

c)

Theeyeispassivelymovedtotherightbyexerting
pressureontheeyeball.Theimageofobjectmoves
acrossretina.

d)

Thecommandtomovetheeyetotheright,causesthe
imagetoshiftfrom1to2,alsocausingafference,but
now,itisexpected.Itisremovedfromthesensory
streaminZ1.
12

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UsingvonHolst andMittelstaedts terminology:

Efference:output(motor)
Afference:input(sensory)
Exafference:sensoryresponsetoeventsintheenvironment.
Reafference:sensoryresponseresultingfromanimalsownmovements.
Efference copy:acopyofthemotorefference,senttothesensorysystem.When
efference copyisaddedtoreafference,theresultiszero.Anyleftoversensationmust
beexafference.

thisoneis
incorrect

http://www.urllabs.com/wad/ia/corollar/corollar.htm
Craspe,T.B.andSommer,M.A.(2008).Corollarydischargeacrosstheanimalkingdom.
NatureReviewsNeuroscience9,587600.

Craspe,T.B.andSommer,M.A.(2008).Corollarydischargeacrosstheanimalkingdom.
NatureReviewsNeuroscience9,587600.

ClassificationschemeforCorollaryDischarges

CrayfishEscapeResponse

invertebrateexamplesonlyinvertebrates

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CricketStridulation

James Poulet and Berthold Hedwig: Corollary discharge maintains

auditory sensitivity during sound production in crickets.
Cricket Gryllus bimaculatus

Omega Neuron 1 (ON1) responds to

continuous sounds
except when stridulating
silent singing; no sound production
stimulus sounds

during fictive singing

ON1 receives inhibition

during fictive singing (nerve

roots between ganglia and
sense organs and muscles
are cut)
mesothoracic ganglia

Mesothoracic ganglion motor

behavior

stimulus sounds
inhibition is from motor program, not from some
other sensory feedback

What about the primary afferent neuron? Is the

afferent nerve silent during singing?

Record from auditory

afferents near the terminals
on ON1.
Afferents respond in phase
with sound. Soft sounds
give primary afferent
depolarizations (PAD)
(arrow).

In response the silent singing (one wing), there are Primary Afferent
Depolarizations in synchrony with the moving wing (no sound).

For silent singing

afferent does not
generate spikes as
before.
Note
N
t the
th primary
i
afferent
depolarizations
(PAD).
Timing of PADs is
similar to timing of
IPSPs in ON1.

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The primary afferent from the ear is not silenced by these

PADs, nor is it excited.

No inhibition or
excitation from PADs.
Response to sound is
normal during silent
wing movements.

Even after removal of the ears, the PAD is present in the auditory
afferent.

PAD during fictive

singing
even get PAD if ears are
removed.

Conclusion: primary afferent depolarizations are a type of presynaptic inhibition

How effective is the inhibition of ON1

(post synaptic and pre-synaptic)
During silent singing, chirps
presented to cricket at
typical volume.
Note decrement during
motor action.

soft sounds evoke spikes

loud, then soft, shows that loud sounds

cause ON1 to adapt, not respond to soft
sounds.
hyperpolarize during loud prevents
spiking,
and prevents adaptation.

Corollary Discharge Interneuron CDI

Conclusion:

Record from auditory neurons in

prothoracic ganglion and from
interneurons in mesothoracic (CPG for
song).

In cricket, motor output is accompanied by a corollary discharge

which interacts with primary acoustic afferents, and with Omega
neuron 1.

CDI: extensive projection throughout CNS

Both inputs inhibit the response to sound, reducing the response

t the
to
th loud
l d sound.
d
The overall effect is to prevent over-stimulation, thereby
maintaining sensitivity.

-- cell body and dendrites in Meso., can

get input from CPG
-- prothroracic dendrites overlap auditory
inputs
-- other terminals interaction with other
sensory inputs consequent on singing.

Poulet, J. F. and Hedwig, B. (2006). The cellular

basis of a corollary discharge. Science
311, 518-22.

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CDI during motor output

CDI fires during singing

CDI is not part of CPG

PSTH corresponds to wing

closure (sound phase)

phase response, Q = duration of

ongoing chirp period N/dur. chirp
period N+1

CDI is inhibited during flight

stimulated by song production

CDI is
unresponsive to
sounds

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Conclusions

Mormyrid electric fish produce an electro-motor command,

and receive a electrosensory response as a consequence.

In the cricket, an efferent signal works at two levels in the auditory

system
Pre-synaptic inhibition by PAD's in the afferent auditory terminal
Post-synaptic inhibition by IPSP's in ON1
The efferent signal is a corollary discharge because it is generated in
the nervous system and it's strength is independent of sound
production
The corollary discharge corresponds closely in timing to sound
production
Corollary discharges effectively reduce desensitization

40

Knollenorgans blank inputs by

inhibition
--Primary afferent (blue)
terminates on nELL cell
(yellow) with

EOD command
ipsp in nELL cell

--large calyx-like
synapses (electrotonic).
--fibers from EOD
command (eocd)
produce spikes that
arrive at same time that
EOD would be fired.

EODc

afferent

command

--sharp inhibition
IPSP blocks spike at the
time when EOD is
expected

EOD

-- removes expected
EOD
XU-FRIEDMAN, M. A. & HOPKINS, C. D., 1999.- J. Exp. Biol., 202:1311-1318.
FRIEDMAN, M.A. & HOPKINS, C.D. 1998 J. Neurosci.18:1171-1185.

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42

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EOD command

Bell, CC (1982)

43

44

Summary

EOD command

1. Sensory systems work to maintain

homeostasis, through reflex arcs.
2. To overcome homeostasis, sensory response
must be inhibited during movement.
3. Sensory systems respond to movement, but
the responses are expected.
4. If brief (saccades) expected responses may be
inhibited (blanked).
If longer lasting, expected response may be
subtracted using efference copy.
45

46

References
Bell,C.C.(1981).Anefference copywhichismodifiedbyreafferent input.Science214,450
53.
Bell,C.C.(1982).Propertiesofamodifiableefference copyinanelectricfish.JNeurophysiol
47,104356.
Bell,C.C.(1986).Durationofplasticchangeinamodifiableefference copy.BrainRes369,29
36.
Craspe,T.B.andSommer,M.A.(2008).Corollarydischargeacrosstheanimalkingdom.
NatureReviewsNeuroscience9,587600.
Holst,E.v.andMittelstaedt,H.(1950).DasReafferenzprincip.Naturvissenschaften37,464
476.
Poulet,J.F.A.andHedwig,B.(2003).Corollarydischargeinhibitionofascendingauditory
neuronsinthestridulatingcricket.JournalofNeuroscience23,47174725.
Poulet,J.F.&Hedwig,B.Newinsightsintocorollarydischargesmediatedbyidentifiedneural
pathways.TrendsNeurosci.30,1421(2007).
Solis,M.M.,Brainard,M.S.,Hessler,N.A.andDoupe,A.J.(2000).Songselectivityand
sensorimotor signalsinvocallearningandproduction.ProcNatl Acad Sci USA97,1183642.
Sperry,R.W.(1950).Neuralbasisofthespontaneousoptokinetic responseproducedbyvisual
inversion. .JournalofComparativeandPhysiologicalPsychology 42,483489.
Sperry,R.W.(1956).Theeyeandthebrain. .ScientificAmerican.