Corollary discharge enables proprioception from lateral line sensory feedback

Animals modulate sensory processing in concert with motor actions. Parallel copies of motor signals, called corollary discharge (CD), prepare the nervous system to process the mixture of externally and self-generated (reafferent) feedback that arises during locomotion. Commonly, CD in the peripheral nervous system cancels reafference to protect sensors and the central nervous system from being fatigued and overwhelmed by self-generated feedback. However, cancellation also limits the feedback that contributes to an animal’s awareness of its body position and motion within the environment, the sense of proprioception. We propose that, rather than cancellation, CD to the fish lateral line organ restructures reafference to maximize proprioceptive information content. Fishes’ undulatory body motions induce reafferent feedback that can encode the body’s instantaneous configuration with respect to fluid flows. We combined experimental and computational analyses of swimming biomechanics and hair cell physiology to develop a neuromechanical model of how fish can track peak body curvature, a key signature of axial undulatory locomotion. Without CD, this computation would be challenged by sensory adaptation, typified by decaying sensitivity and phase distortions with respect to an input stimulus. We find that CD interacts synergistically with sensor polarization to sharpen sensitivity along sensors’ preferred axes. The sharpening of sensitivity regulates spiking to a narrow interval coinciding with peak reafferent stimulation, which prevents adaptation and homogenizes the otherwise variable sensor output. Our integrative model reveals a vital role of CD for ensuring precise proprioceptive feedback during undulatory locomotion, which we term external proprioception.

The Prefrontal-Hippocampal Comparator: Volition and Episodic Memory

This review describes recent research that is relevant to the prefrontal-hippocampal comparator model with the following conclusions: 1. Hippocampal area CA1 serves, at least in part, as an associative match-mismatch comparator. 2. Voluntary movement strengthens episodic memories for goal-directed behavior. 3. Hippocampal theta power serves as a prediction error signal during hippocampal dependent tasks. 4. The self-referential component of episodic memory in humans is mediated by the corollary discharge (the efference copy of the action plan developed by prefrontal cortex and transmitted to hippocampus where it is stored as a working memory; CA1 uses this efference copy to compare the expected consequences of action to the actual consequences of action). 5. Impairments in the production or transmission of this corollary discharge may contribute to some of the symptoms of schizophrenia. Unresolved issues and suggestions for future research are discussed.

A corollary discharge mediates saccade related inhibition of single units in mnemonic structures of the human brain

Despite the critical link between visual exploration and memory, little is known about how single-unit activity (SUA) in the human mesial temporal lobe (MTL) is modulated by saccadic eye movements (SEMs). Here we characterize SEM associated SUA modulations, unit-by-unit, and contrast them to image onset, and to occipital lobe SUA. We reveal evidence for a corollary discharge (CD)-like modulatory signal that accompanies SEMs, inhibiting/exciting a unique population of broad/narrow spiking units, respectively, before and during SEMs, and with directional selectivity. These findings comport well with the timing, directional nature, and inhibitory circuit implementation of a CD. Additionally, by linking SUA to event-related potentials (ERPs), which are directionally modulated following SEMs, we recontextualize the ERP associated with SEM as a proxy for both the strength of inhibition and saccade direction, providing a mechanistic underpinning for the more commonly recorded SEM-related ERP in the human brain.

Corollary discharge promotes a sustained motor state in a neural circuit for navigation

Animals exhibit behavioral and neural responses that persist on longer time scales than transient or fluctuating stimulus inputs. Here, we report that C. elegans uses feedback from the motor circuit to a sensory processing interneuron to sustain its motor state during thermotactic navigation. By imaging circuit activity in behaving animals, we show that a principal postsynaptic partner of the AFD thermosensory neuron, the AIY interneuron, encodes both temperature and motor state information. By optogenetic and genetic manipulation of this circuit, we demonstrate that the motor state representation in AIY is a corollary discharge signal. RIM, an interneuron that is connected with premotor interneurons, is required for this corollary discharge. Ablation of RIM eliminates the motor representation in AIY, allows thermosensory representations to reach downstream premotor interneurons, and reduces the animal's ability to sustain forward movements during thermotaxis. We propose that feedback from the motor circuit to the sensory processing circuit underlies a positive feedback mechanism to generate persistent neural activity and sustained behavioral patterns in a sensorimotor transformation.

The Prefrontal-Hippocampal Comparator: Volition and Episodic Memory

This review article supports the following: (1) Hippocampal area CA1 serves as an associative match-mismatch comparator, (2) Voluntary movement strengthens episodic memories for goal-directed behavior, (3) Hippocampal theta power serves as a prediction error signal during hippocampal dependent tasks, (4) The self-referential component of episodic memory in humans is mediated by the corollary discharge (efference copy of the action plan developed by prefrontal cortex), and (5) Impairments in the production or transmission of this corollary discharge may contribute to some of the symptoms of schizophrenia. <br>

The Prefrontal-Hippocampal Comparator: Volition and Episodic Memory

This review article supports the following: (1) Hippocampal area CA1 serves as an associative match-mismatch comparator, (2) Voluntary movement strengthens episodic memories for goal-directed behavior, (3) Hippocampal theta power serves as a prediction error signal during hippocampal dependent tasks, (4) The self-referential component of episodic memory in humans is mediated by the corollary discharge (efference copy of the action plan developed by prefrontal cortex), and (5) Impairments in the production or transmission of this corollary discharge may contribute to some of the symptoms of schizophrenia. <br>

Corollary discharge prevents signal distortion and enhances sensing during locomotion

Sensory feedback during movement entails sensing a mix of externally- and self-generated stimuli (respectively, exafference and reafference). In many peripheral sensory systems, a parallel copy of the motor command, a corollary discharge, is thought to eliminate sensory feedback during behaviors. However, reafference has important roles in motor control, because it provides real-time feedback on the animal’s motions through the environment. In this case, the corollary discharge must be calibrated to enable feedback while avoiding negative consequences like sensor fatigue. The undulatory motions of fishes’ bodies generate induced flows that are sensed by the lateral line sensory organ, and prior work has shown these reafferent signals contribute to the regulation of swimming kinematics. Corollary discharge to the lateral line reduces the gain for reafference, but cannot eliminate it altogether. We develop a data-driven model integrating swimming biomechanics, hair cell physiology, and corollary discharge to understand how sensory modulation is calibrated during locomotion in larval zebrafish. In the absence of corollary discharge, lateral line afferent units exhibit the highly heterogeneous habituation rates characteristic of hair cell systems, typified by decaying sensitivity and phase distortions with respect to an input stimulus. Activation of the corollary discharge prevents habituation, reduces response heterogeneity, and regulates response phases in a narrow interval around the time of the peak stimulus. This suggests a synergistic interaction between the corollary discharge and the polarization of lateral line sensors, which sharpens sensitivity along their preferred axes. Our integrative model reveals a vital role of corollary discharge for ensuring precise feedback, including proprioception, during undulatory locomotion.