Whisker-related circuitry in the trigeminal nucleus principalis: Ultrastructure

Abstract

Trigeminal (V) nucleus principalis (PrV) is the requisite brainstem nucleus in the whisker-to-barrel cortex model system that is widely used to reveal mechanisms of map formation and information processing. Yet, little is known of the actual PrV circuitry. In the ventral "barrelette" portion of the adult mouse PrV, relationships between V primary afferent terminals, thalamic-projecting PrV neurons, and gamma-aminobutyric acid (GABA)-ergic terminals were analyzed in the electron microscope. Primary afferents, thalamic-projecting cells, and GABAergic terminals were labeled, respectively, by Neurobiotin injections in the V ganglion, horseradish peroxidase injections in the thalamus, and postembedding immunogold histochemistry. Primary afferent terminals (Neurobiotin- and glutamate-immunoreactive) display asymmetric and multiple synapses predominantly upon the distal dendrites and spines of PrV cells that project to the thalamus. Primary afferents also synapse upon GABAergic terminals. GABAergic terminals display symmetric synapses onto primary afferent terminals, the somata and dendrites (distal, mostly) of thalamic-projecting neurons, and GABAergic dendrites. Thus, primary afferent inputs through the PrV are subject to pre- and postsynaptic GABAergic influences. As such, circuitry exists in PrV "barrelettes" for primary afferents to directly activate thalamic-projecting and inhibitory local circuit cells. The latter are synaptically associated with themselves, the primary afferents, and with the thalamic-projecting neurons. Thus, whisker-related primary afferent inputs through PrV projection neurons are pre- and postsynaptically modulated by local circuits.

Whisker-related circuitry in the trigeminal nucleus principalis: Topographic precision

“…Moreover, further differences exist between V ganglion and PrV cells in the extent to which they display spontaneous activity, directional sensitivity, and tonic vs. phasic adaptation to a sustained stimulus. In a recent ultrastructural analysis of identified circuits within PrV barrelettes (Xiang et al 2014), we suggested five possible ways that the receptive fields of PrV cells could be so transformed: (1) Terminal clusters from primary afferents innervating neighboring whiskers overlap in the PrV's somatotopic coronal plane; thus, single whisker afferents span multiple barrelettes.…”

Cortical modulation of sensory flow during active touch in the rat whisker system

“…In rats, sensory gating might act via PAD as well, although, the existence of a PAD-based mechanism is uncertain. The synaptic elements potentially suitable for PAD have been demonstrated 43 , but neither have their functional properties been shown to be suited for PAD nor have their origins been delineated. Pr5 itself contains only a small number of inhibitory neurons 32 , and our finding of a lack of gating and motor-related responses in Sp5i putative inhibitory neurons does not support a mechanism based on an inhibitory cascade involving Sp5i 28 , although these projections could still play a potential role, e.g.…”

“…Many unexplored inhibitory brainstem targets of corticofugal projections may in principle be involved, amongst them Sp5c, which has been reported to project also directly to Pr5 32 . Other than PAD, mechanisms such as postsynaptic modulation might also play a role particularly given that primary afferents terminate on distal dendrites and spines of Pr5 neurons 43 . Finally, corticofugal projections to Pr5 27 may act directly (e.g.…”