Drivers from the deep: the contribution of collicular input to thalamocortical processing

Abstract

A traditional view of the thalamus is that it is a relay station which receives sensory input and conveys this information to cortex. This sensory input determines most of the properties of first order thalamic neurons, and so is said to drive, rather than modulate, these neurons. This holds as a rule for first order thalamic nuclei, but in contrast, higher order thalamic nuclei receive much of their driver input back from cerebral cortex. In addition, higher order thalamic neurons receive inputs from subcortical movement-related centers. In the terminology popularized from studies of the sensory system, can we consider these ascending motor inputs to thalamus from subcortical structures to be modulators, subtly influencing the activity of their target neurons, or drivers, dictating the activity of their target neurons? This chapter summarizes relevant evidence from neuronal recording, inactivation, and stimulation of pathways projecting from the superior colliculus through thalamus to cerebral cortex. The study concludes that many inputs to the higher order nuclei of the thalamus from subcortical oculomotor areas -from the superior colliculus and probably other midbrain and pontine regions -should be regarded as motor drivers analogous to the sensory drivers at the first order thalamic nuclei. These motor drivers at the thalamus are viewed as being at the top of a series of feedback loops that provide information on impending actions, just as sensory drivers provide information about the external environment.

Rhythmic syllable-related activity in a songbird motor thalamic nucleus necessary for learned vocalizations

“…Information about movements can originate from both sensory receptors (peripheral reafference) [65,66], including those in muscles, as well as from internal representations of those movements, known as either collateral discharge or efference copy [67,68]. It is likely that much of the information the brain receives regarding self-generated movements is relayed to the cortex via the thalamus [69]. …”

Parallel Driving and Modulatory Pathways Link the Prefrontal Cortex and Thalamus

“…Driving input, presumably originating in cortical layer V, resembles projections from peripheral sensory systems, or from subcortical movement-related centers to the thalamus. All of these projections terminate in clusters of large boutons, form synapses with relay cells, and interact with ionotropic glutamate receptors in the thalamus [8], [9], [12], [15], [40]. The cortico-thalamic pathway originating from large layer V neurons also innervates motor centers in the brainstem and spinal cord, and is presumed to carry a copy of motor commands to the thalamus [41]–[43].…”

Bottom-Up Activation of the Vocal Motor Forebrain by the Respiratory Brainstem

“…In the only well characterized example of a brainstem to forebrain contribution to motor control, projections from the superior colliculus have been suggested to convey corollary discharge signals regarding impending eye movements back to the frontal eye fields Wurtz, 2002, 2004a,b;Wurtz et al, 2005). Similar to the inability of birds to produce syllable sequences after Uva lesions, monkeys with lesions of the thalamic relay nucleus are impaired in their ability to perform saccade sequences even though single eye saccade performance is unaffected (Sommer and Wurtz, 2002).…”

“…With the recent exception of the motor control of eye movement (Sommer and Wurtz, 2004a,b;Wurtz et al, 2005), little is known about how brainstem nuclei involved in motor output might influence the generation of motor commands by forebrain structures. This is particularly true for vocal motor behavior, where respiratory control is intimately linked to vocal production (Jür-gens, 2002;Goller and Cooper, 2004).…”