Thalamostriatal and cerebellothalamic pathways in a songbird, the Bengalese finch

Abstract

The thalamostriatal system is a major network in the mammalian brain, originating principally from the intralaminar nuclei of thalamus. Its functions remain unclear, but a subset of these projections provides a pathway through which the cerebellum communicates with the basal ganglia. Both the cerebellum and basal ganglia play crucial roles in motor control. Although songbirds have yielded key insights into the neural basis of vocal learning, it is unknown whether a thalamostriatal system exists in the songbird brain. Thalamic nucleus DLM is an important part of the song system, the network of nuclei required for learning and producing song. DLM receives output from song system basal ganglia nucleus Area X and sits within dorsal thalamus, the proposed avian homolog of the mammalian intralaminar nuclei that also receives projections from the cerebellar nuclei. Using a viral vector that specifically labels presynaptic axon segments, we show in Bengalese finches that dorsal thalamus projects to Area X, the basal ganglia nucleus of the song system, and to surrounding medial striatum. To identify the sources of thalamic input to Area X, we map DLM and cerebellar-recipient dorsal thalamus (DT ). Surprisingly, we find both DLM and dorsal anterior DT adjacent to DLM project to Area X. In contrast, the ventral medial subregion of DT projects to medial striatum outside Area X. Our results suggest the basal ganglia in the song system, like the mammalian basal ganglia, integrate feedback from the thalamic region to which they project as well as thalamic regions that receive cerebellar output.

A subcortical circuit linking the cerebellum to the basal ganglia engaged in vocal learning

“…Thus, as already suggested in a previous study ( Person et al, 2008 ), we found anatomical evidence for a disynaptic connection between the cerebellum and the song-related basal ganglia Area X: the lateral DCN sends projections to DTZ which in turn projects to Area X. Importantly, these anatomical results have been replicated very recently, confirming the existence of the DCN-DTZ-Area X pathway ( Nicholson et al, 2018 ).…”

“…Bidirectional tracer injected in the dorsal thalamus revealed a weak, but consistent, projection from the intermediate nucleus, analogous to nucleus interpositus in mammals ( Arends and Zeigler, 1991 ; Sultan and Glickstein, 2007 ; Voogd and Glickstein, 1998 ). Although the labeling was less intense in the intermediate nucleus as compared to the lateral one (suggesting weaker projections to the thalamus), both cerebellar nuclei seem to project to the dorsal thalamus, as reported in Nicholson et al (2018) . Both of them may, thereby, be involved in the cerebello-thalamo-basal ganglia pathway studied here.…”

“…In songbirds, the DTZ relays projections from the DCN to Area X and is composed of several thalamic regions as described previously by anatomical studies ( Person et al, 2008 ; Vates et al, 1997 ). One of these regions, called the dorsal medial posterior thalamic zone (DMP) projects to the medial part of the magnocellular nucleus (MMAN) ( Foster et al, 1997 ; Nicholson et al, 2018 ). MMAN is in turn implicated in a pathway ending in the song-related motor nuclei HVC (used as a proper name) and RA ( Williams et al, 2012 ).…”

“…The cerebellum also drives on-line correction during movements building on the same sensory error prediction ( Tseng et al, 2007 ) and controls the duration of movements and its prediction during sensorimotor learning ( Day et al, 1998 ; Flament and Hore, 1988 ; Izawa et al, 2012 ). The existence of a pathway from the cerebellum to the song-related basal ganglia has been suggested by previous anatomical studies in songbirds ( Person et al, 2008 ; Vates et al, 1997 ; Nicholson et al, 2018 ), but whether cerebellar circuits are involved in avian song learning and production remains unknown.…”

Functional connectivity strength within the auditory forebrain is altered by song learning and predicts song stereotypy in developing male zebra finches

“…Previously, it was known that Area X (basal ganglia) of the AFP projects to the dorsolateral nucleus of the anterior thalamus (DLM). However, it was only recently discovered that Area X also receives a projection from DLM, as well as from an adjacent region that provides cerebellar input (Hamaide et al, 2018;Nicholson, Roberts, & Sober, 2018). Although this connection does not provide a direct structural connectivity pathway between NCM and the cerebellum, it does at least establish a structural link between the cerebellum and the song network.…”