Efference copy is an internal copy of a motor innervation. When a motor command is sent through the nervous system this copy is used to predict the expected sensation which will occur. A motor signal from the central nervous system (CNS) to the periphery is called an efference, and a copy of this signal is called an efference copy (EC). Sensory information coming from sensory receptors in the peripheral nervous system to the central nervous system is called afference. It is theorized that at the same time that an efferent signal is produced and sent to the motor system, a copy of the signal, known as an efference copy, is produced for the purpose of distinguishing between exafference (sensory signals generated from external stimuli in the environment) and reafference (sensory signals resulting from an animal's own actions).

Historical View

In the middle of the 19th century, the German physician and physicist Hermann von Helmholtz suggested that the brain used an efference copy for specific motor commands controlling the eye muscles to determine the location of an object relative to the head. His simple experiment involved gently pressing on his own eye and noticing that the visual world moved as a result of this passive movement. An active movement of the eye muscles would have resulted in the perception that the world was holding still. With passive eye movement, no EC was produced to anticipate the sensory outcome and the world appeared to be moving.

One century later, experimental work by von Holst , Mittelstaedt, and Sperry demonstrated in animal models how sensory information may be cancelled or altered to maintain stable perception. The findings of these early studies would collectively form the experimental and theoretical basis for what is now known as efference copy theory. While the scientific contributions of Sherrington and others in the early 20th Century had sought to explain the physiologic interaction between the world and the CNS in terms of afferent inputs and "reflexive" efferent outputs, this group of scientists proposed that far from a stereotyped response, an EC had a vital role in modulating the amplitude or degree of response across various neuromotor systems. The role of EC in the optokinetic reflex was the first such system to be described.

In 1950, Von Holst and Mittelstadt investigated how species are able to distinguish between exafference and reafference given a seemingly identical percept of the two. To explore this question, they rotated the head of a fly 180 degrees, effectively reversing the right and left edges of the retina and reversing the subject's subsequent reafferent signals. In this state, self-initiated movements of the fly would result in a perception that the world was also moving, rather than standing still as they would in a normal fly. After rotation of the eyes, the animal showed a reinforcement of the optokinetic response in the same direction as the moving visual input. Von Holst and Mittelstadt interpreted their findings as evidence that corollary discharge (i.e. neural inhibition with active movement) could not have accounted for this observed change as this would have been expected to inhibit the optokinetic reaction. They concluded that an "Efferenzkopie" of the motor command was responsible for this reaction due to the persistence of the reafferent signal and given the consequent discrepancy between expected and actual sensory signals which reinforced the response rather than preventing it.

Modern View

Internal models

Internal models simulate the response of the motor system in order to estimate the outcome of a motor command.

The idea of the internal model postulates that the motor system is controlled by the constant interactions of the “plant” and the “controller.” The plant is the body part being controlled, while the internal model itself is considered part of the controller. Information from the controller, such as information from the CNS, feedback information, or in the case of this topic, the efference, is sent to the plant which moves accordingly. Internal models can be controlled through either feed-forward or feedback control. Feed-forward control computes its input into a system using only the current state and its model of the system. It does not use feedback, so it cannot correct for errors in its control. In feedback control, some of the output of the system can be fed back into the system’s input, and the system is then able to make adjustments or compensate for errors from its desired output. Two primary types of internal models exist: forward models and inverse models. These models can be combined together to solve more complex movement tasks.

Forward models

In their simplest form, forward models take the input of a motor command to the “plant” and output a predicted position of the body (Figure 1).

The motor command input to the forward model can be an efference copy, as seen in Figure 2. The output from that forward model, the predicted position of the body, is then compared with the actual position of the body. The actual and predicted position of the body may differ due to noise introduced into the system by either internal (e.g. body sensors are not perfect, sensory noise) or external (e.g. unpredictable forces from outside the body) sources. If the actual and predicted body positions differ, the difference can be fed back as an input into the entire system again so that an adjusted set of motor commands can be formed to create a more accurate movement.

Inverse models

Inverse models use the desired or actual position of the body as the input to then determine or identify the necessary motor commands. For example, in a reaching task, the desired trajectory of the arm is input into the inverse model, and the motor commands to control the arm are output (Figure 3).

Combined forward and inverse models

When used in combination with a forward model, the efference copy of the motor command output from the inverse model can be used as an input to a forward model for further predictions. If, in addition to reaching with the arm, the hand must be controlled to grab an object, an efference copy of the arm motor command can be input into a forward model to estimate the arm's predicted trajectory. With this information, the controller can then generate the appropriate motor command telling the hand to grab the object. This combination of inverse and forward models allows the CNS to take a desired action (reach with the arm), accurately control the reach and then accurately control the hand to grip an object.

Relationship to Adaptive Control theory

With the assumption that new models can be acquired and pre-existing models can be updated, the efference copy is important for the adaptive control of a movement task. Throughout the duration of a motor task, an efference copy is fed into a forward model known as a dynamics predictor whose output allows prediction of the motor output. When applying adaptive control theory techniques to motor control, efference copy is used in indirect control schemes as the input to the reference model.

Experimental Examples

Efference Copy and the Coriolis effect

Efference copy relates to Coriolis effect in a manner that allows for learning and correction of errors experienced from unanticipated Coriolis forces. During self- generated rotational movements there is a learned CNS anticipation of Coriolis effects, mediated by generation of an appropriate efference copy that can be compared to re-afferent information.

Efference Copy and gaze stability

It has been proposed that efference copy has an important roll in maintaining gaze stability with active head movement by augmenting the vestibulo-occular reflex (aVOR) during dynamic visual acuity testing.

Effererence Copy in Tickling

Experiments have been conducted wherein subjects' feet are tickled both by themselves and with a robotic arm controlled by their own arm movements. These experiments have shown that people find a self-produced tickling motion of the foot to be much less “tickly” than a tickling motion produced by an outside source. They have postulated that this is because when a person sends a motor command to produce the tickling motion, the efference copy anticipates and cancels out the sensory outcome. This idea is further supported by evidence that a delay between the self-produced tickling motor command and the actual execution of this movement (mediated by a robotic arm) causes an increase in the perceived tickliness of the sensation. This shows that when the efference copy is incompatible with the afference, the sensory information is perceived as if it were exafference. Therefore, it is theorized that it is not possible to tickle ourselves because when the predicted sensory feedback (efference copy) matches the actual sensory feedback, the actual feedback will be attenuated. If the predicted sensory feedback does not match the actual sensory feedback, whether caused by a delay (as in the mediation by the robotic arm) or by external influences from the environment, the brain cannot predict the tickling motion on the body and a more intense tickling sensation is perceived. This is the reason why one cannot tickle oneself.

Efference Copy in Grip Force

Efference copy within an internal model allows us to grip objects in parallel to a given load. In other words, the subject is able to properly grip any load that they are provided because the internal model provides such a good prediction of the object without any delay. Flanagan and Wing tested to see whether an internal model is used to predict movement-dependent loads by observing grip force changes with known loads during arm movements. They found that even when giving subjects different known loads the grip force was able to predict the load force. Even when the load force was suddenly changed the grip force never lagged in the phase relationship with the load force, therefore affirming the fact that there was an internal model in the CNS that was allowing for the proper prediction to occur. It has been suggested by Kawato that for gripping, the CNS uses a combination of the inverse and forward model. With the use of the efference copy the internal model can predict a future hand trajectory, thus allowing for the parallel grip to the particular load of the known object.

Efference Copy vs. Corollary Discharge

The contention that the CNS is involved in modulating the reafferent sensory signal generated by the action command can be viewed not only in the context of the efference copy of the command, but also in relation to the concept of corollary discharge. Corollary discharge is classically characterized as a copy of the action command used to inhibit any response to the self generated sensory signal which would interfere with the execution of the motor task. The inhibitory commands originate at the same time as the motor command and target the sensory pathway that would report any reafference to higher levels of the CNS. This is unique from the efference copy, since the corollary discharge is actually fed into the sensory pathway to cancel out the reafferent signals generated by the movement.

An example in lower vertebrates of corollary discharge is seen in mormyrid electric fish. Specifically, the knollenorgan sensor (KS) is involved with electro-communication, detecting the electric organ discharges (EOD) of other fish. Unless the reafference was somehow modulated, the KS would also detect self generated EOD’s that would interfere with interpretation of external EOD’s needed for communication between fish. However, these fish display corollary discharges that inhibit the ascending sensory pathway at the first CNS relay point. These corollary discharges are timed to arrive at the same time as the reafference from the KS to minimize the interference of self-produced EOD's with the perception of external EODs, and optimize the duration of inhibition.

More contemporary views dissociated corollary discharge from efference copy by modeling the efference copy as the input to the forward model which is used to generate the predicted sensory feedback (corollary discharge) that estimates the sensory consequences of a motor command (Figure 4). The actual sensory consequences of the motor command are used to compare with the corollary discharge to inform the CNS about external actions. The distinction between efference copy and corollary discharge is not always clear. Recent interpretations have described these effects in a more synonymous light, describing corollary discharge as not uniquely inhibitory, but also inclusive of any transient modulatory input to reafferent signals that helps the organism distinguish between self movement and external sensory input. This more inclusive definition would view efference copy and collary discharge in a more analogous role since both are essential for the CNS predicting self initiated sensory input.

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