Auditory cortical axons contact commissural cells throughout the guinea pig inferior colliculus

Abstract

Projections from auditory cortex (AC) affect how cells in both inferior colliculi (IC) respond to acoustic stimuli. The large projection from the AC to the ipsilateral IC is usually credited with the effects in the ipsilateral IC. The circuitry underlying effects in the contralateral IC is less clear. The direct projection from the AC to the contralateral IC is relatively small. An unexplored possibility is that the large ipsilateral cortical projection contacts the substantial number of cells in the ipsilateral IC that project through the commissure to the contralateral IC. Apparent contacts between cortical boutons and commissural cells were identified in the left IC after injection of different fluorescent tracers into the left AC and the right IC. Commissural cells were labeled throughout the left IC, and many (23–34%) appeared to be contacted by cortical axons. In the central nucleus, both disc-shaped and stellate cells were contacted. Antibodies to glutamic acid decarboxylase (GAD) were used to identify GABAergic commissural cells. The majority (>86%) of labeled commissural cells were GAD-immunonegative. Despite low numbers of GAD-immunopositive commissural cells, some of these cells were contacted by cortical boutons. Nonetheless, most cortically-contacted commissural cells were GAD-immunonegative (i.e., presumably glutamatergic). We conclude that auditory cortical axons contact primarily excitatory commissural cells in the ipsilateral IC that project to the contralateral IC. These corticocollicular contacts occur in each subdivision of the ipsilateral IC, suggesting involvement of commissural cells throughout the IC. This pathway – from AC to commissural cells in the ipsilateral IC - is a prime candidate for the excitatory effects of activation of the auditory cortex on responses in the contralateral IC. Overall this suggests that the auditory corticofugal pathway is integrated with midbrain commissural connections.

Ultrastructural examination of the corticocollicular pathway in the guinea pig: a study using electron microscopy, neural tracers, and GABA immunocytochemistry

“…The present study confirms that such corticocollicular synapses exist. Preliminary studies also suggest that cortical axons directly contact commissural cells, the source of the large pathway connecting left and right IC (Nakamoto and Schofield, 2009). While GABAergic cells are thought to contribute to a number of these pathways (namely, the colliculogeniculate and commissural pathways), glutamatergic cells are predominant in the IC and its outputs.…”

The auditory corticocollicular system: Molecular and circuit-level considerations

“…There are multiple IC cell types that have been defined on morphological, connectional and physiological grounds (Peruzzi, Sivaramakrishnan and Oliver 2000; Ahuja and Wu 2007; Malmierca, Blackstad and Osen 2011). There are data suggesting that both commissural and tectothalamic cells receive axosomatic input from the AC (Coomes Peterson and Schofield 2007; Nakamoto, Sowick and Schofield 2013). However, most of the inputs from the CC system terminate in the neuropil, primarily on distal dendrites and spines (Nakamoto et al 2013), suggesting that the majority of the cell types receiving CC input and their projection targets have not yet been characterized.…”

Decision letter: Intercollicular commissural connections refine the representation of sound frequency and level in the auditory midbrain

“…The anatomical basis for these physiological observations is the CoIC, which tracer experiments demonstrate interconnect the frequency-band laminae in the IC (González- Hernández et al, 1986;Saldaña and Merchán, 1992;Malmierca et al, 1995Malmierca et al, , 2009. Immunohistochemical studies suggest that the majority of commissural fibers are excitatory, with only 10-20% labelling for the inhibitory neurotransmitter GABA (González- Hernández et al, 1996;Hernández et al, 2006;Nakamoto et al, 2013). The changes in response properties we observed are consistent with commissural input exerting both excitatory and inhibitory influences, with much greater inhibition than would be predicted from the ratio of excitatory to inhibitory fibers.…”

“…The CoIC interconnects the ICs in a systematic fashion that mirrors the spatial representation of frequency (tonotopicity) in these nuclei (Adams, 1980;González-Hernández et al, 1986;Saldaña and Merchán, 1992;Malmierca et al, 1995Malmierca et al, , 2009. These fibers are predominantly excitatory although a significant minority (∼10-20%) are GABAergic (González- Hernández et al, 1996;Hernández et al, 2006;Nakamoto et al, 2013). This commissure is the final point of interaction between the two limbs of the ascending auditory pathway prior to the auditory cortex.…”