Influence of the thalamus on spatial visual processing in frontal cortex

By Marc A. Sommer, Robert Wurtz. Nature, 2006

510 citations recorded by the source corpus.

Each of our movements activates our own sensory receptors, and therefore keeping track of self-movement is a necessary part of analysing sensory input. One way in which the brain keeps track of self-movement is by monitoring an internal copy, or corollary discharge, of motor commands. This concept could explain why we perceive a stable visual world despite our frequent quick, or saccadic, eye movements: corollary discharge about each saccade would permit the visual system to ignore saccade-induced visual changes. The critical missing link has been the connection between corollary discharge and visual processing. Here we show that such a link is formed by a corollary discharge from the thalamus that targets the frontal cortex. In the thalamus, neurons in the mediodorsal nucleus relay a corollary discharge of saccades from the midbrain superior colliculus to the cortical frontal eye field. In the frontal eye field, neurons use corollary discharge to shift their visual receptive fields spatially before saccades. We tested the hypothesis that these two components—a pathway for corollary discharge and neurons with shifting receptive fields—form a circuit in which the corollary discharge drives the shift. First we showed that the known spatial and temporal properties of the corollary discharge predict the dynamic changes in spatial visual processing of cortical neurons when saccades are made. Then we moved from this correlation to causation by isolating single cortical neurons and showing that their spatial visual processing is impaired when corollary discharge from the thalamus is interrupted. Thus the visual processing of frontal neurons is spatiotemporally matched with, and functionally dependent on, corollary discharge input from the thalamus. These experiments establish the first link between corollary discharge and visual processing, delineate a brain circuit that is well suited for mediating visual stability, and provide a framework for studying corollary discharge in other sensory systems.

Subfields: Cognitive Neuroscience, Molecular Biology

View Paper: https://www.semanticscholar.org/paper/b9a02099a554be1f9cb7ca6004c2b83b27bc7738

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Citations in the corpus

Computational mechanisms of sensorimotor control. (2011, unknown): “Research on eye movements has also provided strong evidence for the use of efference copy in a manner that illustrates many of the properties of the forward model, in particular for this transformation from motor to sensory representation (Roy and Cullen, 2001, 2004; Sommer and Wurtz, 2002, 2006).”
The Effect of Imagination on Stimulation: The Functional Specificity of Efference Copies in Speech Processing (2013, background): “…(1910) and the biologists Von Holst and Mittelstaedt (1950, 1973), and the importance and utility of the idea now extends to visual perception (Sommer & Wurtz, 2006, 2008; Gauthier, Nommay, & Vercher, 1990a, 1990b), motor control (Todorov & Jordan, 2002; Kawato, 1999; Miall & Wolpert, 1996),…”
Fundamental components of attention. (2007, background): “In the FEF, these corollary discharges shift the locations of visual receptive fields tens of ms before each eye saccade so that FEF neurons represent stimuli at the future locations of their receptive fields (Sommer & Wurtz 2006).”
Neuronal mechanisms of visual stability. (2008, background): “If there were such a slide or expansion, there would be activity between the RF and the FF whereas with the jump there would not be.”
A computational model of inhibitory control in frontal cortex and basal ganglia. (2011, background): “Because the extended model involves multiple components, we progressively introduce each part, beginning with its core and then describing how each new component contributes additional functionality.”
Corollary discharge across the animal kingdom (2008, unknown): “At least some of this CD arises from a pathway that ascends from the midbrai”
microsaccade and saccade generation Similarity of superior colliculus involvement in (2012, background): “…al. 2008; Reppas et al. 2002) and sensorymotor (Bremmer et al. 2009; Duhamel et al. 1992; Ibbotson and Krekelberg 2011; Phongphanphanee et al. 2011; Sommer and Wurtz 2006) areas and an equally rich literature on the effects of saccades on behavioral and perceptual performance (e.g., Cai et al.…”
Compensating time delays with neural predictions: are predictions sensory or motor? (2009, background): “According to a recent proposal, the pathway carrying the motor command information from the superior colliculus via the thalamus to the frontal cortical areas (frontal eye ﬁeld) contains the mechanism responsible for maintaining visual stability during saccades (Sommer & Wurtz 2006).”
Error correction, sensory prediction, and adaptation in motor control. (2010, background): “…(Kording et al., 2004), feedback responses to perturbations to the properties of the target (Izawa and Shadmehr, 2008), and perceptual estimates of position and velocity in the presence of noise (Ernst and Banks, 2002; Weiss et al., 2002; Stocker and Simoncelli, 2006; Sato et al., 2007).”
Early multisensory integration of self and source motion in the auditory system (2016, background): “In the visual system, the organism has to discriminate between movement of the visual scene and movement of the eyes (4, 5).”