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GABAergic and non-GABAergic projections to the superior colliculus from the auditory brainstem

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Abstract

The superior colliculus (SC) contains an auditory space map that is shaped by projections from several subcortical auditory nuclei. Both GABAergic (inhibitory) and excitatory cells contribute to these inputs, but there are contradictory reports regarding the sources of these inputs. We used retrograde tracing techniques in guinea pigs to identify cells in the auditory brainstem that project to the SC. We combined retrograde tracing with immunohistochemistry for glutamic acid decarboxylase (GAD) to identify putative GABAergic cells that participate in this pathway. Following a tracer injection in the SC, the nucleus of the brachium of the inferior colliculus (NBIC) contained the most labeled cells, followed by the inferior colliculus (IC). Smaller populations were observed in the sagulum, paralemniscal area, periolivary nuclei and ventrolateral tegmental nucleus. Overall, only 10% of the retrogradely labeled cells were GAD immunopositive. The presumptive inhibitory cells were observed in the NBIC, IC, superior paraolivary nucleus, sagulum and paralemniscal area. We conclude that the guinea pig SC receives input from a diverse set of auditory brainstem nuclei, some of which provide GABAergic input. These diverse origins of input to the SC likely represent a variety of functions. Inputs from the NBIC and IC likely provide spatial information for guiding orienting behaviors. Inputs from subcollicular nuclei are less likely to provide spatial information; rather, they may provide a shorter route for auditory information to reach the SC, and could generate avoidance or escape responses to an external threat.

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Abbreviations

AQ:

Cerebral aqueduct

cMRF:

Central mesencephalic reticular formation

D:

Dorsal periolivary nucleus

DCN:

Dorsal cochlear nucleus

DL:

Dorsolateral periolivary nucleus

DLL:

Dorsal nucleus of the lateral lemniscus

DpG/W:

Deep gray/white layers of the superior colliculus

FG:

FluoroGold

GAD:

Glutamic acid decarboxylase

GAD+ :

GAD immunopositive

GAD− :

GAD immunonegative

GB:

Green beads

grca:

Granule cell area of cochlear nucleus

IC:

Inferior colliculus

ICc:

Central nucleus of the inferior colliculus

ICd:

Dorsal cortex of the inferior colliculus

IClc:

Lateral cortex of the inferior colliculus

ICrp:

Rostral pole of the inferior colliculus

ICT:

Intercollicular tegmentum

ILL:

Intermediate nucleus of the lateral lemniscus

InG/W:

Intermediate gray/white layers of the superior colliculus

LSO:

Lateral superior olive

LTB:

Lateral nucleus of the trapezoid body

MSO:

Medial superior olivary nucleus

MTB:

Medial nucleus of the trapezoid body

NBIC:

Nucleus of the brachium of the inferior colliculus

op:

Optic layer of the superior colliculus

PAG:

Periaqueductal gray

PL:

Paralemniscal area

PN:

Pontine nuclei

RB:

Red beads

Sag:

Sagulum

SC:

Superior colliculus

scp:

Superior cerebellar peduncle

SOC:

Superior olivary complex

SPN:

Superior paraolivary nucleus

SuG:

Superficial gray layer of the superior colliculus

VCN:

Ventral cochlear nucleus

VLL:

Ventral nucleus of the lateral lemniscus

VLTg:

Ventrolateral tegmental nucleus

VTB:

Ventral nucleus of the trapezoid body

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Acknowledgements

Supported by National Institutes of Health Grant R01 DC004391. We gratefully acknowledge Colleen Sowick for technical assistance and Dr. Denise Inman for critical feedback on an earlier draft of the manuscript.

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  1. Department of Anatomy and Neurobiology, Northeast Ohio Medical University, 4209 State Route 44, PO Box 95, Rootstown, OH, USA

    Jeffrey G. Mellott, Nichole L. Beebe & Brett R. Schofield

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  1. Jeffrey G. Mellott
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  2. Nichole L. Beebe
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  3. Brett R. Schofield
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All authors contributed to data generation and analysis. JGM and BRS designed the experiments and wrote the paper.

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Correspondence to Brett R. Schofield.

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Mellott, J.G., Beebe, N.L. & Schofield, B.R. GABAergic and non-GABAergic projections to the superior colliculus from the auditory brainstem. Brain Struct Funct 223, 1923–1936 (2018). https://doi.org/10.1007/s00429-017-1599-4

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