Spatiotemporal Adaptation in the Corticogeniculate Loop

The thalamus is the major gate to the cortex for almost all sensory signals, for input from various subcortical sources such as the cerebellum and the mammillary bodies, and for reentrant cortical information. Thalamic nuclei do not merely relay information to the cortex but perform some operation on it while being modulated by various transmitter systems and in continuous interplay with their cortical target areas. Indeed, cortical feedback to the thalamus is the anatomically dominant input to relay cells even in those thalamic nuclei that are directly driven by sensory systems. While it is well-established that the receptive fields of cortical neurons are strongly influenced by convergent thalamic inputs of different types, the modulation effected by cortical feedback in thalamic response has been difficult to interpret. Experiments and theoretical considerations have pointed to a variety of operations of the visual cortex on the visual thalamus, the lateral geniculate nucleus (LGN), such as control of binocular disparity for stereopsis (Schmielau & Singer, 1977), attention-related gating of relay cells (Sherman & Koch, 1986), gain control of relay cells (Koch, 1987), synchronizing firing of neighboring relay cells (Sillito et al., 1994; Singer, 1994), increasing visual information in relay cells’ output (McClurkin et al., 1994), and switching relay cells from a detection to an analyzing mode (Godwin et al., 1996; Sherman, 1996; Sherman & Guillery, 1996). Nonetheless, the evidence for any particular function is still sparse and rather indirect to date. Clearly, detailed concepts of the interdependency of thalamic and cortical operation could greatly advance our knowledge about complex sensory, and ultimately cognitive, processing. Here we present a novel view on the corticothalamic puzzle by proposing that control of velocity tuning of visual cortical neurons may be an eminent function of corticogeniculate processing. The hypothesis is advanced by studying a model of the primary visual pathway in extensive computer simulations. At the heart of the model is a biophysical account of the electrical membrane properties of thalamic relay neurons (Huguenard & McCormick, 1992; McCormick & Huguenard, 1992) that includes 12 ionic conductances. Among the different effects that corticogeniculate feedback may have on relay cells, we focus on the modulation of their relay mode (between tonic and burst mode) by control of their resting membrane potential. Employing two distinct temporal-response types of geniculate relay neurons (lagged and nonlagged), we find that shifts in membrane potential affect the temporal response properties of relay cells in a way that alters the tuning of cortical cells for speed.