Cortical and Collicular Inputs to Cells in the Rat Paralaminar Thalamic Nuclei Adjacent to the Medial Geniculate Body

Abstract

The paralaminar nuclei, including the medial division of the medial geniculate nucleus, surround the auditory thalamus medially and ventrally. This multimodal area receives convergent inputs from auditory, visual, and somatosensory structures and sends divergent outputs to cortical layer 1, amygdala, basal ganglia, and elsewhere. Studies implicate this region in the modulation of cortical 40-Hz oscillations, cortical information binding, and the conditioned fear response. We recently showed that the basic anatomy and intrinsic physiology of paralaminar cells are unlike that of neurons elsewhere in sensory thalamus. Here we evaluate the synaptic inputs to paralaminar cells from the inferior and superior colliculi and the cortex. Combined physiological and anatomical evidence indicates that paralaminar cells receive both excitatory and inhibitory inputs from both colliculi and excitatory cortical inputs. Excitatory inputs from all three sources typically generate small summating EPSPs composed of AMPA and NMDA components and terminate primarily on smaller dendrites and occasionally on dendritic spines. The cortical input shows strong paired-pulse facilitation (PPF), whereas both collicular inputs show weak PPF or paired-pulse depression (PPD). EPSPs of cells with no low-threshold calcium conductance do not evoke a burst response when the cell is hyperpolarized. Longer-latency EPSPs were seen and our evidence indicates that these arise from axon collateral inputs of other synaptically activated paralaminar cells. The inhibitory collicular inputs are GABAergic, activate GABA(A) receptors, and terminate on dendrites. Their activation can greatly alter EPSP-generated spike number and timing.

Topography and physiology of ascending streams in the auditory tectothalamic pathway

“…Previous investigations of the auditory tectothalamic pathways used preparations that only preserved the afferent fibers (e.g., brachium of the IC, corticothalamic fibers) to the MGB (9,11,13,24). Despite the lack of intact structures innervating the MGB in these earlier preparations, the parallel organization of the tectothalamic pathways allowed some specificity of responses from fiber stimulation (12,24).…”

“…Anatomical studies suggest that the inhibitory feedforward projections to the MGB arise throughout the IC (9,10), and physiological investigations find several distinct classes of excitatory and inhibitory inputs (11)(12)(13). However, the topographic organization of excitatory and inhibitory inputs in the tectothalamic pathways is largely undefined.…”

Auditory System

“…3 and 18). The MG also receives descending fibers from the auditory cortex (Hazama et al, 2004;Kimura et al, 2005Kimura et al, , 2007aSmith et al, 2007) and reticular thalamic nucleus (Rt; Shosaku and Sumitomo, 1983;Kimura et al, 2007b) (Figs. 24 and 29).…”

Circuits for active vision : parallel tectothalamocortical visual pathways in the mouse.

“…Similar examples of driver-like convergence illustrate the complexity of thalamic organization. The dorsal thalamus may be divided not only into "first order" (driven by ascending peripheral input) or "higher order" (driven by descending cortical input) nuclei (Guillery and Sherman, 2002), but also "second order" nuclei driven by convergent, ascending inputs (Kelly et al, 2003;Smith et al, 2007;Chomsung et al, 2008;Masterson et al, 2009Masterson et al, , 2010, or nuclei that contain unique combinations of ascending and descending driver-like inputs (Baldauf et al, 2005;Rovo et al, 2012;Groh et al, 2014). Such diversity may dramatically increase the computational capabilities of the thalamus, reflecting its essential roles in sensory, motor, and sensory-motor circuits.…”