Corollary discharge across the animal kingdom

Most CD circuits identified in invertebrates are lower-order.

“Most of the CD circuits that have been identified in invertebrates are of this variety.”

Electrophysiological recordings from a transiently inactivated circuit in the brain have shed light on how corollary discharge is used for saccadic sequencing in rhesus monkeys.

“Electrophysiological recordings from a transiently inactivated circuit in the brain have shed some light on how CD is used for saccadic sequencing in rhesus monkeys62,63,65 (FIG. 6Aa).”

• cites [62] Sommer, M. A. & Wurtz, R. H. A pathway in primate brain for internal monitoring of movements. Science 296, 1480–1482 (2002). This was the first study to identify a CD pathway in the primate brain. sourceNot checked yet

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• cites [63] Sommer, M. A. & Wurtz, R. H. What the brain stem tells the frontal cortex. II. Role of the SC-MD-FEF pathway in corollary discharge. J. Neurophysiol. 91, 1403–1423 (2004). sourceNot checked yet

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• cites [65] Lynch, J., Hoover, J. & Strick, P. Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport. Exp. Brain Res. 100, 181–186 (1994). sourceNot checked yet

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When the midbrain-to-prefrontal pathway was inactivated by muscimol, behavioural deficits in the simplest saccadic sequencing task were observed.

“When this pathway was inactivated by muscimol, a GABAA (γ-aminobutyric acid receptor type A) agonist, behavioural deficits in the simplest saccadic sequencing task were observed.”

• cites [62] Sommer, M. A. & Wurtz, R. H. A pathway in primate brain for internal monitoring of movements. Science 296, 1480–1482 (2002). This was the first study to identify a CD pathway in the primate brain. sourceNot checked yet

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• cites [63] Sommer, M. A. & Wurtz, R. H. What the brain stem tells the frontal cortex. II. Role of the SC-MD-FEF pathway in corollary discharge. J. Neurophysiol. 91, 1403–1423 (2004). sourceNot checked yet

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• cites [65] Lynch, J., Hoover, J. & Strick, P. Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport. Exp. Brain Res. 100, 181–186 (1994). sourceNot checked yet

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Evidence for this corollary discharge function was recently found in neurons in the high vocal centre that fired with the same latency irrespective of whether the bird was actively singing or passively listening.

“Evidence for this CD function was recently found in neurons in the high vocal centre (HVC) that fired with the same latency irrespective of whether the bird was actively singing or passively listening74.”

• cites [74] Prather, J. F., Peters, S., Nowicki, S. & Mooney, R. Precise auditory–vocal mirroring in neurons for learned vocal communication. Nature 451, 305–310 (2008). sourceNot checked yet

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Eye movements in a two-step task change if corollary discharge about previous movements is impaired.

“Eye movements in a two-step task, for example, change if CD about previous movements are impaired.”

Experiments thus far have shown that inactivation of corollary discharge pathways can alter behaviour.

“Experiments thus far have shown that inactivation of CD pathways can alter behaviour, and covert perceptual changes might accompany these behavioural changes.”

The decussation from motor to sensory areas can occur at any number of levels of motor control, some remote from the final effector stage.

“However, it has become apparent that the decussation from motor to sensory areas might occur at any number of levels of motor control, some of which are remote from the final effector stage (FIG. 1b).”

Without differentiation, reafference would be confused for exafference.

“However, von Holst and Mittelstaedt2 pointed out that this would lead to a manifold sensory and interpretative problem: reafference would be confused for exafference.”

• cites von Holst and Mittelstaedt2Not checked yet

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Species that survived seem to have overcome the sensory problem with a remarkably uniform mechanism: nervous systems keep track of movement commands and inform the sensory processing stream about imminent movements.

“Those species that survived seem to have overcome the problem with a remarkably uniform mechanism: the animals’ nervous systems keep track of their movement commands and inform the sensory processing stream about movements that are imminent.”

Any ancestral species that failed to solve the sensory problems introduced by movements would have faced an evolutionary disadvantage.

“Because the sensory problems that are introduced by movements are potentially devastating, any ancestral species that failed to solve them would have faced an evolutionary disadvantage.”

A ubiquitous strategy is to route copies of movement commands to sensory structures.

“A ubiquitous strategy is to route copies of movement commands to sensory structures.”

The general strategy involves coincident production of a motor command destined for an effector and a motor-command copy destined for a sensory structure.

“The general strategy involves the coincident production of a motor command destined for an effector and a motor-command copy destined for a sensory structure.”

Movements can induce sensory input that is indistinguishable from input caused by external agents.

“Movements can induce sensory input (for example, when you hit something) that is indistinguishable from the input that is caused by external agents (for example, when something hits you).”

An animal would be unresponsive to independently occurring inputs that followed jarring motor acts.

“The animal would thus be unresponsive to independently occurring inputs that followed jarring motor acts.”

The combination of sensory receptor input and a motor copy indicating how a movement might influence the input allows a moving animal to resolve confusion in sensory input.

“Thus, the combination of the input received from the sensory receptors and the motor copy that indicates how a movement might influence the input signal allows a moving animal to resolve the confusion in sensory input.”

Corollary discharge signals influence sensory processing in many ways.

“These signals, which are referred to as corollary discharge (CD), influence sensory processing in myriad ways.”

On receipt of the copy signal, the sensory structure adjusts to minimize, eliminate or compensate for the sensory consequences of the movement.

“On receipt of the copy signal, the sensory structure adjusts appropriately to minimize, eliminate or compensate for the sensory consequences of the movement.”

It is critical for nervous systems to differentiate between self-caused and externally caused sensory input.

“It is critical for nervous systems to be able to differentiate between these two scenarios.”

In gastropods such as Pleurobranchaea, the withdrawal response to tactile stimulation of the oral veil does not occur while the animal is feeding.

“Normally, gastropods such as Pleurobranchaea repel if contact is made with the tactile mechanoreceptors of its oral veil (its ‘mouth’; FIG. 3b, schematic). However, this withdrawal response does not occur while the animal is feeding, despite there being comparable tactile stimulation.”

• cites [10] Davis, W. J., Siegler, M. V. S. & Mpitsos, G. J. Distributed neuronal oscillators and efference copy in the feeding system of Pleurobranchaea. J. Neurophysiol. 36, 258–274 (1973). This was one of the first electrophysiological studies to characterize CD signals at the cellular level. sourceNot checked yet

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In C. elegans, inhibitory neurons silence the second reflex pathway and annul the effect of reafference.

“However, inhibitory neurons quickly silence the second reflex pathway and annul the effect of the reafference.”

• cites [8] Chalfie, M. et al. The neural circuit for touch sensitivity in Caenorhabditis elegans. J. Neurosci. 5, 956–964 (1985). sourceNot checked yet

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CD circuits conform to a common neuronal plan, with only minor modifications in motor source and sensory termination.

“We find that CD circuits conform to a common neuronal plan, with only minor modifications in motor source and sensory termination.”

The reflex-inhibition examples are instances of CD regulating sensation by reflex inhibition.

“These examples are thus instances of CD regulating sensation by reflex inhibition (FIG. 3c).”

In monkeys, CD of head-movement commands suppresses neurons of the vestibular nucleus during voluntary head movement, preventing the inappropriate reflex response.

“It has been demonstrated in monkeys that CD of head-movement commands suppresses neurons of the vestibular nucleus during voluntary head movement, thus preventing the inappropriate reflex response80.”

• cites [80] Roy, J. E. & Cullen, K. E. Dissociating self-generated from passively applied head motion: neural mechanisms in the vestibular nuclei. J. Neurosci. 24, 2102–2111 (2004). sourceNot checked yet

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Lower-order CD serves a sentinel function by intervening along a sensorimotor pathway to regulate sensory information entering the system and the motor responses it elicits.

“This type of CD serves a sentinel function by intervening at various points along a sensorimotor pathway to regulate the sensory information that enters the system (in the case of sensory filtration) and the motor responses that the information elicits (in the case of reflex inhibition).”

CD signals influence proprioceptive processing at multiple points in the neuraxis, ranging from the spinal cord to the cortex.

“More generally, CD signals influence proprioceptive processing at multiple points in the neuraxis, ranging from the spinal cord83 to the cortex84.”

• cites [83] Seki, K., Perlmutter, S. I. & Fetz, E. E. Sensory input to primate spinal cord is presynaptically inhibited during voluntary movement. Nature Neurosci. 6, 1309–1316 (2003). sourceNot checked yet

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• cites [84] Voss, M., Ingram, J. N., Haggard, P. & Wolpert, D. M. Sensorimotor attenuation by central motor command signals in the absence of movement. Nature Neurosci. 9, 26–27 (2006). sourceNot checked yet

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The muscle spindle is regulated directly through projections from gamma motor neurons that receive CD of the movement commands sent to alpha motor neurons.

“One type of proprioceptor, the muscle spindle, is regulated directly through projections from gamma motor neurons that receive CD of the movement commands sent to muscle-innervating alpha motor neurons82.”

• cites [82] Matthews, P. B. C. Where does sherrington's “muscular sense” originate? Muscles, joints, corollary discharges? Annu. Rev. Neurosci. 5, 189–218 (1982). sourceNot checked yet

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The crayfish escape response is triggered by information entering through arrays of hair cells on its tail and abdomen.

“This escape response is triggered by information that enters the system through arrays of hair cells located on its tail and abdomen12–14.”

• cites [12] Edwards, D., Heitler, W. & Krasne, F. Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish. Trends Neurosci. 22, 153–161 (1999). sourceNot checked yet

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• cites [13] Hatsopoulos, N., Gabbiani, F. & Laurent, G. Elementary computation of object approach by a wide-field visual neuron. Science 270, 1000–1003 (1995). sourceNot checked yet

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• cites [14] Levi, R. & Camhi, J. Wind direction coding in the cockroach escape response: winner does not take all. Neuroscience 20, 3814–3821 (2000). sourceNot checked yet

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The C. elegans avoidance response consists of two main reflexes: forward and backward progression.

“Its avoidance response consists of two main reflexes: forward and backward progression7.”

• cites [7] Rankin, C. H. Interactions between two antagonistic reflexes in the nematode Caenorhabditis elegans. J. Comp. Physiol. A 169, 59–67 (1991). sourceNot checked yet

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A CD regulatory circuitry remarkably similar to that of C. elegans modulates Xenopus laevis tadpole avoidance reflexes during locomotion.

“A comparable problem is faced by Xenopus laevis tadpoles during locomotion, and a CD regulatory circuitry remarkably similar to that of C. elegans modulates their avoidance reflexes9.”

• cites [9] Sillar, K. T. & Roberts, A. A neuronal mechanism for sensory gating during locomotion in a vertebrate. Nature 331, 262–265 (1988). sourceNot checked yet

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Animals that occupy diverse niches show differences in their use of CD that can be summarized with a functional taxonomy.

“Animals that occupy diverse niches show differences in their use of CD that, we propose, can be summarized with a functional taxonomy.”

In saccadic suppression, a CD of the gaze shift lowers the gain of target visual structures to reduce information transfer between visual areas.

“In this process, a CD of the gaze shift lowers the gain of target visual structures to reduce information transfer between visual areas33.”

• cites [33] Ross, J., Morrone, M. C., Goldberg, M. E. & Burr, D. C. Changes in visual perception at the time of saccades. Trends Neurosci. 24, 113–121 (2001). sourceNot checked yet

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In terms of function, the crayfish CD circuit is almost identical to one identified in the cockroach, another organism with a behaviourally important hair-cell/escape-response circuit.

“In terms of function, this circuit is almost identical to one that has been identified in the cockroach, another organism with a behaviourally important hair-cell/escape-response circuit16.”

• cites [16] Delcomyn, F. Corollary discharge to cockroach giant interneurons. Nature 269, 160–162 (1977). sourceNot checked yet

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The crayfish circuitry contains CDIs that receive signals from the lateral giant command neurons, which initiate the escape response.

“The circuitry contains CDIs that receive signals from the lateral giant command neurons, which initiate the escape response (FIG. 4a).”

• cites [15] Krasne, F. B. & Bryan, J. S. Habituation: regulation through presynaptic inhibition. Science 182, 590–592 (1973). sourceNot checked yet

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The predictive nature and dependence on self-vocalization of marmoset auditory suppression implicate CD as its cause.

“Both the predictive nature of the effect and the dependence on self-vocalization implicate CD as the cause of the suppression.”

To avoid reafferent saturation, CDs of swimming commands directly inhibit the lateral-line hair cells in the dogfish.

“To avoid reafferent saturation, CDs of swimming commands directly inhibit the lateral-line hair cells20.”

• cites [20] Roberts, B. L. & Russell, I. J. The activity of lateral line efferent neurones in stationary and swimming dogfish. J. Exp. Biol. 57, 435–448 (1972). sourceNot checked yet

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The crayfish CD arrangement prevents a feedback cycle of movement and escape that would otherwise ensue with each movement.

“This arrangement prevents a dizzying feedback cycle of movement–escape that would otherwise ensue with each movement.”

Overall, lower-order CD has a common functional impact: transient, protective inhibition of sensory networks.

“Overall, it seems that lower-order CD has a common functional impact: transient, protective inhibition of sensory networks.”

The crayfish CDIs synapse on interneurons that presynaptically inhibit primary afferents from the tail hair cells.

“The CDIs synapse on to interneurons (called primary afferent depolarizing interneurons) that presynaptically inhibit primary afferents from the tail hair cells.”

• cites [15] Krasne, F. B. & Bryan, J. S. Habituation: regulation through presynaptic inhibition. Science 182, 590–592 (1973). sourceNot checked yet

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In the marmoset primary auditory cortex, many neurons are suppressed during self-vocalizations.

“A protective mechanism is observable in the marmoset primary auditory cortex, where many neurons are suppressed during self-vocalizations27,28.”

• cites [27] Eliades, S. J. & Wang, X. Sensory-motor interaction in the primate auditory cortex during self-initiated vocalizations. J. Neurophysiol. 89, 2194–2207 (2003). sourceNot checked yet

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• cites [28] Eliades, S. J. & Wang, X. Dynamics of auditory-vocal interaction in monkey auditory cortex. Cereb. Cortex 15, 1510–1523 (2005). sourceNot checked yet

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In vision, problems arise not from autogenic energy but from the actions of the animal.

“In vision, problems arise not from autogenic energy (energy originating from the animal itself — for example, the sound that results from a vocalization) but from the actions of the animal.”

CD mechanisms allow crayfish to move freely without inadvertently triggering or habituating their reflexive escape responses.

“CD mechanisms allow crayfish to move freely without inadvertently triggering or habituating their reflexive escape responses15.”

• cites [15] Krasne, F. B. & Bryan, J. S. Habituation: regulation through presynaptic inhibition. Science 182, 590–592 (1973). sourceNot checked yet

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CD mechanisms devoted to sensory filtration have evolved concurrently with the motor and sensory systems involved in acoustic communication.

“CD mechanisms devoted to sensory filtration have evolved concurrently with the motor and sensory systems that are involved in acoustic communication.”

The transient blur that occurs during saccades is minimized by saccadic suppression.

“The transient blur that occurs during saccades is minimized by a process called saccadic suppression33.”

• cites [33] Ross, J., Morrone, M. C., Goldberg, M. E. & Burr, D. C. Changes in visual perception at the time of saccades. Trends Neurosci. 24, 113–121 (2001). sourceNot checked yet

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It is crucial that the brain distinguish artefactual aspects of the jumpy visual inflow due to saccades from real aspects due to changes in the world.

“It is crucial that the brain be able to distinguish what aspects of the ‘jumpy’ visual inflow are artefactual (due to saccades) as opposed to real (due to changes in the world).”

Many neurons of the primate visual system alter their visual sensitivity at the time of a saccade, shifting visual responsiveness before the saccade from current receptive fields to the future field.

“Many neurons of the primate visual system alter their visual sensitivity at the time of a saccade (see figure, part a). Visual responsiveness shifts before the saccade from the neurons’ current visual receptive fields (RFs) to the location (the future field; FF) where the RFs will rest after the saccade.”

Inactivation of the CD pathway at its thalamic relay reduces the ability of frontal eye field neurons to shift their receptive fields.

“Inactivation of this pathway at its point of relay in the thalamus reduces the ability of these FEF neurons to shift their RFs (see figure, parts b and c).”

Motor pathways are known to target the barrel cortex from the motor cortex, the superior colliculus and other brainstem areas.

“Motor pathways are known to target the barrel cortex from the motor cortex, the superior colliculus and other brainstem areas45,46.”

• cites [45] Ahissar, E. & Kleinfeld, D. Closed-loop neuronal computations: focus on vibrissa somatosensation in rat. Cereb. Cortex 13, 53–62 (2003). sourceNot checked yet

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• cites [46] Kleinfeld, D., Berg, R. W. & O'Conner, S. M. Anatomical loops and their electrical dynamics in relation to whisking by rat. Somatosens. Mot. Res. 16, 69–88 (1999). sourceNot checked yet

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The frontal eye field contains neurons with shifting receptive fields.

“One brain area that contains neurons with this property is the frontal eye field (FEF), a cortical structure that is involved in vision and eye-movement control42.”

• cites [42] Schall, J. D. On the role of frontal eye field in guiding attention and saccades. Vision Res. 44, 1453–1467 (2004). sourceNot checked yet

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At least some of the CD for shifting receptive fields arises from a pathway that ascends from the midbrain to the frontal eye field.

“At least some of this CD arises from a pathway that ascends from the midbrain40,41 to the frontal eye field, a cortical structure that is involved in visual processing and eye-movement control42.”

• cites [40] Sommer, M. A. & Wurtz, R. H. Influence of the thalamus on spatial visual processing in frontal cortex. Nature 444, 374–377 (2006). sourceNot checked yet

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• cites [41] Sommer, M. A. & Wurtz, R. H. Brain circuits for the internal monitoring of movements. Annu. Rev. Neurosci. 31, 317–338 (2008). sourceNot checked yet

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• cites [42] Schall, J. D. On the role of frontal eye field in guiding attention and saccades. Vision Res. 44, 1453–1467 (2004). sourceNot checked yet

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Because a saccade can have any direction and amplitude, a neuron with a shifting receptive field requires the appropriate CD to calculate the new receptive field.

“Because a saccade can have any direction and any amplitude, a neuron with a shifting RF requires the appropriate CD to calculate the new RF.”

Because the whisking-related barrel cortex signal was of central origin, a CD seems to have been at work.

“Because the signal was of central origin, a CD seems to have been at work.”

CD for perceptual cohesion allows an organism to move and continue to experience the world as stable and continuous rather than as it is sensed at the receptor level.

“CD for perceptual cohesion allows an organism to move and yet continue to experience the world as it is (stable and continuous) rather than as it is sensed at the receptor level (in a chaotic and piecemeal fashion).”

Higher-order CD is crucial in action sequencing because it provides internal feedback that escapes the afferent lags and bandwidth constraints of sensory or external feedback loops.

“Higher-order CD is crucial in this process of action sequencing because it provides internal feedback that escapes the afferent lags and bandwidth constraints of sensory or external feedback loops.”

Although saccadic suppression systems differ anatomically across species, each circuit involves a CD operating as a gate that regulates signal traffic from the periphery, a lower-order CD function.

“Although the suppressive systems of these species differ with respect to the anatomical structures concerned, each circuit involves a CD operating as a gate that regulates signal traffic from the periphery — by definition a lower-order CD function.”

Saccadic suppression mechanisms have been identified in pigeons, chickens, locusts, monkeys and cats.

“Saccadic suppression mechanisms have been identified in a host of different species, such as pigeons, chickens, locusts, monkeys and cats34–38.”

• cites [34] Marin, G., Letelier, J. C. & Wallman, J. Saccade-related responses of centrifugal neurons projecting to the chicken retina. Exp. Brain Res. 82, 263–270 (1990). sourceNot checked yet

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• cites [35] Zaretsky, M. & Rowell, C. H. F. Saccadic suppression by corollary discharge in the locust. Nature 280, 583–584 (1979). sourceNot checked yet

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• cites [36] Thiele, A., Henning, P., Kubischik, M. & Hoffmann, K. P. Neural mechanisms of saccadic suppression. Science 295, 2460–2462 (2002). sourceNot checked yet

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• cites [37] Lee, D. & Malpeli, J. G. Effects of saccades on the activity of neurons in the cat lateral geniculate nucleus. J. Neurophysiol. 79, 922–936 (1998). sourceNot checked yet

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• cites [38] Yang, Y., Cao, P., Yang, Y. & Wang, S. R. Corollary discharge circuits for saccadic modulation of the pigeon visual system. Nature Neurosci. 11, 595–602 (2008). sourceNot checked yet

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Bats explore the environment by emitting high-intensity, high-frequency beams of sound and then comparing spatiotemporal aspects of the returning echo with the emitted sound.

“Bats explore the environment by emitting high-intensity, high-frequency beams of sound and then comparing spatiotemporal aspects of the returning echo with the emitted sound53,54.”

• cites [53] Moss, C. F. & Sinha, S. R. Neurobiology of echolocation in bats. Curr. Opin. Neurobiol. 13, 751–758 (2003). sourceNot checked yet

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• cites [54] Neuweiler, G. Evolutionary aspects of bat echolocation. J. Comp. Physiol. A 189, 245–256 (2003). sourceNot checked yet

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In the mormyrid ampullary system, ELL neurons respond to the CD in a manner dependent on recent experience.

“ELL neurons responded to the CD in a manner that was dependent on recent experience.”

• cites [52] Bell, C. C. An efference copy which is modified by reafferent input. Science 214, 450–453 (1981). This was a pioneering study that unveiled a plastic CD in the mormyrid that was modifiable by recent sensory experience. sourceNot checked yet

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The mormyromast corollary discharge amplifies the respective electroreceptor during electric-organ discharge.

“These systems differ from the ampullary system in that they require CDs that amplify (mormyromast) or inhibit (knollenorgan) the respective electroreceptor during EOD.”

• cites [50] Mohr, C., Roberts, P. D. & Bell, C. C. The mormyromast region of the mormyrid electrosensory lobe. I. Responses to corollary discharge and electrosensory stimuli. J. Neurophysiol. 90, 1193–1210 (2003). sourceNot checked yet

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• cites [51] Bell, C. C. & Grant, K. Corollary discharge inhibition and preservation of temporal information in a sensory nucleus of mormyrid electric fish. J. Neurosci. 9, 1029–1044 (1989). sourceNot checked yet

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A modifiable corollary discharge is evolutionarily advantageous because mormyrids navigate diverse aquatic environments that differ subtly in conductivity and resistivity.

“A modifiable CD is evolutionarily advantageous because mormyrids navigate diverse aquatic environments that differ subtly in conductivity and resistivity.”

The knollenorgan corollary discharge inhibits the respective electroreceptor during electric-organ discharge.

“These systems differ from the ampullary system in that they require CDs that amplify (mormyromast) or inhibit (knollenorgan) the respective electroreceptor during EOD.”

• cites [50] Mohr, C., Roberts, P. D. & Bell, C. C. The mormyromast region of the mormyrid electrosensory lobe. I. Responses to corollary discharge and electrosensory stimuli. J. Neurophysiol. 90, 1193–1210 (2003). sourceNot checked yet

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• cites [51] Bell, C. C. & Grant, K. Corollary discharge inhibition and preservation of temporal information in a sensory nucleus of mormyrid electric fish. J. Neurosci. 9, 1029–1044 (1989). sourceNot checked yet

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The CD of the mormyrid ampullary system is effectively a plastic photo negative of the expected reafference.

“The CD of the ampullary system is effectively a plastic photo negative of the expected reafference”

• cites [52] Bell, C. C. An efference copy which is modified by reafferent input. Science 214, 450–453 (1981). This was a pioneering study that unveiled a plastic CD in the mormyrid that was modifiable by recent sensory experience. sourceNot checked yet

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For the mormyrid ampullary system, an adaptable CD mechanism is at work.

“For the ampullary system, an adaptable CD mechanism was found to be at work52.”

• cites [52] Bell, C. C. An efference copy which is modified by reafferent input. Science 214, 450–453 (1981). This was a pioneering study that unveiled a plastic CD in the mormyrid that was modifiable by recent sensory experience. sourceNot checked yet

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Each time a motor command exits the mormyrid electric-organ command centre, a CD of the motor command also exits, targeting the electrosensory lateral line lobe.

“Each time a motor command exits the electric-organ command centre, a CD of the motor command also exits, targeting the ELL.”

• cites [52] Bell, C. C. An efference copy which is modified by reafferent input. Science 214, 450–453 (1981). This was a pioneering study that unveiled a plastic CD in the mormyrid that was modifiable by recent sensory experience. sourceNot checked yet

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As a primate looks around a scene, it must continuously update its internal record of the current saccade to facilitate planning the next.

“As a primate looks around a scene, it must continuously update its internal record of the current saccade to facilitate planning the next.”

Such signals convey information related to the distance of approaching obstacles and the dimensions of environmental objects.

“Such signals convey information that is related to the distance of approaching obstacles and the dimensions of environmental objects.”

In all of the reviewed different species, corollary discharges aid the construction of an internal representation of the environment.

“In all of these different species, CDs aid the construction of an internal representation of the environment.”

Neurons that connect the midbrain to the prefrontal cortex transmit bursts of action potentials that encode saccadic parameters.

“Neurons that connect the midbrain to the prefrontal cortex transmit bursts of action potentials that encode saccadic parameters.”

• cites [62] Sommer, M. A. & Wurtz, R. H. A pathway in primate brain for internal monitoring of movements. Science 296, 1480–1482 (2002). This was the first study to identify a CD pathway in the primate brain. sourceNot checked yet

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• cites [63] Sommer, M. A. & Wurtz, R. H. What the brain stem tells the frontal cortex. II. Role of the SC-MD-FEF pathway in corollary discharge. J. Neurophysiol. 91, 1403–1423 (2004). sourceNot checked yet

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• cites [65] Lynch, J., Hoover, J. & Strick, P. Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport. Exp. Brain Res. 100, 181–186 (1994). sourceNot checked yet

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If the echo returns within a specific time frame, then neurons primed for analysis within that particular window will respond optimally and convey information to perceptual structures for further analysis.

“If the echo returns within a specific time frame, then neurons that have been primed for analysis within that particular window will respond optimally and convey information to perceptual structures for further analysis.”

Echo-sensitive neurons are thought to be primed by corollary discharges of vocalizations that open time windows of echo analysis.

“The echo-sensitive neurons are thought to be primed by CDs of vocalizations that open time windows of echo analysis.”

Corollary discharge has repeatedly been implicated in the process of updating the internal record of the current saccade to facilitate planning the next.

“CD has repeatedly been implicated in this process59–64.”

• cites [59] Bellebaum, C., Daum, I., Koch, B., Schwarz, M. & Hoffmann, K. P. The role of the human thalamus in processing corollary discharge. Brain 128, 1139–1154 (2005). sourceNot checked yet

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• cites [60] Bellebaum, C., Hoffmann, K. P., Koch, B., Schwarz, M. & Daum, I. Altered processing of corollary discharge in thalamic lesion patients. Eur. J. Neurosci. 24, 2375–2388 (2006). sourceNot checked yet

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• cites [61] Guthrie, B. L., Porter, J. D. & Sparks, D. L. Corollary discharge provides accurate eye position information to the oculomotor system. Science 221, 1193–1195 (1983). sourceNot checked yet

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• cites [62] Sommer, M. A. & Wurtz, R. H. A pathway in primate brain for internal monitoring of movements. Science 296, 1480–1482 (2002). This was the first study to identify a CD pathway in the primate brain. sourceNot checked yet

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• cites [63] Sommer, M. A. & Wurtz, R. H. What the brain stem tells the frontal cortex. II. Role of the SC-MD-FEF pathway in corollary discharge. J. Neurophysiol. 91, 1403–1423 (2004). sourceNot checked yet

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• cites [64] Tanaka, M. Inactivation of the central thalamus delays self-timed saccades. Nature Neurosci. 9, 20–22 (2006). sourceNot checked yet

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Intricate feedback loops that course throughout the avian song system are thought to convey the auditory, memory and corollary discharge signals.

“Intricate feedback loops that course throughout the avian song system are thought to convey the auditory, memory and CD signals70,71 (FIG. 6Ba).”

• cites [70] Margoliash, D. Functional organization of forebrain pathways for song production and perception. J. Neurobiol. 33, 671–693 (1997). sourceNot checked yet

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• cites [71] Reiner, A., Yamamoto, K. & Karten, H. Organization and evolution of the avian forebrain. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 287, 1080–1102 (2005). sourceNot checked yet

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In this saccadic sequencing example, corollary discharge emerges from a lower-level motor structure and ascends the neuraxis to impinge on a higher-level executive centre.

“This is an example in which CD emerges from a lower-level motor structure and ascends the neuraxis to impinge on a higher-level executive centre (FIG. 6Ab).”

• cites [62] Sommer, M. A. & Wurtz, R. H. A pathway in primate brain for internal monitoring of movements. Science 296, 1480–1482 (2002). This was the first study to identify a CD pathway in the primate brain. sourceNot checked yet

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• cites [63] Sommer, M. A. & Wurtz, R. H. What the brain stem tells the frontal cortex. II. Role of the SC-MD-FEF pathway in corollary discharge. J. Neurophysiol. 91, 1403–1423 (2004). sourceNot checked yet

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• cites [65] Lynch, J., Hoover, J. & Strick, P. Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport. Exp. Brain Res. 100, 181–186 (1994). sourceNot checked yet

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The pathway from the midbrain to the prefrontal cortex also has a sensory analysis and stability function.

“As discussed above and in BOX 2, this pathway also has a sensory analysis and stability function.”

Errors between the memory of tutors' songs and the actual auditory feedback are corrected through an iterative cycle of vocal production followed by adjustment of the motor programme.

“The errors between the memory and the actual feedback are corrected through an iterative cycle of vocal production, followed by adjustment of the motor programme.”

The feedback loops execute a delay function by increasing the distance over which corollary discharge issued from vocal centres travels before it collides with auditory feedback.

“The feedback loops execute a delay function by increasing the distance over which CD that is issued from vocal centres travels before it collides with auditory feedback72,73.”

• cites [72] Troyer, T. W. & Doupe, A. J. An associational model of birdsong sensorimotor learning I. Efference copy and the learning of song syllables. J. Neurophysiol. 84, 1204–1223 (2000). sourceNot checked yet

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• cites [73] Troyer, T. W. & Doupe, A. J. An associational model of birdsong sensorimotor learning II. Temporal hierarchies and the learning of song sequence. J. Neurophysiol. 84, 1224–1239 (2000). sourceNot checked yet

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Corollary discharge is especially important while vocalization is being learned.

“CD is especially important while vocalization is being learned.”

The bird has to keep track of its own motor commands in order to properly adjust and calibrate its subsequent commands.

“The bird has to keep track of its own motor commands in order to properly adjust and calibrate its subsequent commands.”

Corollary discharge seems to have a key role during the second phase of vocal learning.

“CD seems to have a key role during the second phase of vocal learning68,69.”

• cites [68] Brainard, M. & Doupe, A. J. Auditory feedback in learning and maintenance of vocal behaviour. Nature Rev. Neurosci. 1, 31–40 (2000). sourceNot checked yet

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• cites [69] Margoliash, D. Evaluating theories of bird song learning: implications for future directions. J. Comp. Physiol. A 188, 851–866 (2002). sourceNot checked yet

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The first stage of song development is a sensory phase in which the juvenile bird listens to the songs of other adult birds known as tutors.

“The first stage is a sensory phase in which the juvenile bird listens to the songs of other adult birds known as tutors.”

• cites [67] Catchpole, D. K. & Slater, P. J. B. Bird Song: Biological Themes and Variations (Cambridge Univ. Press, Cambridge, 1995).Not checked yet

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The second stage of song development consists of sensorimotor training in which the bird begins to sing spontaneously with syllables of varying intensity and motifs of high variability.

“The second stage consists of sensorimotor training in which the bird begins to sing spontaneously with syllables of varying intensity and motifs of high variability.”

• cites [67] Catchpole, D. K. & Slater, P. J. B. Bird Song: Biological Themes and Variations (Cambridge Univ. Press, Cambridge, 1995).Not checked yet

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Male juvenile songbirds exhibit a stereotyped song that emerges gradually following several developmental stages.

“Male juvenile songbirds (see FIG. 6Ba) exhibit a stereotyped song that emerges gradually following several developmental stages67.”

• cites [67] Catchpole, D. K. & Slater, P. J. B. Bird Song: Biological Themes and Variations (Cambridge Univ. Press, Cambridge, 1995).Not checked yet

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These bilateral feedback pathways ascend from midbrain and medullary vocal-control nuclei up to the forebrain song system.

“These pathways ascend from midbrain and medullary vocal-control nuclei up to the forebrain song system.”

• cites [66] Striedter, G. F. & Vu, E. T. Bilateral feedback projections to the forebrain in the premotor network for singing in zebra finches. J. Neurobiol. 34, 27–40 (1998). sourceNot checked yet

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The bird is thought to fine-tune its song during the second phase by comparing auditory feedback of its own vocalizations with copies of tutors' songs that are stored in memory.

“The bird is thought to fine-tune its song during this phase by comparing auditory feedback of its own vocalizations with copies of tutors’ songs that are stored in memory.”

• cites [68] Brainard, M. & Doupe, A. J. Auditory feedback in learning and maintenance of vocal behaviour. Nature Rev. Neurosci. 1, 31–40 (2000). sourceNot checked yet

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• cites [69] Margoliash, D. Evaluating theories of bird song learning: implications for future directions. J. Comp. Physiol. A 188, 851–866 (2002). sourceNot checked yet

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Singing birds are thought to use updated, internal records of current phonations to generate subsequent phonations.

“Singing birds are thought to use updated, internal records of current phonations to generate subsequent phonations.”

Bilateral feedback pathways have been identified in the singing finch that might convey updated internal records of current phonations.

“Bilateral feedback pathways have been identified in the singing finch that might convey such vital information66.”

• cites [66] Striedter, G. F. & Vu, E. T. Bilateral feedback projections to the forebrain in the premotor network for singing in zebra finches. J. Neurobiol. 34, 27–40 (1998). sourceNot checked yet

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The main characteristic of lower-order corollary discharge circuits is the presence of a single interneuron, the CDI, which exerts inhibitory actions on various cellular components and controls interactions between motor and sensory circuitries through its suppressive influences.

“The main characteristic of these circuits is the presence of a single interneuron, the CDI, which exerts inhibitory actions on various cellular components and controls interactions between motor and sensory circuitries through its suppressive influences.”

Higher-order corollary discharge underwrites complex behavioural phenotypes and cognitive operations, such as motor sequencing, sensorimotor learning and perceptual stabilization.

“This type of CD underwrites complex behavioural phenotypes and cognitive operations, such as motor sequencing, sensorimotor learning and perceptual stabilization.”

Higher-order corollary discharge operates in the context of internal feedback circuitry, which involves multiple components and spans various levels of the neuraxis.

“Higher-order CD operates in the context of internal feedback circuitry, which involves multiple components and spans various levels of the neuraxis.”

In the nematode and gastropod examples of reflex inhibition, corollary discharge intervenes at the precise time of the motor act to prevent an antagonistic reflex response.

“This point is illustrated best in the nematode and gastropod examples of reflex inhibition. Here, CD intervenes at the precise time of the motor act to prevent an antagonistic reflex response.”

Corollary discharge systems have evolved in tandem with the sensory systems of organisms that operate in diverse environments.

“CD systems have evolved in tandem with the sensory systems of organisms that operate in diverse environments.”

Unlike corollary discharge involved with the central control of sensation, which is almost solely time-modulated, corollary discharge involved with the central control of action and perception carries information that represents a number of variables.

“Unlike CD that is involved with the central control of sensation, which is almost solely time-modulated, CD that is involved with the central control of action and perception carries information that represents a number of variables.”

Each subtype of lower-order corollary discharge signal provides information about when the sensory input that is elicited from the motor act should occur.

“In short, each subtype of lower-order signal provides information about when the sensory input that is elicited from the motor act should occur.”

Lower-order corollary discharge circuits are illustrated best in invertebrates.

“We explained that lower-order CD circuits are illustrated best in invertebrates.”

In the cricket, corollary discharge is synchronized rhythmically with singing to protect the auditory system.

“In the cricket, for instance, CD is synchronized rhythmically with singing to protect the auditory system.”

At the lower-order level, corollary discharge is a discriminatory mechanism that prevents maladaptive responses and sensory saturation by restricting or filtering information.

“At one level (the lower-order level) CD is a discriminatory mechanism that prevents maladaptive responses and sensory saturation by restricting or filtering information.”

Computationally, the information content of lower-order corollary discharge types is probably minimal, as they generally implement a gain mechanism that modulates a reflex or gates the inflow of sensory information at the periphery.

“Computationally, the information content of these CD types is probably minimal, as they generally implement a gain mechanism that modulates a reflex or gates the inflow of sensory information at the periphery.”

In the monkey, corollary discharge in the visuosaccadic system encodes spatial as well as temporal information about imminent saccades.

“In the monkey, for example, CD in the visuosaccadic system encodes spatial as well as temporal information about imminent saccades.”

Lower-order corollary discharge signals seem to be one-dimensional in nature, with time as the most crucial variable.

“As such, these signals seem to be one-dimensional in nature: time is the most crucial variable.”

On exiting the motor domain, the corollary discharge signal impinges on higher-level structures that are highly sensory and/or executive in nature.

“Accordingly, on exiting the motor domain, the CD signal impinges on higher-level structures that are highly sensory and/or executive in nature.”

Corollary discharge is also present in the animal kingdom as a higher-order mechanism that mediates sophisticated predictive computations.

“CD is also present in the animal kingdom as a higher-order mechanism that mediates sophisticated predictive computations.”

Suppressive influences by an inhibitory corollary discharge are also found in vertebrates.

“Suppressive influences by an inhibitory CD are also found in vertebrates, and it is tempting to speculate that in some species these operations could also be carried out by a type of CDI.”

Functions such as reflex inhibition and sensory filtration are tightly controlled by lower-order corollary discharge, which is a type of access control.

“Functions such as reflex inhibition and sensory filtration are tightly controlled by this mode of signalling, which is a type of access control.”

The comparable latencies found for singing and passive listening imply that there is a delay function performed by a corollary discharge.

“The comparable latencies that were found for singing and passive listening imply that there is a delay function performed by a CD.”

• cites [74] Prather, J. F., Peters, S., Nowicki, S. & Mooney, R. Precise auditory–vocal mirroring in neurons for learned vocal communication. Nature 451, 305–310 (2008). sourceNot checked yet

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In rhesus monkeys, it seems to be possible to assess what an animal is perceiving.

“Although it is challenging to assess what an animal is perceiving, in rhesus monkeys, for example, it seems to be possible78,79.”

• cites [78] Logothetis, N. K. Single units and conscious vision. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 1801–1818 (1998). sourceNot checked yet

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• cites [79] Parker, A. J. & Newsome, W. T. Sense and the single neuron: probing the physiology of perception. Annu. Rev. Neurosci. 21, 227–277 (1998). sourceNot checked yet

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To date, only a few large-scale circuit-level investigations of corollary discharge that combined behaviour with physiology have been performed.

“To date, only a few large-scale circuit-level investigations of CD that combined behaviour with physiology have been performed38,40.”

• cites [38] Yang, Y., Cao, P., Yang, Y. & Wang, S. R. Corollary discharge circuits for saccadic modulation of the pigeon visual system. Nature Neurosci. 11, 595–602 (2008). sourceNot checked yet

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• cites [40] Sommer, M. A. & Wurtz, R. H. Influence of the thalamus on spatial visual processing in frontal cortex. Nature 444, 374–377 (2006). sourceNot checked yet

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For the species that use reflex inhibition and sensory filtration, which are both cases of lower-order corollary discharge, the motor-to-sensory crossing points were schematically similar, all being lower-motor-area-to-sensory-area neurons.

“For the species that use reflex inhibition and sensory filtration, which are both cases of lower-order CD, the motor-to-sensory crossing points were schematically similar (that is, they were all lower-motor-area-to-sensory-area neurons).”

The exact content and functional role of the corollary discharge signal varies from species to species and from system to system.

“As we have described, the exact content and functional role of the signal (whether the CD is the prediction or whether it enables the recipient substrate to generate the prediction) varies from species to species and from system to system.”

In the visuosaccadic system of the primate, a corollary discharge circuit has a role in sensorimotor planning as well as in sensory stability.

“One example we reviewed was from the visuosaccadic system of the primate40,62. In this system, a CD circuit has a role in sensorimotor planning as well as in sensory stability (compare FIG. 6A with BOX 2).”

• cites [40] Sommer, M. A. & Wurtz, R. H. Influence of the thalamus on spatial visual processing in frontal cortex. Nature 444, 374–377 (2006). sourceNot checked yet

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• cites [62] Sommer, M. A. & Wurtz, R. H. A pathway in primate brain for internal monitoring of movements. Science 296, 1480–1482 (2002). This was the first study to identify a CD pathway in the primate brain. sourceNot checked yet

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There is evidence that components of the olfactory system are modulated by 'motor signals' during the act of sniffing.

“There is evidence that components of the olfactory system are modulated by ‘motor signals’ during the act of sniffing75.”

• cites [75] Mainland, J. & Sobel, N. The sniff is part of the olfactory percept. Chem. Senses 31, 181–196 (2006). sourceNot checked yet

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Although the corollary discharge signals of the mormyrid and the bat emerged from differing motor tiers, their sensory-termination level was comparable, at lower sensory areas.

“Although the CD signals of the mormyrid and the bat, two sensory analysis/stability cases, emerged from differing motor tiers, their sensory-termination level was comparable (lower sensory areas).”

It is this coordination between the sensory and motor systems that makes it possible to analyse the world while moving within it.

“It is this coordination between the two systems that makes it possible to analyse the world while moving within it.”

All animals, from the nematode to the cognitively advanced primate, require the type of signalling that is enabled by corollary discharge.

“All animals, from the humble nematode to the cognitively advanced primate, require the type of signalling that is enabled by CD.”

In addition to the usual flow of information from sensory systems to motor systems, there is extensive signalling in the opposite direction by motor systems reporting their activities to sensory structures.

“In addition to the usual flow of information from sensory systems to motor systems, there is extensive signalling in the opposite direction by motor systems reporting their activities to sensory structures.”

In general, higher-order corollary discharges are multidimensional and encode more parameters than just time.

“In general, higher-order CDs are multidimensional and encode more parameters than just time.”

In all cases, the corollary systems of remarkably diverse species could be easily accommodated into a common template that illustrates their underlying similarities.

“In all cases the corollary systems of remarkably diverse species could be easily accommodated into a common template that illustrates their underlying similarities.”

• AssumptionThe authors state this as an assumption: The sensory target occupies increasingly higher tiers as one ascends from lower-order corollary discharge through the stages of higher-order corollary discharge.

A single corollary discharge circuit can mediate many different functions.

“A single CD circuit can mediate many different functions.”