Visual cells in the inferior colliculus of the cat

Extracellular recordings from 91 cells of the pericentral nucleus (ICP) of the inferior colliculus of the cat revealed that 83 of them were responsive to auditory stimuli and the other 8 to visual stimuli. All visually driven cells were binocular and showed large receptive fields located in the contralateral hemifield. The best stimulus was either a spot or a bar moved in any direction across the receptive field. No directional selectivity was found. It is suggested that the visual input to the ICP participates in an integrated reflex-orienting behavior, in which the visual information is important for the localization of the sound source.     

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.     

Influence of auditory deprivation upon the tonopic organization in the inferior colliculus: a Fos immunocytochemical study in the rat

The frequency organization in the inferior colliculus of neonatally-deafened rats was investigated using electrical stimulation of the cochlea and immunoreactivity for Fos as a marker of neuronal activity. An electrode implanted either at the base or at the apex of the right cochlea delivered a unique 45-min stimulation at two different level intensities and at two time points, i.e. either at 4 weeks or at 4 months. In 4-week-old rats stimulated at 5x threshold, a site-for-site organization was observed since basal or apical stimulation induced a strong labelling in the ventro-medial or in the dorsolateral part of the left inferior colliculus, respectively. In 4-month-old rats, stimulation of the base induced an extremely weak Fos labelling without any specific location in the left inferior colliculus while stimulation of the apex induced a diffuse labelling with two discrete bands being distinguishable in the left inferior colliculus. In 4-week-old rats stimulated at 15x threshold, basal stimulation elicited a diffuse Fos-like immunoreactivity in the left inferior colliculus while apical stimulation yielded a response restricted to the dorsal part of the left inferior colliculus. In 4-month-old rats, no response was detected in the left inferior colliculus after stimulation of the basal part of the cochlea. Stimulation of the apex could still induce a labelling in the dorsolateral left inferior colliculus. Thus, the inferior colliculus exhibits an adult-like tonotopic organization early on independently of any acoustic stimulation. Prolonged absence of auditory input dramatically alters this organization in the inferior colliculus, especially for high frequencies. From a clinical standpoint, these results could argue for early implantation in deaf children.     

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.     

Frequency tuning properties of neurons in the inferior colliculus of an FM bat.

We examined frequency tuning characteristics of single neurons in the inferior colliculus of the echolocating bat, Eptesicus fuscus, in order to determine whether there are different classes of spectral selectivity at this level and to relate frequency tuning properties to the design of the echolocation signal. In unanesthetized but tranquilized animals, we recorded responses from 363 single units to pure tones, frequency-modulated (FM) sweeps, or broad-band noise. Most units were selective for stimulus type; 50% responded only to pure tones, 14% responded only to FM sweeps, and 5% responded only to noise. The remainder responded to two or more types of stimuli. Tuning curves could be classified as follows: 1) V-shaped tuning curves (57%) were the most common type; 2) closed tuning curves (20%) had thresholds at both low and high sound levels; 3) narrow filters (14%) had Q values above 20 at 10 dB and 30 dB above threshold or 10 dB and 40 dB above threshold; 4) frequency-opponent tuning (6%) was found in units with high spontaneous activity; within a center range of frequencies, firing rate increased above spontaneous level, but at higher or lower frequencies, firing rate decreased below spontaneous level; 5) double-tuned units (3%) had two best frequencies (BF). The most clear evidence of topographic distribution was seen for filter units, which were only found in the dorsal part of the 20-30 kHz isofrequency contour. Filter units were also the most clearly related to the echolocation signal of the bat. Their BFs were all within the range of the dominant frequency (approximately 20-30 kHz) that Eptesicus uses during the searching phase of echolocation.     

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.     

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.     

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.     

Development of tone response thresholds, latencies and tuning in the mouse inferior colliculus.

The development of tone response thresholds, latencies and tuning of neurons in the inferior colliculus (IC) of the mouse has been investigated between postnatal days 10 (first responses) and 20. As in adults, response thresholds of neurons are lowest in the center of the IC compared with other areas right from the beginning of responsiveness at day 10. Thresholds decrease rapidly until at days 16-20 (depending on the characteristic frequency of the neurons) adult levels are reached. Response latencies decrease rapidly to adult levels at days 16-18. Broad frequency tuning curves can be measured at days 10 and 11. From day 12 onwards, tuning curve shapes differentiate and adult diversity occurs which indicates presence of inhibition and summation in the pathway to or within the IC at that early age. The tip lengths of the tuning curves increase faster than the sharpness of the tips (Q10 dB values). The developmental courses of the measured parameters are expressed by power functions. The time constants of these functions are used in the discussion of processes underlying the functional maturation in the auditory system of the mouse. The general course of the development of all the here investigated response properties of single neurons in the IC, except tuning curve shape, appears to be determined by maturation at or peripheral to the cochlear level.     

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.     

Long-term regulation in calretinin staining in the rat inferior colliculus after unilateral auditory cortical ablation

In this study we analyzed the effects in the inferior colliculus of a unilateral ablation of the auditory cortex in rats. Variations in both calretinin immunoreactivity and protein levels determined by Western blot suggest that such lesions induce changes in the regulation of this calcium-binding protein. Stereological counts of calretinin-immunoreactive neurons in the inferior colliculus 15, 90, and 180 days after the lesion showed a progressive increase in the number of immunoreactive neurons, with a parallel increase in the intensity of staining. Two hundred forty days after the cortical lesion, both the number of immunoreactive neurons and the staining intensity had returned to control values. The effects of the cortical lesion on calretinin regulation are more intense in those inferior colliculus subdivisions more densely innervated by the corticocollicular projection. This finding, along with the time course of calretinin regulation suggests that degeneration of the descending projection is linked to calretinin regulation in the inferior colliculus. We hypothesize, based on the role of calretinin, that the observed increase in immunoreactivity levels seen in the inferior colliculus after lesioning of the auditory cortex may be related to altered excitability in deafferented neurons. Our finding, may reflect adaptive mechanisms to changes in calcium influx and excitability in inferior colliculus neurons induced by lesions of the descending projection from the cortex to the inferior colliculus.     

Effect of auditory cortex lesions on NADPH-diaphorase staining in the inferior colliculus of rat.

Projections from the auditory cortex (AC) in the rat terminate in the dorsal cortex (DC) and in the external cortex (EC) of the inferior colliculus (IC), areas which exhibit a moderate number of nicotinamide-adenine dinucleotide phosphate-diaphorase (NADPH-d) positive neurons. NADPH-d co-localizes with nitric oxide synthase, which is responsible for the production of the transcellular messenger, nitric oxide. Changes in NADPH-d staining in the IC were found after unilateral lesions of the AC. Lesions resulted in a reduction in NADPH-d staining in neurons and neuropil within the ipsilateral DC and EC with the maximum reduction occurring 3-4 days after lesion. The reduction in NADPH-d staining in the contralateral IC was less pronounced. Lesions affecting auditory areas Te 1 and Te 3 produced the largest decrease in NADPH-d staining in neurons and neuropil. This finding may be related to the abolition of the influence of glutamatergic corticocollicular and commissural pathways.     

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.     

Electrical stimulation of the inferior colliculus at low rates protects the cochlea from auditory desensitization

The effects of inferior collicular (IC) stimulation on cochlear responses were tested with pulsed electrical trains and with 1 min long continuous bursts. Pulsed trains did not cause any effects at the contralateral cochlea. However, a 1 min burst, containing pulses at low rates, was able to significantly reduce temporary threshold shifts (TTS) in cochlear sensitivity caused by a loud sound exposure. Intracochlear perfusion of hexamethonium blocked this effect. The time course of the hexamethonium blocking action paralleled its blocking action on the cochlear effects of electrical stimulation at the brainstem of an auditory efferent pathway, the crossed olivocochlear bundle (COCB). The protective IC effects were persistent and TTS reductions could be obtained even with a 5 min delay between IC stimulus and the loud sound. However, these persistent protective effects did not appear to occur at the cochlea. Finally, electrical stimulation at the IC ipsilateral to a cochlea exposed to loud sound also reduced TTS, but only by smaller amounts and at higher stimulation rates. Thus the IC appears to provide a strong descending influence that modulates the excitability levels of the olivocochlear nuclei in the brainstem. Both crossed and uncrossed OCB appear to be involved and able to reduce TTS. It is proposed that the protective effects may be due solely to the medial olivocochlear system and possibly only those fibres originating from one of the nuclei of the medial system.     

Role of commissural projections in the representation of bilateral auditory space in the barn owl's inferior colliculus

The central nucleus of the barn owl's inferior colliculus (ICc) contains a representation of both the ipsilateral and contralateral auditory hemifields. The representation of ipsilateral space is found in the "core" of the ICc, a subdivision defined by the terminal field of nucleus laminaris, the avian analogue of the medial superior olivary nucleus. The representation of contralateral space is found in the lateral portion of the "shell" of the ICc. The shell surrounds the core and is defined by the terminal field of the nucleus angularis, one of the cochlear nuclei. The representation of ipsilateral space in the core of the ICc may be accounted for by the crossed projection from the nucleus laminaris because most of the nucleus laminaris is devoted to a representation of contralateral space. We present evidence to suggest that the representation of contralateral space is due to a commissural projection from the core of one side to the lateral shell of the opposite side. Injection of horseradish peroxidase (HRP) into the lateral portion of the ICc shell produced retrogradely labeled somata in the core of the opposite side. Injection of tritiated proline into the core produced anterograde label confined to the lateral shell, thus confirming the observations made with HRP. Thus, for example, the left ICc core, which contains predominantly a representation of the left hemifield, innervates the right lateral shell, endowing it with a representation of the left, or contralateral hemifield. The representation of contralateral space in the lateral shell is ultimately conveyed to the external nucleus of the inferior colliculus where it contributes the horizontal axis to a two-dimensional map of space.     

A topographic representation of auditory space in the external nucleus of the inferior colliculus of the guinea-pig

The possibility that the external nucleus of the inferior colliculus (ICX) of the pigmented guinea-pig contains a map of auditory space has been investigated. Auditory stimuli consisted of broad-band sound delivered under free-field anechoic conditions from a range of positions around the animal's azimuthal axis. The responses of clusters of neurons in the ICX to threshold and to near-threshold stimuli displayed sharp spatial tuning. The responses recorded from rostral ICX revealed a preference for auditory stimuli in the anterior field while more caudal neurons preferentially responded to sounds presented in the posterior field. Neurons at intermediate points, along the rostro-caudal axis of the nucleus, displayed preferences for sound stimuli in appropriately intermediate field positions along the contralateral azimuthal axis. At higher stimulus intensities the spatial tuning of the responses decreased, but the optimal direction of preference was usually retained. The contribution of binaural processing to auditory spatial tuning was evident, since unilateral cochlea ablation destroyed the spatial tuning at higher stimulus intensities. The results presented provide the first evidence that a topographically ordered representation of the contralateral auditory azimuth is present in the ICX of a mammal.