Research paperCerebral origins of the auditory projection to the superior colliculus of the cat
Introduction
The superior colliculus (SC) has been identified as a key component in visual, visuomotor, auditory, and audiomotor processing (Apter, 1946; Hess et al., 1946; King et al., 1998; Lomber et al., 2001; Meredith and Stein, 1990; Sprague and Meikle, 1965; Stein and Meredith, 1993). Internally, the SC can be divided into superficial and deep (intermediate and deep) layers based on cytoarchitecture (Kanaseki and Sprague, 1974), neural responses properties (Meredith and Stein, 1986), and behavior (Lomber et al., 2001). The superficial layers are connected almost exclusively to visual structures (Graybiel, 1975; Harting and Guillery, 1976, 1992), whereas deeper layers receive afferents from loci processing visual, auditory, and somatosensory signals (Clemo and Stein, 1984; Harting et al., 1992; Meredith and Clemo, 1989; Tortelly et al., 1980). Accordingly, superficial layer neurons respond exclusively to visual stimulation, whereas deeper neurons respond to sight, sound and/or touch. Many neurons are responsive to more than one modality (Meredith and Stein, 1986; Peck, 1990; Stein et al., 1976; Wallace et al., 1993). Visual, auditory, and tactile maps have been identified in the SC and the maps are overlapping across modalities and layers (reviewed by Stein and Meredith, 1993).
In visual cortex, areas involved in orienting the head and eyes to a visual stimulus have direct projections to the SC (Harting et al., 1992; Lomber and Payne, 2004). Previous studies have demonstrated that the deeper layers of the SC are critical for motor response and integration, primarily concerned with head and eye orientation (Casagrande and Diamond, 1974; Edwards, 1980; Stein and Meredith, 1993). Therefore, it is reasonable to hypothesize that regions of auditory cortex involved in orienting the head and eyes to an acoustic stimulus would have direct projections to the SC.
Of the thirteen commonly recognized areas of cat auditory cortex (Fig. 1A), four have been identified as critical for accurate orienting of the head and body to an acoustic target (Malhotra and Lomber, 2007, Malhotra et al., 2004, 2008). These areas include primary auditory cortex (A1), the posterior auditory field (PAF), the dorsal zone of auditory cortex (DZ), and the auditory field of the anterior ectosylvian sulcus (fAES) (Fig. 1A shaded grey). Furthermore, recent electrophysiological investigations have also identified that areas A1, DZ, and PAF play important roles in sound localization (Lee and Middlebrooks, 2013).
Previous work has identified fAES as having strong descending corticotectal inputs (Meredith and Clemo, 1989; Tortelly et al., 1980), though no study has quantified the auditory cortical projections to the SC. FAES has also been shown to be one of the areas responsible for accurate acoustic localization (Malhotra and Lomber, 2007; Malhotra et al., 2004, 2008). Interestingly, the findings of Malhotra et al. (2008) show that deactivation of either A1 or DZ alone produces partial sound localization deficits, whereas deactivation of either the posterior auditory field (PAF) or fAES produces profound sound localization deficits. These findings suggest that PAF and fAES make more significant contributions to sound localization than either A1 or DZ. This begs the questions of whether other cortical areas involved in acoustic orienting (A1, PAF, and DZ) are communicating with the SC directly, similar to fAES, or by means of a multi-synaptic corticotectal network. Furthermore, if these projections exist, what is their relative strength?
We hypothesized that cortical areas A1, PAF, DZ, and fAES, which contribute to sound localization as identified by lesion or reversible deactivation studies (Jenkins and Merzenich, 1984; Lomber and Malhotra, 2008; Malhotra and Lomber, 2007, Malhotra et al., 2004, 2008; Masterton and Diamond, 1964; Riss, 1959; Strominger, 1969), should project to the deeper layers of the SC. The present study had three goals: 1) to examine the origin of corticotectal neurons that arise in auditory cortex and project to the SC, 2) to describe the laminar pattern of connections and the ipsilateral and contralateral origins of the pathways, and 3) to confirm if these pathways originate in areas that contribute to accurate sound localization. To test our hypothesis, retrograde tracer was deposited into the superficial and deep layers of the SC which in turn labeled cortical cells of origin (Fig. 1B). Data from the present study reveals that nearly all labeled cells in auditory cortex are lateralized to the hemisphere ipsilateral to the SC injection. The vast majority of the corticotectal pathway originates in the fAES. Overall, our data partially support our hypothesis and demonstrate that, unlike the visual system, cortical areas involved in acoustic localization and orienting do not all have strong direct projections to the SC.
Section snippets
Materials and methods
Ten adult (>6 months) female domestic cats were examined. Each cat was obtained from a USDA licensed commercial animal breeding facility (Liberty Laboratories, Waverly, N.Y., USA). All surgical and experimental procedures were conducted in accord with the US National Research Council's Guidelines for the Care and Use of Mammals in Neuroscience and Behavioral Research (2003) and the Canadian Council on Animal Care's Guide to the Care and Use of Experimental Animals (Olfert et al., 1993) and were
Evaluation of tracer deposits
Ten cats received deposits of WGA-HRP in order to expose axon terminals throughout all seven layers of the left superior colliculus. From the center of the deposit, the spread of the tracer was between 1.25 and 1.75 mm in the mediolateral plane and 1.5–2.0 mm in the anteroposterior plane. In all cases, the tracer spread throughout stratum griseum superficiale (SGS), stratum griseum intermediale (SGI) and stratum griseum profundum (SGP). Four of the ten cases had tracer spread into the
Summary
The present study investigated the origin of the corticotectal pathway from auditory cortex following injections of WGA-HRP made into the superficial and deep layers of the SC. Labeled corticotectal neurons were abundant in the infragranular layers of the hemisphere ipsilateral to the SC injection. Interestingly, the dominant projections to the superior colliculus from the auditory cortex emerged from ipsilateral and contralateral fAES. Few, if any, direct corticotectal inputs to the SC from
Conclusion
Our findings demonstrate that, unlike the visual areas involved in orienting the head and eyes to a visual stimulus which are known to have direct projections to the SC (Harting et al., 1992; Lomber and Payne, 2004), only one of four auditory cortical areas (fAES) involved with spatial acoustic processing projects directly to the superior colliculus. The reason for this meager connectivity between A1, DZ and PAF and the superior colliculus remains to be determined.
Contributors
All authors had full access to all data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: NC, JGM, SGL. Acquisition of data: NC, JGM, ELT. Analysis and interpretation of data: NC, JGM. Drafting of the manuscript: NC, JGM. Critical revision of the manuscript for important intellectual content AJH, SGL. Statistical analysis: NC. Obtained funding: SGL. Study supervision: SGL.
Acknowledgments
We would like to thank Pam Nixon for the assistance with animal care and Zachary J. Hall and Sam Yi for help with various phases of the project. This work was supported by grants from the Canadian Institutes of Health Research and the Natural Science and Engineering Research Council of Canada.
Glossary
- A
- Anterior
- AAF
- anterior auditory field
- aes
- anterior ectosylvian sulcus
- AEV
- anterior ectosylvian visual area
- A1
- primary auditory cortex
- A2
- second auditory cortex
- ca
- cerebral aqueduct
- cc
- corpus callosum
- CO
- cytochrome oxidase
- dPE
- dorsal posterior ectosylvian area
- D
- Dorsal
- DZ
- dorsal zone of auditory cortex
- fAES
- auditory field of the anterior ectosylvian sulcus
- HRP-DAB
- horseradish peroxidase-diaminobenzidine
- HRP-TMB
- horseradish peroxidase-tetramethyl benzidine
- IC
- inferior colliculus
- IN
- insular area
- iPE
- intermediate posterior
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