Effects of arousal and movement on secondary somatosensory and visual thalamus

Neocortical sensory areas have associated primary and secondary thalamic nuclei. While primary nuclei transmit sensory information to cortex, secondary nuclei remain poorly understood. We recorded juxtasomally from secondary somatosensory (POm) and visual (LP) nuclei of awake mice while tracking whisking and pupil size. POm activity correlated with whisking, but not precise whisker kinematics. This coarse movement modulation persisted after facial paralysis and thus was not due to sensory reafference. This phenomenon also continued during optogenetic silencing of somatosensory and motor cortex and after lesion of superior colliculus, ruling out a motor efference copy mechanism. Whisking and pupil dilation were strongly correlated, possibly reflecting arousal. Indeed LP, which is not part of the whisker system, tracked whisking equally well, further indicating that POm activity does not encode whisker movement per se. The semblance of movement-related activity is likely instead a global effect of arousal on both nuclei. We conclude that secondary thalamus monitors behavioral state, rather than movement, and may exist to alter cortical activity accordingly.

The Efference Copy Signal as a Key Mechanism for Consciousness

Animals need to distinguish sensory input caused by their own movement from sensory input which is due to stimuli in the outside world. This can be done by an efference copy mechanism, a carbon copy of the movement-command that is routed to sensory structures. Here I tried to link the mechanism of the efference copy with the idea of the philosopher Thomas Reid that the senses would have a double province, to make us feel, and to make us perceive, and that, as argued by psychologist Nicholas Humphrey, the former would identify with the signals from bodily sense organs with an internalized evaluative response, i.e., with phenomenal consciousness. I discussed a possible departure from the classical implementation of the efference copy mechanism that can effectively provide the senses with such a double province, and possibly allow us some progress in understanding the nature of consciousness.

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.

Saccadic suppression in schizophrenia

About 40% of schizophrenia patients report discrete visual disturbances which could occur if saccadic suppression, the decrease of visual sensitivity around saccade onset, is impaired. Two mechanisms contribute to saccadic suppression: efference copy processing and backwards masking. Both are reportedly altered in schizophrenia. However, saccadic suppression has not been investigated in schizophrenia. 17 schizophrenia patients and 18 healthy controls performed a saccadic suppression task using a Gabor stimulus with individually adjusted contrast, which was presented within an interval 300 ms around saccade onset. Visual disturbance scores were higher in patients than controls, but saccadic suppression strength and time course were similar in both groups with lower saccadic suppression rates being similarly related to smaller saccade amplitudes. Saccade amplitudes in the saccadic suppression task were reduced in patients, in contrast to unaltered amplitudes during a saccade control task. Notably, smaller saccade amplitudes were related to higher visual disturbances scores in patients. Saccadic suppression performance was unrelated to symptom expression and antipsychotic medication. Unaltered saccadic suppression in patients suggests sufficiently intact efference copy processing and backward masking as required for this task. Instead, visual disturbances in patients may be related to restricted saccadic amplitudes arising from cognitive load while completing a task.

Erasing motion: Scrambling direction selectivity in visual cortex during saccades

A prominent feature of sensory processing is the ability to distinguish whether the activation of the sensory periphery is caused by changes in the external world or by the animal's own actions. Saccades, rapid eye movements executed by animals across phyla, cause the visual scene to momentarily shift on the retina. The mechanisms by which visual systems differentiate between motion of the visual scene induced by saccades from motion due to changes in the external world are not fully understood. Here, we discovered that in mouse primary visual cortex (V1), the two types of motion evoke distinct patterns of activity across the population of neurons. As a result, a decoder of motion direction trained on the response to motion in the external world fails to generalize when tested on the response to saccades that induce similar motion on the retina. This is because during saccades, V1 combines the visual input with a strong non-visual input arriving from the pulvinar nucleus of the thalamus. This non-visual input is an efference copy - a copy of the oculomotor command that differs depending on the direction of the saccades. Silencing the pulvinar prevented the non-visual input from reaching V1, such that the pattern of activity in V1 was now similar no matter whether the motion was generated in the external world or by saccades. Thus, the pulvinar input to V1 ensures differential responses to the external and self-generated motion and may prevent downstream areas from extracting motion information about visual stimulus shifts generated by saccades. Changing the pattern of evoked activity through an efference copy may be a general mechanism that enables sensory cortices in mammals to distinguish between external and self-generated stimuli.

Action-based predictions affect visual perception, neural processing, and pupil size, regardless of temporal predictability

Sensory consequences of one’s own action are often perceived as less intense, and lead to reduced neural responses, compared to externally generated stimuli. Presumably, such sensory attenuation is due to predictive mechanisms based on the motor command (efference copy). However, sensory attenuation has also been observed outside the context of voluntary action, namely when stimuli are temporally predictable. Here, we aimed at disentangling the effects of motor and temporal predictability-based mechanisms on the attenuation of sensory action consequences. During fMRI data acquisition, participants (N = 25) judged which of two visual stimuli was brighter. In predictable blocks, the stimuli appeared temporally aligned with their button press (active) or aligned with an automatically generated cue (passive). In unpredictable blocks, stimuli were presented with a variable delay after button press/cue, respectively. Eye tracking was performed to investigate pupil-size changes and to ensure proper fixation. Self-generated stimuli were perceived as darker and led to less neural activation in visual areas than their passive counterparts, indicating sensory attenuation for self-generated stimuli independent of temporal predictability. Pupil size was larger during self-generated stimuli, which correlated negatively with blood oxygenation level dependent (BOLD) response: the larger the pupil, the smaller the BOLD amplitude in visual areas. Our results suggest that sensory attenuation in visual cortex is driven by action-based predictive mechanisms rather than by temporal predictability. This effect may be related to changes in pupil diameter. Altogether, these results emphasize the role of the efference copy in the processing of sensory action consequences.

Efference copy in kinesthetic perception: A copy of what is it?

A number of notions in the fields of motor control and kinesthetic perception have been used without clear definitions. In this review, we consider definitions for efference copy, percept, and sense of effort based on recent studies within the physical approach, which assumes that the neural control of movement is based on principles of parametric control and involves defining time-varying profiles of spatial referent coordinates for the effectors. The apparent redundancy in both motor and perceptual processes is reconsidered based on the principle of abundance. Abundance of efferent and afferent signals is viewed as the means of stabilizing both salient action characteristics and salient percepts formalized as stable manifolds in high-dimensional spaces of relevant elemental variables. This theoretical scheme has led recently to a number of novel predictions and findings. These include, in particular, lower accuracy in perception of variables produced by elements involved in a multi-element task compared to the same elements in single-element tasks, dissociation between motor and perceptual effects of muscle co-activation, force illusions induced by muscle vibration, and errors in perception of unintentional drifts in performance. Taken together, these results suggest that participation of efferent signals in perception frequently involves distorted copies of actual neural commands, particularly those to antagonist muscles. Sense of effort is associated with such distorted efferent signals. Distortions in efference copy happen spontaneously and can also be caused by changes in sensory signals, e.g., those produced by muscle vibration.

Locomotion-induced ocular motor behavior in larval Xenopus is developmentally tuned by visuo-vestibular reflexes

Locomotion requires neural computations to maintain stable perception of the world despite disturbing consequences of the motor behavior on sensory stability. The developmental establishment of locomotor proficiency is therefore accompanied by a concurrent maturation of gaze-stabilizing motor behaviors. Using developing Xenopus larvae, we demonstrate mutual plasticity of predictive spinal locomotor efference copies and multi-sensory motion signals with the aim to constantly ensure dynamically adequate eye movements during swimming. Following simultaneous ontogenetic onsets of locomotion, spino-ocular, optokinetic and otolith-ocular motor behaviors, locomotor efference copy-driven eye movements improve through gradually augmenting influences of semicircular canal signals. Accordingly, neuronal computations change from predominating cancelation of angular vestibulo-ocular reflexes by locomotor efference copies in young larvae to summation of these signals in older larvae. The developmental switch occurs in synchrony with the reduced efficacy of the tail-undulatory locomotor pattern generator causing gradually declining influences on the ocular motor output.

Locomotion-induced ocular motor behavior in larval Xenopus is developmentally tuned by visuo-vestibular reflexes

ABSTRACTLocomotion requires neural computations to maintain stable perception of the world despite disturbing consequences of the motor behavior on sensory stability. The developmental establishment of locomotor proficiency is therefore accompanied by a concurrent maturation of gaze-stabilizing motor behaviors. Using developing larval Xenopus, we demonstrate mutual plasticity of predictive spinal locomotor efference copies and multi-sensory motion signals with the aim to constantly ensure dynamically adequate eye movements during swimming. Following simultaneous ontogenetic onsets of locomotion, spino-ocular, optokinetic and otolith-ocular motor behaviors, locomotor efference copy-driven eye movements improve through gradually augmenting influences of semicircular canal signals. Accordingly, neuronal computations change from a predominating cancelation of angular vestibulo-ocular reflexes by locomotor efference copies in young larvae to a summation of these signals in older larvae. The developmental switch occurs in synchrony with a reduced efficacy of the tail-undulatory locomotor pattern generator causing gradually decaying influences on the ocular motor output.