Ultrastructure, synaptic organization, and molecular components of bushy cell networks in the anteroventral cochlear nucleus of the rhesus monkey

Abstract

Bushy cells (BCs) process auditory information in the ventral cochlear nucleus (VCN). Yet, most neuroanatomical findings come from studies in cats and rodents, and the ultrastructural morphological features of BCs in humans and higher nonhuman primates are unknown. In this study, we combined histological, immunocytochemical, and ultrastructural methods to examine the morphology and synaptic organization of BCs in the rhesus monkey VCN. We observed that BCs were organized in a complex neural network that appears to interconnect the cells. The fine structure of BC somata and dendrites, as well as their synaptic inputs, are similar to those in other mammals. We found that BCs received numerous endbulb-like VGLUT1- and VGLUT2-immunopositive endings. In addition, they expressed glutamate AMPA (GluR2/3 and GluR4), NMDA (NR1), delta1/2 receptor subunits, and the α1 subunit of the glycine receptor. These receptor types and subunits mediate fast excitatory synaptic transmission from the cochlea and inhibitory neurotransmission from noncochlear inputs. Parvalbumin immunostaining and semithin sections showed that BC dendrites are oriented toward neighboring BC somas to form neuronal clusters. Within the cluster, the incoming inputs established multiple, divergent synaptic contacts. Thus, BCs were connected by specialized dendrosomatic and somasomatic membrane junctions. Our results indicate that the cytoarchitectural organization of BCs is well conserved between primates and other mammalian species.

Connexin36 expression in major centers of the auditory system in the CNS of mouse and rat: Evidence for neurons forming purely electrical synapses and morphologically mixed synapses

“…This conclusion is consistent with our report of ultrastructurally characterized gap junctions between the somata of bushy cells in the rat AVCN (Gómez-Nieto and Rubio, 2009) as well as the AVCN of rhesus monkey (Gómez-Nieto and Rubio, 2011). The existence of somato-somatic and somato-dendritic gap junctions in the AVCN was reported much earlier by Sotelo and colleagues (Sotelo et al, 1976), but in this early study the cell types involved were not identified, though they too found that these gap junctions persisted after 8 th nerve deafferentation.…”

“…This may occur in the auditory system because, among the cell types on which we find mixed synapses, individual cells can receive collateral inputs from single auditory afferents. In the AVCN, for example, fibers forming endbulb synapses on the soma of one bushy cell can form synapses on the dendrite of another bushy cell, the so called ‘synaptic dyads’ (Gómez-Nieto and Rubio, 2009, 2011). Further, we have found examples of one auditory ending synapsing with two bushy somata (Rubio, unpublished observations), which could allow electrical coupling of those cells by way of these presynaptic fibers, even further contributing to the potential for synchronous activity of bushy cells.…”

“…However, Cx36 protein was not detected in the cochlear nucleus of mouse, but was reported to occur in this nucleus of brown bats (Howowitz et al, 2008). More recently, ultrastructural studies have described neuronal gap junctions between the somata of bushy cells in the AVCN of rat and monkey (Gómez-Nieto and Rubio, 2009, 2011). In addition, in vitro electrophysiological approaches have demonstrated functional electrical coupling between stellate cells and fusiform cells in the dorsal cochlear nucleus (DCN) (Apostolides and Trussell, 2013).…”

Auditory System

“…A detailed analysis of the geometry and synaptic organization of the dendritic arbors of bushy cells have demonstrated that bushy cells dendrites participate in a large number of compartmentalized excitatory and inhibitory synaptic interactions (Gómez-Nieto and Rubio, 2009Rubio, , 2011. The dendritic inputs on bushy cells are of both cochlear and noncochlear origin, and their proportion and distribution are dependent on the branching pattern and orientation of the dendritic arbor (Fig.…”

Listening to another sense: somatosensory integration in the auditory system

“…Specific sensory projection neurons to the CN originate in the trigeminal ganglion and the spinal trigeminal nucleus (Sp5) (Haenggeli, et al, 2005, Shore, et al, 2000, Zhou and Shore, 2004), dorsal root ganglion and dorsal column nuclei (Itoh, et al, 1987, Zeng, et al, 2011, Zhan, et al, 2006, Zhou and Shore, 2004), saccule and vestibular nucleus (Barker, et al, 2012, Bukowska, 2002, Burian and Gstoettner, 1988). Most of the projections from non-auditory sensory ganglia and brainstem nuclei terminate in the CN granule cell domain (GCD), but some of them end in magnocellular CN regions (Gomez-Nieto and Rubio, 2011). Anterograde and retrograde tract tracing demonstrate that the trigeminal ganglia directly innervate neurons in the cochlea, middle ear, shell area of the ventral CN (VCN) including the GCD and the fusiform cell layer of the dorsal CN (DCN).…”