Abstract
Ascending and descending information is relayed through the thalamus via strong, “driver” pathways. According to our current knowledge, different driver pathways are organized in parallel streams and do not interact at the thalamic level. Using an electron microscopic approach combined with optogenetics and in vivo physiology, we examined whether driver inputs arising from different sources can interact at single thalamocortical cells in the rodent somatosensory thalamus (nucleus posterior, POm). Both the anatomical and the physiological data demonstrated that ascending driver inputs from the brainstem and descending driver inputs from cortical layer 5 pyramidal neurons converge and interact on single thalamocortical neurons in POm. Both individual pathways displayed driver properties, but they interacted synergistically in a time-dependent manner and when co-activated, supralinearly increased the output of thalamus. As a consequence, thalamocortical neurons reported the relative timing between sensory events and ongoing cortical activity. We conclude that thalamocortical neurons can receive 2 powerful inputs of different origin, rather than only a single one as previously suggested. This allows thalamocortical neurons to integrate raw sensory information with powerful cortical signals and transfer the integrated activity back to cortical networks.
Highlights
Thalamic activity is indispensable for normal cortical function (Steriade et al 1997; Jones 2007)
To test whether driver afferents of cortical and brainstem origin can innervate the same thalamic territories or converge on single thalamocortical cells, we labeled layer 5 (L5) input from the somatosensory cortex by anterograde tracing and the brainstem inputs by type 2 vesicular glutamate transporter immunocytochemistry a well-established marker of subcortical excitatory inputs (Fremeau et al 2001; Herzog et al 2001; Land et al 2004; Lavallee et al 2005; Graziano et al 2008)
We examined whether subcortical inputs were present in the entire posterior nucleus of the thalamus (POm) since as a recent work in primates (Rovó et al 2012) indicates large thalamic regions lack vesicular glutamate transporter type 2 (vGluT2)-positive inputs
Summary
Thalamic activity is indispensable for normal cortical function (Steriade et al 1997; Jones 2007). In the present model of information flow through the thalamus, separation of parallel channels is achieved by a simple wiring principle, a single thalamic relay cell is innervated by a single type of sensory input (Steriade et al 1997). These afferents form few, but powerful, giant terminals (drivers), which establish several synapses on the proximal dendrites of thalamic relay cells. Drivers carrying distinct types of messages do not converge in the thalamus; these messages are rather integrated at the level of sensory cortices (Sherman and Guillery 2006)
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