Thalamic relays and cortical functioning

Abstract

Studies on the visual thalamic relays, the lateral geniculate nucleus and pulvinar, provide three key properties that have dramatically changed the view that the thalamus serves as a simple relay to get information from subcortical sites to cortex. First, the retinal input, although a small minority (7%) in terms of numbers of synapses onto geniculate relay cells, dominates receptive field properties of these relay cells and strongly drives them; 93% of input thus is nonretinal and modulates the relay in dynamic and important ways related to behavioral state, including attention. We call the retinal input the driver input and the nonretinal, modulator input, and their unique morphological and functional differences allow us to recognize driver and modulator input to many other thalamic relays. Second, much of the modulation is related to control of a voltage-gated, low threshold Ca²⁺ conductance that determines response properties of relay cells —burst or tonic — and this, among other things, affects the salience of information relayed. Third, the lateral geniculate nucleus and pulvinar (a massive but generally mysterious and ignored thalamic relay), are examples of two different types of relay: the LGN is a first order relay, transmitting information from a subcortical driver source (retina), while the pulvinar is mostly a higher order relay, transmitting information from a driver source emanating from layer 5 of one cortical area to another area. Higher order relays seem especially important to general corticocortical communication, and this view challenges the conventional dogma that such communication is based on direct corticocortical connections. In this sense, any new information reaching a cortical area, whether from a subcortical source or another cortical area, benefits from a thalamic relay. Other examples of first and higher order relays also exist, and generally higher order relays represent the majority of thalamus. A final property of interest emphasized in chapter 17 by Guillery (2005) is that most or all driver inputs to thalamus, whether from a subcortical source or from layer 5 of cortex, are axons that branch, with the extrathalamic branch innervating a motor or premotor region in the brainstem, or in some cases, spinal cord. This suggests that actual information relayed by thalamus to cortex is actually a copy of motor instructions (Guillery, 2005). Overall, these features of thalamic relays indicate that the thalamus not only provides a behaviorally relevant, dynamic control over the nature of information relayed, it also plays a key role in basic corticocortical communication.

Introduction

Virtually all information reaching cortex, and thus conscious perception, must first pass through thalamus. It thus follows that the thalamus sits in a strategically vital position for brain functioning. One would think this enough to ensure that the thalamus was constantly a major focus of neuroscience research, but that has not been so. Indeed, we have recently emerged from the dark ages of thinking about thalamus: the prevalent idea being that its main purpose during normal waking behavior was simply to relay information from the periphery to cortex, a relay function that was machine-like, unvarying, and rather boring. According to this view, the thalamus only behaved in an interesting fashion during sleep or certain pathological conditions, such as epilepsy (Steriade and Llinaás, 1988; Steriade et al., 1993; McCormick and Bal, 1997), but this aspect of thalamic functioning, while interesting and still viable, is beyond the scope of the present study. Rather, the focus here is on the more recent finding that the thalamus plays an interesting and dynamic role during normal, waking behavior of the animal, and there are three aspects to this. First, it is considered that the thalamus provides a changeable relay of information to cortex, the purpose of which is to adjust the nature of relayed information to varying behavioral demands. Second, the thalamus serves not only to relay peripheral information to cortex, but it continues to play a vital role in further cortical processing of this information by acting as a central link in various corticothalamocortical routes of information processing. Third, most or all inputs to thalamus that are relayed to cortex carry information about ongoing motor instructions, so that the main role of thalamic relays is to provide a copy to cortex of these instructions. This last point has enormous implications for cortical functioning, and has been discussed in detail in Chapter 17 of this book (Guillery, 2005).

The vast majority of detailed information we have about the cell and circuit properties of the thalamus comes from studies of the lateral geniculate nucleus, which is the thalamic relay of retinal input to cortex. Studies of the lateral geniculate nucleus derive mostly from carnivores, rodents, and primates. Fortunately, this nucleus has served as an excellent model for thalamus, and all of the major concepts learned from study of this relay that are described below apply widely to thalamus.