Brain Research 881 (2000) 244–247
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Short communication
Projections from the rostral pole of the inferior colliculus to the cat
superior colliculus
*
John K. Harting , David P. Van Lieshout
Department of Anatomy, University of Wisconsin Medical School, Madison, WI 53706, USA
Accepted 15 August 2000
Abstract
The neuroanatomical data given here reveal a dense projection from the rostral pole of the cat inferior colliculus (rpIC) to the superior colliculus (SC). A portion of this pathway distributes in ‘patches’ across the ventral portion of the intermediate grey layer. These finding suggest that the rpIC input to the SC might play a role in determining the auditory receptive fields of SGI neurons and in the construction of the SC’s precise two dimensional map of auditory space. 2000 Elsevier Science B.V. All rights reserved.
Theme: Sensory systems
Topic: Auditory and visual systems
Keywords: Cat; Module; Patch; Sensorimotor integration
The mammalian superior colliculus plays an important pathway, the trigeminotectal [8,10,16]. This was accom-role in the integration of visual, somatosensory, and plished by injecting different anterograde tracers into the auditory information into purposeful motor responses rpIC (tritiated amino acids) and the contralateral spinal [14,15,26,27]. Much of this sensorimotor integration oc- trigeminal nucleus (biocytin) in the same animals. We curs within the modularly organized stratum griseum emphasize that all details regarding tracer, survival intermediale (SGI) [8–10]. As part of ongoing analyses of periods, and tissue processing are similar to what we have the spatial relationships of different SGI afferents, the described previously [8–10].
distribution of various auditory-related inputs are being Fig. 1A shows a Nissl-stained section in which the explored. In the current communication we present data location of the rpIC has been enclosed by a box. Fig. 1B that reveal a prominent and patchy input to the SGI from a shows the locations of retrogradely labeled cells within the little known and poorly understood region of the inferior rpIC following a unilateral injection of WGA-HRP into the colliculus called the rostral pole (or nucleus; rpIC). SC. The labeled rpIC cells form a well-circumscribed In one series of experiments, wheat germ agglutinin ‘pocket’ beneath the deep layers of the caudal SC (see also conjugated to horseradish peroxidase was injected unilater- level D of Fig. 3 in Ref. [7]). While the majority of labeled ally into the SC and the tissue then processed for the cells lie ipsilateral to the WGA-HRP injection, scattered location of auditory related SC-projecting neurons [21]. cells are also apparent within the contralateral rpIC. Since these experiments revealed many SC-projecting cells Fig. 1C shows the distribution of anterogradely trans-in the rpIC, a second group of experiments which trans-involved ported protein following an injection of labeled
3 3 3
injections of an equal mixture of [ H]proline and [ H]proline and [ H]leucine into the ipsilateral rpIC. In
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[ H]leucine into the rpIC [5] allowed us to analyze the this case the label was slightly more dense within the distribution of anterogradely transported protein within the caudal SC and absent from the rostral one fourth. The rpIC SC. In a final series of experiments the sublaminar location fibers distribute in dense patches across the most ventral of rpIC patches was compared to another well documented portion or tier of the SGI. The patches sometimes exhibit a columnar appearance, and many labeled axons may be seen coursing dorsally to distribute throughout the more *Corresponding author. Fax:11-608-262-7306.
E-mail address: jharting@facstaff.wisc.edu (J. K. Harting). dorsal tiers of the SGI. Fig. 1D clearly shows that these
246 J. K. Harting, D.P. Van Lieshout / Brain Research 881 (2000) 244 –247
dense patches of rplC-tectal label (black) lie ventral to the the BIC of the ferret, convey spatially sensitive infor-tier of trigeminotectal axons (red) that has been described mation to the SGI. One potential problem with this as ending in the middle tier of the SGI [8]. There are hypothesis is that rpIC projections to rostral pole of the SC several dense foci of label in the deeper layers of the SC, have not been observed in the current experiments. Studies particularly in the lateral SGP and SAI. Some of these are currently underway to explore the response properties dense zones underlie the regularly spaced patches of label of rpIC cells, the presence or absence of topographic order in the ventralmost SGI and, in fact, sometimes the two sets in the rpIC-tectal projection, and the extent to which the of patches appear to be continuous. pathway distributes to the entire SC.
The current findings are novel in that they reveal the The present findings strengthen the concept that the cat presence of an extensive projection to the SC from a SGI is functionally dependent upon connections that relatively poorly studied region of the auditory midbrain exhibit a modular organization (see Ref. [9] for review). (rpIC). The dense, patchy projection demonstrated in these Moreover, without also labeling the trigeminotectal tract in experiments appears to be more substantial than other the same experiments, we would not have been able to auditory brain stem inputs previously observed using precisely localize the densest patches to the ventral tier of anterograde transport methods [1,2,4,6,7,12,17–19,22]. the SGI. The finding that rpIC-tectal axons / terminals Since the rpIC receives direct projections from the dorsal distribute in distinct patches within the SGI supports cochlear nucleus [23], as well as projections from the physiological data in the cat showing that acoustically medial and lateral superior olives (MSO, LSO) [11,25], the sensitive cells occur in patches within the SGI [13]. Like rpIC input to the SGI could underlie many of the auditory the rpIC projection, patchy projections from the auditory latencies and receptive fields properties of SGI neurons portion of the anterior ectosylvian sulcus (AES) [3,20], the (average of 12.9 ms) [13]. substantia nigra pars reticulata [8], and the medial division The rpIC inputs from the LSO and MSO are topographi- of the frontal eye fields [9] distribute across the ventral tier cally organized and convey frequency specific information of the SGI. It would be interesting to determine if the to different parts of the rpIC [11,25]. While we have not as patchy descending input from the AES overlaps the yet examined the rpIC-tectal projection for topographic ascending rpIC input. It has been shown that descending order, physiological data have shown that frequency is not somatosensory cortical fibers from the AES overlap with mapped within the SGI [13]. However, a neural map of ascending fibers from the spinal trigeminal nucleus in auditory space has been found across the SGI, and it might patches across the middle tier of the SGI, and that these be that cells in the rpIC integrate ascending binaural somatosensory zones are spatially associated with tectospi-information and in turn convey space specific signals to the nal (TS) neurons [10]. Moreover, the
somatosensory-re-SGI [22]. lated cortical fibers end upon the proximal dendrites of
Little is known regarding the circuitry underlying the these TS neurons while the brain stem trigeminal inputs establishment of the two-dimensional map of auditory synapse upon more distal locations [10]. We are currently space within the SGI. None of the previously described exploring whether this same pattern of inputs is true for brain stem input to the SC would appear to give rise to a ascending and descending auditory pathways and thus projection that could account for the extensive distribution might represent a general ultrastructural feature of SGI of auditory responsive cells within the SGI. Data from organization.
studies in the ferret [17,24] indicate that the major brain stem auditory projection to the SGI arises from cells in the
nucleus of the brachium of the inferior colliculus (BIC) Acknowledgements and that such cells are selective for sound azimuth and
elevation. However, since only information regarding Supported by Grants IBN-9904770 and DC03693-01A2. azimuth appears to be conveyed to the SGI in a
topog-raphically organized manner [23], it has been suggested
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