Evaluation of auditory evoked potentials from the inferior colliculus in rat

This study aimed to investigate the usefulness of auditory evoked potentials (AEPs) in rats. To this end, N1, P2 latencies, and the N1-P2 amplitude of responses to different acoustic stimuli from rats, which were implanted with permanent electrodes in the inferior colliculus (IC), were evaluated and used to demonstrate the frequency characteristics of IC region. Permanent electrodes were implanted in IC regions of 7 male albino rats by the stereotaxic method. The animals were exposed to five tones series of stimuli (1000 Hz, 2000 Hz, 4000 Hz, 6000 Hz, and 8000 Hz tones with 1500 ms interstimulus intervals) of 70 dB with a duration of 1000 ms. AEPs) were recorded and analyzed with the Brain-Data Acquisition system. There were no statistically significant differences in N1, P2 latencies, and the N1-P2 amplitude of AEPs from IC regions of rats as a result of changes in the frequency of stimulus. It was determined that the dominant frequency activity of the IC to acoustic stimulus was theta-alpha band, with theta as the peak frequency.     

Representation of the cochlea within the inferior colliculus of the cat

The representation of the cochlear partition within the 3 dimensions of the inferior colliculus of the cat was studied by determining the best frequency of neurons isolated in series of parallel electrode penetrations. Cats were anesthetized with sodium pentobarbital. There was a systematic representation of the cochlea within the pericentral nucleus of the inferior colliculus. The boundary between the pericentral nucleus and underlying central nucleus could be sharply drawn on physiological bases. There was a highly ordered representation of the cochlea across the 3 dimensions of the central nucleus. Neurons within the dorsomedial nucleus and external nucleus of the inferior colliculus were not driven by simple tonal stimulation. The change in best frequency as a function of depth in the colliculus was the same for parallel penetrations entering over almost the entire dorsal surface of the central nucleus. This indicated that a given frequency-band was represented across a laminar figure completely sectioning the nucleus; and that laminae were flat except along the extreme margins of the nucleus. Definition of ‘isofrequency contours’ from reconstruction of rows of parallel penetrations confirmed these conclusions. Frequency-band laminae were tilted down rostrally, especially in the middle and lateral aspects of the central nucleus. They were also tilted down laterally. Orientation of isofrequency contours paralleled that of laminae described within anatomical studies of the central nucleus²⁹. The disk-shaped regions representing lowest frequency octaves were not as thick nor as extensive as those representing middle and high frequency octaves. However, when best frequency values were converted to corresponding cochlear place, cochlear place was observed to be a nearly linear function of colliculus depth for the representation of the apical half of the cochlear partition. There was a somewhat larger representation, across colliculus depth, of the basal half of the cochlea. The change in best frequency with change of depth in the central nucleus was stepwise. This suggested that small sectors of the basilar membrane of approximately equal length were represented across individual anatomically defined cellular laminae within the nucleus.     

The inferior colliculus encodes the Franssen auditory spatial illusion

Illusions are effective tools for the study of the neural mechanisms underlying perception because neural responses can be correlated to the physical properties of stimuli and the subject's perceptions. The Franssen illusion (FI) is an auditory spatial illusion evoked by presenting a transient, abrupt tone and a slowly rising, sustained tone of the same frequency simultaneously on opposite sides of the subject. Perception of the FI consists of hearing a single sound, the sustained tone, on the side that the transient was presented. Both subcortical and cortical mechanisms for the FI have been proposed, but, to date, there is no direct evidence for either. The data show that humans and rhesus monkeys perceive the FI similarly. Recordings were taken from single units of the inferior colliculus in the monkey while they indicated the perceived location of sound sources with their gaze. The results show that the transient component of the Franssen stimulus, with a shorter first spike latency and higher discharge rate than the sustained tone, encodes the perception of sound location. Furthermore, the persistent erroneous perception of the sustained stimulus location is due to continued excitation of the same neurons, first activated by the transient, by the sustained stimulus without location information. These results demonstrate for the first time, on a trial‐by‐trial basis, a correlation between perception of an auditory spatial illusion and a subcortical physiological substrate.     

Topography of projections from the auditory cortex to the inferior colliculus in the rat

We examined the organization of descending projections from auditory and adjacent cortical areas to the inferior colliculus (IC) in the rat by using the retrograde and anterograde transport of wheat germ agglutinin-horseradish peroxidase. Small tracer injections were placed into cytologically defined subnuclei of the IC. On the basis of the resulting pattern of retrogradely labeled neurons in the cortex, different cortical areas and fields were defined. Two secondary areas located ventrocaudally (Te2) and ventrally (Te3) to the primary auditory area (Te1) were delineated. The primary auditory area was subdivided into a posterior (Te1.p), a medial (Te1.m), and an anterior (Te1.a) auditory field. In addition, we outlined an area located rostrally to the auditory areas comprising a part of the secondary somatosensory cortex, as well as a dorsal belt surrounding dorsally the auditory areas. The following basic patterns of corticocollicular projections are revealed: 1) layers 2 and 3 of the dorsal cortex of the IC (DC2, DC3) are differentially innervated by the primary auditory fields (Te1.p and Te1.a project bilaterally to DC2, while Te1.m projects bilaterally and in topographical order to DC3); cells in Te1.m, arranged in caudal to rostral sequence, project to corresponding loci in DC3 arranged from dorsolateral to ventromedial; 2) the fibrocellular capsule of the IC, comprising layer 1 of the dorsal and external cortex of the IC, receives input from the secondary auditory area Te2; 3) layers 2 and 3 of the external cortex of the IC are only weakly innervated by the primary and secondary auditory cortex; 4) the intercollicular zone receives its major input from the secondary auditory area Te3, the secondary somatosensory cortex, and the dorsal belt; and 5) finally, the central nucleus of the IC receives no input from the temporal cortex at all. Our results demonstrate that the corticocollicular projections are highly organized. These pathways may modulate auditory processing in different functional circuits of the inferior colliculus.     

Visual deprivation modifies auditory directional tuning in the inferior colliculus

The aim of this study was to assess whether early visual deprivation could modulate the auditory directional tunings of single neurons in the central nucleus of the inferior colliculus of the rat. Extracellular recordings were carried out in normal and early bilaterally enucleated rats. Direction-specific auditory neurons were found in both groups, and no evidence was found for a topographical order of best azimuthal direction. Although the distribution of best azimuthal direction was unaltered in enucleated rats, our data suggest that early visual deprivation modifies the width of auditory directional receptive fields in the central nucleus of the inferior colliculus. This suggests that visual input plays a substantial role in refining auditory receptive fields in the inferior colliculus.     

Topography of descending projections from the inferior colliculus to auditory brainstem nuclei in the rat

We examined the organization of descending projections from the inferior colliculus (IC) to auditory brainstem nuclei and to pontine and reticular nuclei in the rat by employing the anterograde axonal tracer Phaseolus vulgaris-leucoagglutinin (PHA-L). Small PHA-L injections into cytologically defined subnuclei of the IC revealed that each subnucleus has a unique pattern of efferent projections. The central nucleus of the IC projects in a topographic order to the dorsal nucleus of the lateral lemniscus (DLL), the rostral periolivary nucleus (RPO), the ventral nucleus of the trapezoid body (VNTB), and the dorsal cochlear nucleus (DCN). It is assumed that this topography represents a cochleotopic arrangement. The external cortex of the IC projects to the nucleus sagulum (Sag), the RPO, the VNTB, and the DCN. Minor projections were found to pontine and reticular nuclei. Efferent fibers from the dorsal cortex of the IC terminate mainly in the Sag, while other nuclei of the auditory and extra-auditory brainstem receive only minor projections. The intercollicular zone sends a moderate number of fibers to the DLL and very few, if any, to the remaining auditory brainstem nuclei. In contrast, fairly strong projections from the intercollicular zone to the reticular formation were found. The present data demonstrate that the four subnuclei of the IC have a differential pattern of descending projections to nuclei in the pontine and medullary brainstem. These parallel colliculofugal pathways, assumed to belong to functionally separate circuits, may modulate auditory processing at different levels of the auditory neuraxis. © 1993 Wiley-Liss, Inc.     

Descending projections from the auditory cortex to the inferior colliculus in the gerbil, Meriones unguiculatus

Corticofugal projections to the auditory midbrain, the inferior colliculus (IC), influence the way in which specific sets of IC neurons process acoustic signals. We used retrograde tracer (Fluorogold, Fluororuby, microbeads) injections in the IC to study the morphology and location of cortico-collicular projecting neurons and anterograde tracer (dextran biotin) injections in auditory cortical fields to describe the distribution of terminals in the IC. Nissl staining, cytochrome oxidase activity, and neurofilament SMI32 immunostaining were used to delimit the different auditory areas. We defined a primary or "core" auditory cortex and a secondary "caudal" auditory area containing layer V pyramidal neurons that project to the IC. These projections target the central nucleus of the IC (CNIC) ipsilaterally and the IC cortices bilaterally, with the ipsilateral component predominant. Other secondary auditory areas, dorsal and ventral to the core, do not directly participate in this projection. The ventral secondary cortex targets midbrain periaqueductal gray. The projection from the core cortex originates from two classes of layer V pyramidal cells. Cells presenting a tufted apical dendrite in layer I have dense terminal fields in the IC cortices. Pyramids lacking layer I dendritic tufts target the CNIC in a less dense but tonotopic manner. The caudal cortex projection originates from smaller layer V pyramids and targets the IC cortices with dense terminal fields. Descending auditory inputs from the core and caudal areas converge in the dorsal and external cortices of the IC. Descending connections to the gerbil IC form a segregated system in which multiple descending channels originating from different neuronal subpopulations may modulate specific aspects of ascending auditory information.     

The subparafascicular thalamic nucleus of the rat receives projection fibers from the inferior colliculus and auditory cortex

The sources of afferent fibers to the subparafascicular thalamic nucleus (SPF) of the rat were investigated by the retrograde WGA-HRP and anterograde PHA-L methods. Layer V of the areas 3, 1 and 2 of the temporal cortex as well as the dorsal and external cortices of the inferior colliculus were found to send projection fibers to the whole rostrocaudal extent of the SPF bilaterally with a clear-cut ipsilateral dominance. The results indicate that the SPF of the rat may constitute a relay nucleus in the central auditory pathways.     

Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections

To ascertain whether the auditory neocortex also innervates the central nucleus of the inferior colliculus (CNIC) and not only its dorsal (DCIC) and external (ECIC) cortices, the anterograde tracers Phaseolus vulgaris-leucoagglutinin (PHA-L) and biotinylated dextran (BD) were injected into the primary auditory neocortex of albino rats (Te1), and labeled corticocollicular fibers were studied via light and electron microscopy. Axons from discrete regions of Te1 form two rostrocaudally oriented laminar plexuses of terminal fibers in the ipsilateral inferior colliculus (IC) and one in the contralateral IC. The first ipsilateral plexus, located in the medial half of the IC, has a dorsomedial to ventrolateral orientation, parallel to the isofrequency planes of the IC; is continuous through the CNIC and DCIC; and extends into the rostral ECIC. The second plexus is located in the deep layers of the lateral ECIC. These two plexuses meet caudally and ventrally, at the border between the CNIC and the lateral ECIC. The plexus in the contralateral IC is less dense and shorter than the two ipsilateral plexuses and is symmetric to the medial plexus. The thickness of the three plexuses is correlated with the size of the injection site, and their mediolateral and dorsoventral positions change as the injection site in Te1 is displaced rostrocaudally, with more caudal injections resulting in more dorsolateral medial plexuses and more dorsomedial lateral plexuses. Furthermore, the ventromedial border of the IC receives nontopographic, convergent projections from wide regions of rostral portions of Te1. The distribution of these corticocollicular plexuses mimics the topography of previously described intracollicular fibers. Electron microscopy shows that, in all three subdivisions of the ipsilateral IC, corticocollicular fibers form small boutons with features generally associated with excitatory transmission; i.e., they contain round synaptic vesicles and form asymmetric synapses with thin dendritic shafts and spines. These results demonstrate that the auditory corticocollicular projections innervate more extensive regions of the IC than were previously observed. Although peripheral regions receive the densest projection, the entire IC appears to be the target of corticofugal input. © 1996 Wiley-Liss, Inc.     

Binaural acoustic stimulation exercises protective effects at the cochlea that mimic the effects of electrical stimulation of an auditory efferent pathway

Low-level acoustic stimulation of one (contralateral) ear reduced the neural desensitization caused by a simultaneous loud sound exposure in the other (ipsilateral) ear in a loss-related manner. Greatest reductions in the temporary threshold shifts (TTS) in the exposed ear were obtained when the exposure would have caused large amounts of TTS. Low-level exposures (reduced intensity or duration of exposure) which caused low levels of TTS, from which the cochlea could recover relatively quickly, were not affected by the contralateral stimulus. Intermediate levels of TTS showed intermediate levels of reduction for the same contralateral acoustic stimulus. These effects were similar to effects previously demonstrated with electrical stimulation of an efferent pathway to the cochlea, the crossed olivocochlear bundle (COCB); lesioning the COCB prevented the contralateral stimulus from having any effect on TTS due to an ipsilateral exposure. Like COCB stimulation, the contralateral acoustic stimulus had tonic effects, so that reductions in ipsilateral TTS could be obtained even when the contralateral stimulus was presented 5 min before the ipsilateral exposure. With 10 min delay no effect on TTS occurred. The contralateral stimulus did not appear to cause any changes in responses in the ipsilateral cochlea prior to the loud sound exposure. These results are discussed as indicating an interaction between the two inputs at a central locus, leading to activation of the COCB fibres to the cochlea exposed to the loud sound.     

Attention modulates sound processing in human auditory cortex but not the inferior colliculus

Auditory attention powerfully influences perception and modulates sound processing in auditory cortex, but the extent of attentional modulation in the subcortical auditory pathway remains poorly understood. We examined the effects of intermodal attention using functional magnetic resonance imaging of the inferior colliculus and auditory cortex in a demanding intermodal selective attention task using a silent imaging paradigm designed to optimize inferior colliculus activations. Both the inferior colliculus and auditory cortex showed strong activations to sound, but attentional modulations were restricted to auditory cortex.     

Projections from the rostral pole of the inferior colliculus to the cat superior colliculus

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.     

Topographic projection from the optic tectum to the auditory space map in the inferior colliculus of the barn owl

In the barn owl (Tyto alba), the external nucleus of the inferior colliculus (ICX) contains a map of auditory space that is calibrated by visual experience. The source of the visually based instructive signal to the ICX is unknown. Injections of biotinylated dextran amine and Fluoro-Gold in the ICX retrogradely labelled neurons in layers 8-15 of the ipsilateral optic tectum (OT) that could carry this instructive signal. This projection was point-to-point and in register with the feed-forward, auditory projection from the ICX to the OT. Most labelled neurons were in layers 10-11, and most were bipolar. Tripolar, multipolar, and unipolar neurons were also observed. Multipolar neurons had dendrites that were oriented parallel to the tectal laminae. In contrast, most labelled bipolar and tripolar neurons had dendrites oriented perpendicular to the tectal laminae, extending superficially into the retino-recipient laminae and deep into the auditory recipient laminae. Therefore, these neurons were positioned to receive both visual and auditory information from particular locations in space. Biocytin injected into the superficial layers of the OT labelled bouton-laden axons in the ICX. These axons were generally finer than, but had similar bouton densities as, feed-forward auditory fibers in the ICX, labelled by injections of biocytin into the central nucleus of the inferior colliculus (ICC). These data demonstrate a point-to-point projection from the OT to the ICX that could provide a spatial template for calibrating the auditory space map in the ICX.     

Ascending auditory projections to the inferior colliculus in the adult gerbil, Meriones unguiculatus

Ascending auditory projections to the inferior colliculus (IC) of the adult gerbil were studied using the retrograde transport of horseradish peroxidase. Our results indicate that in gerbils, the IC receives afferent projections from most brainstem auditory nuclei. A strong contralateral projection originates in the cochlear nuclear complex (CN). A smaller but consistent projection from all three divisions of ipsilateral CN is also present. The medial superior olive (MSO), superior parolivary nucleus, and ventral nucleus of the lateral lemniscus all maintain ipsilateral projections to the IC. Bilateral projections arise from the lateral superior olive, lateral nucleus of the trapezoid body, and dorsal nucleus of the lateral lemniscus. Previous investigations in other mammalian species provide conflicting data concerning the magnitude of a direct ipsilateral projection from CN to the IC. Our quantitative data indicate that the ipsilateral projection from CN in the gerbil is nearly one third as large as the projection from ipsilateral MSO. The projection from contralateral CN is six times larger than the MSO projection. The distribution of labeled cells across the rostrocaudal extent of MSO and the three divisions of the cochlear nuclear complex are presented.     

Evoked potentials from the inferior colliculus in man

Sound-evoked potentials were recorded from the inferior colliculus in man when it was exposed during surgery. The earliest response to contralateral stimulation with 2000 Hz tone bursts at 90 dB was a positive deflection with a latency of about 6.5 msec that was followed by a slow, negative deflection that lasted about 5 msec. It is supposed that this surface-positive peak originates in the lateral lemniscus. Its latency matched that of the fifth vertex-positive wave (V) of the BSEP recorded from the scalp. Superimposed on the slow potential were several peaks. These peaks emerged clearly after the slow components were removed by filtering. The peaks then were shown to have latencies that matched the latencies of peaks VI, VII and VIII of the scalp-recorded BSEP.     

Topographical projection from the superior colliculus to the nucleus of the brachium of the inferior colliculus in the ferret: convergence of visual and auditory information

The normal maturation of the auditory space map in the deeper layers of the ferret superior colliculus (SC) depends on signals provided by the superficial visual layers, but it is unknown where or how these signals influence the developing auditory responses. Here we report that tracer injections in the superficial layers label axons with en passant and terminal boutons, both in the deeper layers of the SC and in their primary source of auditory input, the nucleus of the brachium of the inferior colliculus (nBIC). Electron microscopy confirmed that biocytin-labelled SC axons form axodendritic synapses on nBIC neurons. Injections of biotinylated dextran amine in the nBIC resulted in anterograde labelling in the deeper layers of the SC, as well as retrogradely labelled superficial and deep SC neurons, whose distribution varied systematically with the rostrocaudal placement of the injection sites in the nBIC. Topographical order in the projection from the SC to the ipsilateral nBIC was confirmed using fluorescent microspheres. We demonstrated the existence of functional SC-nBIC connections by making whole-cell current-clamp recordings from young ferret slices. Both monosynaptic and polysynaptic EPSPs were generated by electrical stimulation of either the superficial or deep SC layers. In addition to unimodal auditory units, both visual and bimodal visual-auditory units were recorded in the nBIC in vivo and their incidence was higher in juvenile ferrets than in adults. The SC-nBIC circuit provides a potential means by which visual and other sensory or premotor signals may be delivered to the nBIC to calibrate the representation of auditory space.     

Responses from two ifring patterns in inferior colliculus neurons to stimulation of the lateral lemniscus dorsal nucleus

Theγ-aminobutyric acid neurons (GABAergic neurons) in the inferior colliculus are classiifed into various patterns based on their intrin-sic electrical properties to a constant current injection. Although this classiifcation is associated with physiological function, the exact role for neurons with various ifring patterns in acoustic processing remains poorly understood. In the present study, we analyzed characteristics of inferior colliculus neuronsin vitro, and recorded responses to stimulation of the dorsal nucleus of the lateral lemniscus using the whole-cell patch clamp technique. Seven inferior colliculus neurons were tested and were classiifed into two ifring patterns: sustained-regular (n = 4) and sustained-adapting ifring patterns (n = 3). The majority of inferior colliculus neurons exhibited slight changes in response to stimulation and bicuculline. The responses of one neuron with a sustained-adapting ifring pattern were suppressed after stimulation, but recovered to normal levels following application of theγ-aminobutyric acid receptor antagonist. One neuron with a sustained-regular pattern showed suppressed stimulation responses, which were not affected by bicuculline. Results suggest that GABAergic neurons in the inferior colliculus exhibit sustained-regular or sustained-adapting ifring patterns. Additionally, GABAergic projections from the dorsal nu-cleus of the lateral lemniscus to the inferior colliculus are associated with sound localization. The different neuronal responses of various ifring patterns suggest a role in sound localization. A better understanding of these mechanisms and functions will provide better clinical treatment paradigms for hearing deifciencies.